« December 2007 | Main | February 2008 »

Two New Papers on Polyfunctional T cell Responses

Two new papers add to the literature demonstrating that the presence of polyfunctional HIV-specific T cell responses correlates with low viral load in HIV infection. In one paper, in the European Journal of Immunology, Rick Koup and colleagues report that virus-specific CD4 and CD8 T cells capable of multiple functions (involving various combinations of IL-2, TNF alpha, interferon gamma and MIP-1 beta production and expression of CD107a, a marker indicating cell-killing ability) are far more frequently detectable in HIV-2 than HIV-1 infection. The study also confirms prior reports that such polyfunctional T cells make 15-20 times more interferon gamma and TNF alpha on a per-cell basis than monofunctional T cells. The authors note that the data do not prove a causative role of the T cell responses in controlling viral load and preventing or slowing disease progression in HIV-2-infected individuals, but cite evidence from other recent studies - including Robert Seder's murine Leishmania vaccine work - as suggesting that polyfunctional T cells do contribute to control of pathogens and are thus unlikely to have arisen simply as a consequence of low viral load in HIV-2 infection.

In a second paper - just published online in J. Virology by Marybeth Daucher from Daniel Douek's laboratory at NIAID - polyfunctional CD8 T cell responses targeting HIV-1 are reported to be associated with maintenance of low viral loads subsequent to antiretroviral therapy interruption. The study only involves six individuals so the authors are appropriately cautious in interpreting the data, but they emphasize that other parameters such as the magnitude and breadth of the HIV-specific CD8 T cell response showed no correlations with post-interruption outcomes.  In summing up their work, the researchers state: "Despite the small number of patients and the inherent issues associated with the interpretation of observational studies in humans, these data suggest that functional attributes of the HIV-specific CD8 T-cell response might be important correlates of virological outcome after exposure to SIT regimens and could represent useful biological parameters to measure in the clinical context."

European Journal of Immunology
Volume 38, Issue 2 , Pages 350 - 363
Published Online: 17 Jan 2008

Polyfunctional T cell responses are a hallmark of HIV-2 infection (free access to full text)

Melody G. Duvall 1 2, Melissa L. Precopio 2, David A. Ambrozak 2, Assan Jaye 4, Andrew J. McMichael 1, Hilton C. Whittle 4, Mario Roederer 3, Sarah L. Rowland-Jones 1 4, Richard A. Koup, Dr. 2

1MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, University of Oxford, Oxford, UK
2Immunology Laboratory, Vaccine Research Center, NIAID, National Institutes of Health, Bethesda, MD, USA
3Immuno Technology Section, Vaccine Research Center, NIAID, National Institutes of Health, Bethesda, MD, USA
4MRC Laboratories Fajara, Banjul, The Gambia, West Africa

Funded by:
National Institutes of Health, USA
Medical Research Council, UK

Abstract

HIV-2 is distinguished clinically and immunologically from HIV-1 infection by delayed disease progression and maintenance of HIV-specific CD4+ T cell help in most infected subjects. Thus, HIV-2 provides a unique natural human model in which to investigate correlates of immune protection against HIV disease progression. Here, we report a detailed assessment of the HIV-2-specific CD4+ and CD8+ T cell response compared to HIV-1, using polychromatic flow cytometry to assess the quality of the HIV-specific T cell response by measuring IFN-, IL-2, TNF-, MIP-1, and CD107a mobilization (degranulation) simultaneously following Gag peptide stimulation. We find that HIV-2-specific CD4+ and CD8+ T cells are more polyfunctional that those specific for HIV-1 and that polyfunctional HIV-2-specific T cells produce more IFN- and TNF- on a per-cell basis than monofunctional T cells. Polyfunctional HIV-2-specific CD4+ T cells were generally more differentiated and expressed CD57, while there was no association between function and phenotype in the CD8+ T cell fraction. Polyfunctional HIV-specific T cell responses are a hallmark of non-progressive HIV-2 infection and may be related to good clinical outcome in this setting.

JVI Accepts, published online ahead of print on 30 January 2008

J. Virol. doi:10.1128/JVI.02212-07

Virological Outcome After Structured Interruption of Antiretroviral Therapy For HIV Infection is Associated with the Functional Profile of Virus-Specific CD8+ T-Cells

Marybeth Daucher*, David A Price, Jason M Brenchley, Laurie Lamoreaux, Julia A Metcalf, Catherine Rehm, Elizabeth Nies-Kraske, Elizabeth Urban, Christian Yoder, Diane Rock, Julie Gumkowski, Michael R Betts, Mark R Dybul, and Daniel C Douek

Laboratory of Immunoregulation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892; Graduate Genetics Program, George Washington University, Washington, DC 20522; Human Immunology Section, and Immunology Laboratory, Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892; Department of Medical Biochemistry and Immunology, University of Cardiff, Heath Park, Cardiff CF14 4XN, UK; Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104; Office of the U.S. Global AIDS Coordinator, U.S. Department of State, Washington, DC 20522

A clear understanding of the antiviral effects of CD8+ T-cells in the context of chronic HIV infection is critical for the development of prophylactic vaccines and therapeutics designed to support T-cell-mediated immunity. However, defining the potential correlates of effective CD8+ T-cell immunity has proven difficult; notably, comprehensive analyses have demonstrated that the size and shape of the CD8+ T-cell response is not necessarily indicative of efficacy determined by measures of plasma viral load. Here, we conducted a detailed quantitative and qualitative analysis of CD8+ T-cell responses to autologous virus in a cohort of six HIV-infected individuals with a history of structured interruption of antiretroviral therapy (SIT). The magnitude and breadth of the HIV-specific response did not, by itself, explain the changes observed in plasma virus levels after cessation of ART. Furthermore, mutational escape from targeted epitopes could not account for the differential virological outcomes in this cohort. However, the functionality of HIV-specific CD8+ T-cell populations upon antigen encounter, determined by the simultaneous and independent measurement of five CD8+ T-cell functions (degranulation, IFN{gamma}, MIP1{beta}, TNF{alpha} and IL2) reflected the emergent level of plasma virus with multiple functions being elicited in those individuals with lower viremia after SIT. These data show that the quality of the HIV-specific CD8+ T-cell response, rather than the quantity, is associated with the dynamics of viral replication in the absence of ART and suggest that the effects of SIT can be assessed by measuring the functional profile of HIV-specific CD8+ T-cells.

The Fate of Virus-Infected Cells in Natural Hosts of SIV

The extent and importance of direct, HIV-mediated killing of CD4 T cells in AIDS pathogenesis has long been a subject of contentious debate. Many early pathogenesis theories were based on the reasonable assumption that there was a direct connection between the virus-induced CD4 T cell death observed in lab dishes and the decline of peripheral blood CD4 T cell counts in people with HIV infection. In one famous formulation, HIV was portrayed as Pac Man, vigorously gobbling up CD4 T cells until they were gone. However, over time – and particularly over recent years – the role of virus-induced immune activation in indirectly depleting CD4 T cells (and draining other important immune system reserves such as naïve CD8 T cells) has come to prominence as new data has been published and presented. Two new papers in J. Virology underscore this shift in the understanding of AIDS pathogenesis by reporting data on the dynamics of SIV-infected CD4 T cells in two different monkey species in which SIV is typically benign: sooty mangabeys and African green monkeys (AGMs).

The researchers (one group led by Shari Gordon, the other by Ivona Pandrea, with considerable overlap between the two) set out to address whether SIV-infected CD4 T cells live longer in these monkey species, potentially explaining the absence of virus-induced disease. In both studies, antiretroviral therapy (emitricitabine and tenofovir) was administered and SIV viral load measured very frequently in order to establish the decay of the infected cell population. The results echo those reported for humans and SIV-infected rhesus macaques: there was a rapid initial phase of viral load decline (albeit with a blip on day 2 in the AGMs) with the vast majority of infected cells (>90%) disappearing in a week. Accordingly, mathematical modeling showed the vast majority of infected cells had a very short half-life of ~1.1 days in sooty mangabeys and ~9.5 hours in AGMs. In most mangabeys, a second phase decay involving cells with a longer half-life (~15 days) was also observed but in AGMs the rapid decline of viral load to undetectable levels (<100 copies) meant that no second phase decay was measurable.

Interestingly, in both monkey species, viral load rebounded after ART and settled at a steady state setpoint in a manner akin to that seen in HIV infection (although the setpoint SIV viral load levels were much higher). The establishment of the post-ART setpoint was associated with a significant increase in CD4 and CD8 T cell proliferation in both studies, which may offer support for Amitinder Kaur’s longstanding contention that SIV-specific immune responses do exert some control over SIV replication in non-pathogenic infections.

In discussing the broader implications of their work, the authors note that it establishes there are no significant differences in the death rates of infected cells in non-pathogenic vs. pathogenic SIV infections, presenting a stern challenge to the notion that the cytopathic effects of the virus play a key role in the development of disease. They also emphasize that their findings buttress the view that it is not viral replication per se that is important in driving pathogenesis, but the way the host copes with the virus.

JVI Accepts, published online ahead of print on 23 January 2008

J. Virol. doi:10.1128/JVI.02408-07

Short-lived infected cells support virus replication in naturally SIV-infected sooty mangabeys: implications for AIDS pathogenesis

Shari N. Gordon, Richard M. Dunham, Jessica C. Engram, Jacob Estes, Zichun Wang, Nichole R. Klatt, Mirko Paiardini, Ivona V. Pandrea, Cristian Apetrei, Donald L. Sodora, Ha Youn Lee, Ashley T. Haase, Michael D. Miller, Amitinder Kaur, Silvija I. Staprans, Alan S. Perelson, Mark. B. Feinberg, and Guido Silvestri*

Department of Pathology, University of Pennsylvania, Philadelphia, PA; Emory Vaccine Center and Yerkes National Primate Research Center, Atlanta, GA; Department of Microbiology, University of Minnesota, Minneapolis, MN; New England Primate Research Center, Harvard Medical School, Southborough, MA; Tulane National Primate Research Center, Covington, LA; Seattle Biomedical Research Institute, Seattle, WA; Los Alamos National Laboratory, Los Alamos, NM; University of Rochester, Rochester, NY; Gilead Sciences, Inc., Foster City, CA; Merck Vaccine Division, Merck & Co., Inc. West Point, PA

Abstract

Naturally SIV-infected sooty mangabeys (SMs) do not develop AIDS despite high levels of virus replication. At present, the mechanisms underlying this disease-resistance are poorly understood. Here we tested the hypothesis that SIV-infected SMs avoid immunodeficiency as a result of virus replication occurring in infected cells that live significantly longer than HIV-infected human cells. To this end, we treated six SIV-infected SMs with potent antiretroviral therapy (ART) and longitudinally measured the decline in plasma viremia. We applied the same mathematical models used in HIV-infected individuals, and observed that naturally SIV-infected SMs also present a two-phase decay of viremia following ART, with the bulk (92-99%) of virus replication sustained by short-lived cells (average lifespan 1.06 days) and only 1-8% occurring in longer-lived cells. In addition, we observed that ART had a limited impact on CD4+ T cells and the prevailing level of T cell activation and proliferation in SIV-infected SMs. Collectively, these results suggest that in SIV-infected SMs, similar to HIV-1-infected humans, short-lived activated CD4+ T cells, rather than macrophages, are the main source of virus production. These findings indicate that a short in vivo lifespan of infected cells is a common feature of both pathogenic and non-pathogenic primate lentivirus infections, and support a model for AIDS pathogenesis whereby the direct killing of infected cells by HIV is not the main determinant of disease progression.

JVI Accepts, published online ahead of print on 23 January 2008

J. Virol. doi:10.1128/JVI.02402-07

SIVagm Dynamics in African Green Monkeys

Ivona Pandrea*, Ruy M. Ribeiro, Rajeev Gautam, Thaidra Gaufin, Melissa Pattison, Mary Barnes, Christopher Monjure, Crystal Stoulig, Jason Dufour, Wayne Cyprian, Guido Silvestri, Michael D. Miller, Alan S. Perelson, and Cristian Apetrei

Divisions of Comparative Pathology, Microbiology, and Veterinary Medicine Tulane National Primate Research Center, Covington Louisiana 70433, USA; Department of Pathology, School of Medicine, Tulane University, New Orleans, Louisiana 70112, USA; Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545, USA; Department of Pathology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19107, USA; Gilead Sciences, Inc, Foster City, California 94404, USA; Department of Tropical Medicine, School of Public Health, Tulane University, New Orleans, Louisiana 70112, USA

Abstract

The mechanisms underlying the lack of disease progression in natural SIV hosts are still poorly understood. To test the hypothesis that SIV-infected AGMs avoid AIDS due to virus replication occurring in long-lived infected cells, we infected six animals with SIVagm and treated them with potent antiretroviral therapy [ART: (PMPA, tenofovir) and (FTC, emtricitabine)]. All AGMs showed a rapid decay of plasma viremia that became undetectable 36 hours after ART initiation. Significant decrease of viral load was observed in PBMCs and intestine. Mathematical modeling of viremia decay post-ART indicates a half-life of productively infected cells ranging from 4 to 9.5 h, i.e., faster than previously reported for HIV and SIV. ART induced a slight but significant increase in peripheral CD4+ T-cell counts but no significant changes in CD4+ T-cell levels in LNs and intestine. Similarly, ART did not significantly change the levels of cell proliferation, activation and apoptosis, already low in chronically SIVagm-infected AGMs. Collectively, these results indicate that, in SIVagm-infected AGMs, the bulk of virus replication is sustained by short-lived cells; therefore, differences in disease outcome between SIVmac infection of macaques and SIVagm infection of AGMs are unlikely due to intrinsic differences of the in vivo cytopathicity between the two viruses.

Merck & VRC HIV Vaccines: Immune Response Data

As a follow-up to yesterday's post, here is a quick round up of the published data relating to immune responses generated by the Merck and VRC HIV vaccine candidates. I've also added the recent conference presentations that I could find, but note that this almost certainly omits some additional presentations for which the abstracts are not accessible online (e.g. the annual Keystone HIV vaccine conference). A full comparative analysis will have to await a future post but a few things jump out immediately:

  • The Merck vaccine appears to have been surprisingly poor at inducing HIV-specific CD4 T cell responses. During initial talks about the vaccine, my recollection is that the rates of CD4 T cell responses were said to be comparable to CD8 T cell responses, but according to the CROI abstract from 2005, only ~30% of people with detectable HIV-specific CD8 T cells also displayed HIV-specific CD4 T cells. This raises a number of questions about the functionality of the HIV-specific CD8 T cell response in people who lacked detectable CD4 T cells (CD4 T cell help is required for the efficient generation and secondary expansion of CD8 T cells) and also whether the activation of pre-existing Ad5-specific CD4 T cell responses by the vector somehow interfered with the development of CD4 T cell responses to the HIV proteins encoded by the vaccine.
  • The limited polyfunctionality data presented by Merck at the AIDS Vaccines 2007 conference does appear to support the contention that the VRC construct induces a more polyfunctional CD8 T cell response than the Merck HIV vaccine.
  • Given the importance of the topic, the HIV vaccine field urgently needs more comprehensive published data than the limited amount that is currently available; it should not be necessary to try and read immunological tea leaves when considering the implications of the Merck vaccine failure for other candidates such as the VRC's.

Merck – published papers:

J Acquir Immune Defic Syndr. 2007 May 1;45(1):20-7.

Detection of HIV vaccine-induced cell-mediated immunity in HIV-seronegative clinical trial participants using an optimized and validated enzyme-linked immunospot assay.

Dubey S, Clair J, Fu TM, Guan L, Long R, Mogg R, Anderson K, Collins KB, Gaunt C, Fernandez VR, Zhu L, Kierstead L, Thaler S, Gupta SB, Straus W, Mehrotra D, Tobery TW, Casimiro DR, Shiver JW.

Department of Vaccine and Biologics Research, Merck Research Laboratories, West Point, PA 19486, USA.

An effective vaccine for HIV is likely to require induction of T-cell-mediated immune responses, and the interferon-gamma (IFNgamma) enzyme-linked immunospot (ELISPOT) assay has become the most commonly used assay for measuring these responses in vaccine trials. We optimized and validated the HIV ELISPOT assay using an empirical method to establish positivity criteria that results in a < or =1% false-positive rate. Using this assay, we detected a broad range of HIV-specific ELISPOT responses to peptide pools of overlapping 20mers, 15mers, or 9mers in study volunteers receiving DNA- or adenovirus vector-based HIV vaccines and in HIV-seropositive donors. We found that 15mers generally had higher response magnitudes than 20mers and lower false-positive rates than 9mers. These studies show that our validated ELISPOT assay using 15mer peptide pools and the positivity criteria of > or =55 spots per 10(6) cells and > or =4-fold over mock (negative control) is a sensitive and specific assay for the detection of HIV vaccine-induced cell-mediated immunity.

AIDS Res Hum Retroviruses. 2006 Nov;22(11):1081-90.

A comparison of standard immunogenicity assays for monitoring HIV type 1 gag-specific T cell responses in Ad5 HIV Type 1 gag vaccinated human subjects.

Tobery TW, Dubey SA, Anderson K, Freed DC, Cox KS, Lin J, Prokop MT, Sykes KJ, Mogg R, Mehrotra DV, Fu TM, Casimiro DR, Shiver JW.

Department of Vaccines and Biologics Research, Merck Research Laboratories, West Point, Pennsylvania 19486, USA.

Currently, there are numerous candidate HIV vaccines aimed at inducing T-cell mediated immune responses against HIV. To assess the immunogenicity of such vaccines, a reliable T cell assay must be utilized and typically one of the following assays is chosen for this purpose: bulk culture CTL, MHC I tetramer staining, IFN-gamma ELISPOT, or IFN-gamma intracellular cytokine staining. In this paper we report a comparison of the T cell responses detected by each assay in a large cohort of healthy normal volunteers vaccinated with adenovirus serotype 5 expressing HIV gag. Using stringently validated formats of each of these assays and pools of overlapping HIV gag peptides, we demonstrate that there is a high degree of correlation between all four of the common T cell assays, but inherent differences in the sensitivity of each assay to detect responders. In this study, the ELISPOT assay is shown to have the greatest sensitivity in detecting vaccine responses, while the ICS assay, although less sensitive, has the advantage of providing additional information on the phenotype of the responding cells.

AIDS Res Hum Retroviruses. 2007 Jan;23(1):86-92

Enhanced rates and magnitude of immune responses detected against an HIV vaccine: effect of using an optimized process for isolating PBMC.

Kierstead LS, Dubey S, Meyer B, Tobery TW, Mogg R, Fernandez VR, Long R, Guan L, Gaunt C, Collins K, Sykes KJ, Mehrotra DV, Chirmule N, Shiver JW, Casimiro DR.

Vaccine and Biologics Research, Merck Research Laboratories, West Point and Wayne, PA 19087, USA.
Quantitative analysis of cell-mediated immune responses induced by candidate HIV vaccines requires robust procedures for collecting and processing human peripheral mononuclear blood cells (PBMCs). We evaluated several parameters in order to optimize a sample handling process that would be suitable for a multicenter clinical trial. Among the findings, systematic increases in the magnitude of IFN-gamma ELISpot responses were observed when the time from blood collection to PBMC freezing was reduced to <12 h. By implementing these improvements within an ongoing clinical trial, the estimated immunologic response rates to an adenovirus- based HIV vaccine increased by more than 20 percentage points to approximately 80% of the vaccine recipients against any of the vaccine antigens and the average levels of T cell response improved more than 3-fold. These studies establish the importance of optimal conditions for PBMC collection and handling to the success of a clinical development program.

Merck – conference presentations:

AIDS Vaccines 2007

http://www.hivvaccineenterprise.org/_dwn/Oral_Sessions.pdf

OA08-02
Safety and immunogenicity of the MRKAd5 gag HIV-1 vaccine in a worldwide phase I study of healthy adults (Merck V520-018/HVTN 050)

S Hammer5, M Miller12, J Pape10, P Pitisuttithum11, V Suriyanon3, S Nitayaphan1, J Sanchez2, E Kallas6, C Harro9, G Gray4, M Cardinali7, K Turner8, X Sun12, D Mehrotra12 and E Quirk12

1 Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; 2 Asociación Civil Impacta Salud y Educación, Lima, Peru; 3 Chiang Mai University, Chiang Mai, Thailand; 4 Chris Hani Baragwanath Hospital, Johannesburg, South Africa; 5 Columbia University, New York, NY, USA; 6 Federal University of Sao Paulo, Sao Paolo, Brazil; 7 Henry M. Jackson Foundation at the Division of AIDS, NIAID, Bethesda, MD, USA; 8 HIV Vaccine Trials Network, Seattle, WA, USA; 9 Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA; 10 Les Centres GHESKIO, Port-au- Prince, Haiti; 11 Mahidol University, Bangkok, Thailand; 12 Merck Research Laboratories, West Point, PA, USA

Background: Phase I studies indicate the monovalent MRKAd5 HIV-1 gag vaccine is well tolerated and immunogenic in N. American populations. High prevalence of preexisting immunity to adenovirus type 5 (Ad5) may affect vaccine response rates. Aim: We analyzed the preliminary data through Week 30 of this international Phase I study testing the safety and immunogenicity of an Ad5 HIV vaccine candidate. Methods: Healthy adults aged 18-50 at low risk for HIV infection were randomized 1:3:3 to receive placebo, 1x109 or 1x1010 viral particles (vp) of the MRKAd5 HIV-1 gag vaccine at Day 1, Week 4 and Week 26 in a dose-escalating staged study in 24 centers in Africa, Asia, Caribbean, N. and S. America. Enrollment was not stratified by baseline Ad5 titer. Adverse events (AE) and lab values were assessed after each dose. Immunogenicity was evaluated using an IFN-γ ELISPOT gag 15-mer assay. Positive ELISPOT responses were defined as >55 SFC/106 PBMC and ≥4-fold over mock control. Results: 360 people (55% male, median age 30) were enrolled (87 each in Asia and N. and S.America; 75 in the Caribbean; 24 in Africa). The vaccine was generally well tolerated at both doses. The most common AEs were injection site reaction, headache, fever, and diarrhea. At Week 30, pooled ELISPOT responses were 57/133 (43%) in the 1x109 vp group and 108/139 (78%) in the 1x1010 vp group. Overall, responses to 1x1010 vp were 85% and 68% in subjects with low (≤200, n=75) and high (>200, n=62) baseline Ad5 titers, respectively. Response rates among subjects with high baseline Ad5 titers who received 1x1010 vp were: 23/26 (88%) in Asia, 2/7 (29%) in N. America, 10/13 (77%) in S. America, 7/12 (58%) in the Caribbean, and 0/4 in Africa. Conclusion: The MRKAd5 HIV-1 gag vaccine was generally well tolerated and immunogenic in diverse world regions. The 1x1010 vp dose was generally more immunogenic than 1x109 vp. Although there may be a modest effect of high baseline Ad5 titers on ELISPOT responses, overall most subjects with high levels of preexisting Ad5 immunity had positive ELISPOT responses to 1x1010 vp. These data indicate that the MRKAd5 HIV-1 gag vaccine may be immunogenic in regions with high prevalence of Ad5 immunity. This international study of the MRKAd5 gag vaccine supports ongoing Phase II test-of-concept trials of a next generation MRKAd5 trivalent gag/pol/nef vaccine.

http://www.hivvaccineenterprise.org/_dwn/Poster_Sessions.pdf

P06-29
Evaluation of multi-functional T cell responses elicited by the Merck trivalent Ad5gag/pol/nef vaccine using a qualified 9 color flow cytometric assay

KS Cox, JH Clair, MT Prokop, S Dubey, J Shiver and D Casimiro

Merck Research Laboratories, West Point, PA, USA

Background: Cellular immunity has been shown to play a critical role in the control of HIV-1 infections. To date, the most commonly measured T cell response in HIV vaccine programs is IFN-gamma (IFN-γ) production. Recently, there has been increased interest in the examination of additional T cell markers to measure the quality and breadth of the immune response, which may be important in HIV viral control. Although these types of multi-color flow cytometeric assays have been emerging across various laboratories, data sets have not been generated using a statistically qualified assay, which is critical for the accurate interpretation of results. Objective: To qualify a multi-color intracellular cytokine staining (ICS) assay to determine the positivity criteria, false positive rates, and the repeatability of positive responses and utilize this assay to measure the immune responses in a cohort of forty HIV clinical trial vaccinees. Methods: A flow based assay was developed to simultaneously examine five T cell functions (CD107a, IFN-γ, IL-2, MIP1-β, and TNFα). This analysis results in 31 subsets each for the CD8 and CD4 populations. To qualify the assay, 10 HIV gag responders were repeated in 4 assay runs, and 10 HIV seronegative subjects were each run twice with HIV gag, nef and pol 15 mer peptide pools. After statistical analysis of the qualification data set, a cohort of forty HIV seronegative clinical trial participants who were vaccinated with 3 x1010 v.p. of the Merck Trivalent Adenovirus type 5 vaccine (MRKAd5 HIV-1 gag/pol/nef) were tested. The pre-vaccination samples from the same cohort were tested for clinical confirmation of the false positive rates. Results: Assay qualification demonstrated that a two-dimensional positivity cut-off of >90 antigen-specific events per million lymphocytes and >3-fold over background (no antigen) would result in false positive rate of <5% per subset of responses. When the qualified assay was used to evaluate responses in the 40 vaccinees, we observed positive responses in 9 of the 31 CD8 subsets and 10 of the 31 CD4 subsets. Conclusion: A data set from MRKAd5 HIV-1 gag/pol/nef vaccinees was generated using a qualified multi-color ICS assay. The vaccine elicited multifunctional T cell responses to HIV gag, pol and nef in both the CD8 and CD4 T cell populations.

P08-17
Flow cytometric analysis of T cell proliferation using a CFSE dye assay

KJ Sykes, S Dubey, Y Wang, Shiver and D Casimiro

Merck and Co., West Point, PA, USA

Background: Greater understanding of the role of HIV-specific immunity remains fundamental to current and future therapies to prevent and treat HIV infection. Very early in HIV infection, prior to a decrease in absolute CD4 cell number, functional defects in HIV-specific CD4+ T helper cells become apparent, including the ability of the CD4+ peripheral blood mononuclear cells (PBMCs) to proliferate in response to HIV antigens. A flow cytometrybased proliferation assay using CFSE has become a widely used method to measure proliferation in samples from HIV infected patients and in HIV vaccine recipients. However, high backgrounds and low sensitivity have often been observed with this assay, prompting further optimization and characterization in order for it to be a useful tool in vaccine studies. Objective: To assess the proliferative capacity of HIV seropositive donors and HIV seronegative vaccinees using an optimized CFSE flow cytometric assay measuring CD4 and CD8 T cell proliferation. Methods: The CFSE assay was optimized by comparing serum sources, cell concentrations and culturing conditions using frozen-thawed PBMC. Using the optimized CFSE assay, data was collected from 39 HIV seropositive individuals and 10 HIV seronegative vaccinees who received Adenovirus-5 HIV gag vaccine (Ad5 gag). CFSE labeled cells were cultured in 96-deep well plates in the presence or absence of Gag 15mer peptide for 7 days. After 7 days, cells were stained using CD3, CD4 and CD8 monoclonal antibodies and run on a BD FACsCalibur. Data was analyzed using FlowJo software. Results: The assay was successfully optimized to give low backgrounds and measurable proliferation in both cohorts analyzed. Proliferation in HIV seropositive individuals ranged from 1.0% to 4.5% for CFSElowCD8highand 1.5% to 2.0% for CFSElowCD4high. HIV seronegative vaccinees showed gagspecific proliferation at similar yet higher levels compared to HIV-infected donors, with post vaccination proliferation ranging from 2.0% to 8.0% for CFSElowCD8highand 1.0% to 6.0% for CFSElowCD4high. Conclusion: Optimizing the CFSE assay has allowed detection of proliferation in HIV-infected donors and in seronegative HIV gag vaccinees. This optimized assay shows that the Merck Ad5 gag vaccine induces HIV-specific proliferation in our vaccine recipients.

CROI 2005 Abstract #506

Detailed Characterization of the Cellular Immune Responses in Healthy Volunteers Immunized with Replication-defective Adenovirus HIV Vaccines

Danilo Casimiro*, S Dubey, T Tobery, L Kierstead, J Condra, A Finnefrock, R Isaacs, M Robertson, R Leavitt, R Mogg, D Mehrotra, J Kublin, J Shiver, and V520 Merck Study Group
Merck & Co, West Point, PA, USA

Background:  We have recently been developing replication-defective adenovirus type 5 (MRKAd5)-based vaccines that express reasonably conserved viral antigens (gag, pol, nef) of the B clade in several phase I studies. It is important to assess the potential of this vaccine to elicit potent cytotoxic activity as well as to provide broad coverage against viruses both intraclade and interclade.

Methods:  Peripheral mononuclear cells (PBMC) were obtained from subjects in 3 phase I studies, each evaluating a different MRKAd5-based vaccine. MRKAd5 HIV-1 gag and the trivalent MRKAd5 gag/pol/nef vaccines were independently tested in healthy adults at low risk of HIV infection (18 to 50 years of age). HIV-specific T-cell responses were evaluated by IFN-γ ELISpot and intracellular cytokine staining (ICS) against full antigen peptide pools. The responses were also dissected by testing PBMC against series of smaller pools of the gag, pol, or nef peptides. PBMC from responders were also analyzed for cross-reactivity against peptide pools representing near-consensus sequences of clade A and C antigens.

Results:  The MRKA5 vaccines elicited predominantly antigen-specific CD8+ T cells; a smaller fraction (20 to 30%) of patients with positive ICS responses contained detectable levels of virus-specific helper T cells. Cross-clade gag- and nef-specific responses were evaluated using the ELIspot method; cross-clade responses against pol were not evaluated because of its high protein sequence conservation (90% across clades vs 80% for gag and 70% for nef). About 66% of individuals (73 of 110 receiving either the MRKAd5 gag or MRKAd5 trivalent vaccine) with responses to the vaccine CAM1 HIV-1 gag (clade B) peptide pool cross-reacted with either clade A gag or clade C gag sequences. Of those receiving the MRKAd5 trivalent vaccine who had responses against JRFL HIV-1 nef (clade B), 38% (10 of 26) were able to respond to the clade A nef pool, while 19% (5 of 26) cross-reacted with clade C nef. PBMC were also assayed against a series of smaller pools (mini-pools) each consisting of 8 sequence-consecutive 9-aa peptides from gag, pol, and nef. The median numbers of positive mini-pools for clade B gag, pol, and nef were 2, 2, and 1, respectively

Conclusions:  The MRKAd5 vaccines are potent in eliciting CD8+ and to a lesser degree CD4+ T cells in human clinical trials. The vaccine antigens exhibited levels of immune coverage across multiple clades although at varying levels depending on the antigen.

VRC -  published papers:

Vaccine. 2007 May 16;25(20):4085-92. Epub 2007 Mar 7.

Phase I clinical evaluation of a six-plasmid multiclade HIV-1 DNA candidate vaccine.

Catanzaro AT, Roederer M, Koup RA, Bailer RT, Enama ME, Nason MC, Martin JE, Rucker S, Andrews CA, Gomez PL, Mascola JR, Nabel GJ, Graham BS; VRC 007 Study Team.

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 40 Convent Drive, Building 40, Bethesda, MD 20892-3017, USA.

Needle-free delivery of a six-plasmid HIV-1 DNA vaccine encoding EnvA, EnvB, EnvC, and subtype B Gag, Pol, and Nef underwent open-label evaluation in 15 subjects; 14 completed the 0, 1, 2 month vaccination schedule. T cell responses to HIV-specific peptide pools were detected by intracellular cytokine staining of CD4(+) [13/14 (93%)] and CD8(+) [5/14 (36%)], and by ELISpot in 11/14 (79%). Ten of 14 (71%) had ELISA antibody responses to Env proteins. Compared to a four-plasmid product, Gag- and Nef-specific T cell responses were improved, while Env-specific responses were maintained. This candidate vaccine has now advanced to Phase II evaluation.

J Acquir Immune Defic Syndr. 2007 Apr 15;44(5):601-5.

Safety and immunogenicity of a Gag-Pol candidate HIV-1 DNA vaccine administered by a needle-free device in HIV-1-seronegative subjects.

Tavel JA, Martin JE, Kelly GG, Enama ME, Shen JM, Gomez PL, Andrews CA, Koup RA, Bailer RT, Stein JA, Roederer M, Nabel GJ, Graham BS.

Division of Clinical Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, USA.

OBJECTIVE: To evaluate the safety and immunogenicity of a candidate HIV DNA vaccine administered using a needle-free device. DESIGN: In this phase 1, dose escalation, double-blind, placebo-controlled clinical trial, 21 healthy adults were randomized to receive placebo or 0.5, 1.5, or 4 mg of a single plasmid expressing a Gag/Pol fusion protein. Each participant received repeat immunizations at days 28 and 56 after the first inoculation. Safety and immunogenicity data were collected. RESULTS: The vaccine was well tolerated, with most adverse events being mild injection site reactions, including pain, tenderness, and erythema. No dose-limiting toxicities occurred. HIV-specific antibody response was not detected in any vaccinee by enzyme-linked immunosorbent assay. HIV-specific T-cell responses to Gag or Pol as measured by enzyme-linked immunospot assay and intracellular cytokine staining were of low frequency and magnitude. CONCLUSIONS: This candidate HIV DNA vaccine was safe and well tolerated. No HIV-specific antibody responses were detected, and only low-magnitude HIV-specific T-cell responses were detected in 8 (53%) of 15 vaccinees. This initial product led to the development of a 4-plasmid multiclade HIV DNA Vaccine Research Center vaccine candidate in which envelope genes expressing Env from clades A, B, and C and a Nef gene from clade B have been added.

J Infect Dis. 2006 Dec 15;194(12):1650-60. Epub 2006 Nov 8.

Comment in:
J Infect Dis. 2006 Dec 15;194(12):1625-7.

Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 DNA candidate vaccine. (free full text access)

Graham BS, Koup RA, Roederer M, Bailer RT, Enama ME, Moodie Z, Martin JE, McCluskey MM, Chakrabarti BK, Lamoreaux L, Andrews CA, Gomez PL, Mascola JR, Nabel GJ; Vaccine Research Center 004 Study Team.

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892-3017, USA.

BACKGROUND: Gene-based vaccine delivery is an important strategy in the development of a preventive vaccine for acquired immunodeficiency syndrome (AIDS). Vaccine Research Center (VRC) 004 is the first phase 1 dose-escalation study of a multiclade HIV-1 DNA vaccine. METHODS: VRC-HIVDNA009-00-VP is a 4-plasmid mixture encoding subtype B Gag-Pol-Nef fusion protein and modified envelope (Env) constructs from subtypes A, B, and C. Fifty healthy, uninfected adults were randomized to receive either placebo (n=10) or study vaccine at 2 mg (n=5), 4 mg (n=20), or 8 mg (n=15) by needle-free intramuscular injection. Humoral responses (measured by enzyme-linked immunosorbant assay, Western blotting, and neutralization assay) and T cell responses (measured by enzyme-linked immunospot assay and intracellular cytokine staining after stimulation with antigen-specific peptide pools) were measured. RESULTS: The vaccine was well tolerated and induced cellular and humoral responses. The maximal CD4(+) and CD8(+) T cell responses occurred after 3 injections and were in response to Env peptide pools. The pattern of cytokine expression by vaccine-induced HIV-specific T cells evolved over time, with a diminished frequency of interferon- gamma -producing T cells and an increased frequency of interleukin-2-producing T cells at 1 year. CONCLUSIONS: DNA vaccination induced antibody to and T cell responses against 3 major HIV-1 subtypes and will be further evaluated as a potential component of a preventive AIDS vaccine regimen.

J Infect Dis. 2006 Dec 15;194(12):1638-49. Epub 2006 Nov 8.

Comment in:
J Infect Dis. 2006 Dec 15;194(12):1625-7.

Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 candidate vaccine delivered by a replication-defective recombinant adenovirus vector. (free full text access)

Catanzaro AT, Koup RA, Roederer M, Bailer RT, Enama ME, Moodie Z, Gu L, Martin JE, Novik L, Chakrabarti BK, Butman BT, Gall JG, King CR, Andrews CA, Sheets R, Gomez PL, Mascola JR, Nabel GJ, Graham BS; Vaccine Research Center 006 Study Team.

Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892-3017, USA.

BACKGROUND: The development of an effective human immunodeficiency virus (HIV) vaccine is a high global priority. Here, we report the safety, tolerability, and immunogenicity of a replication-defective recombinant adenovirus serotype 5 (rAd5) vector HIV-1 candidate vaccine. METHODS: The vaccine is a mixture of 4 rAd5 vectors that express HIV-1 subtype B Gag-Pol fusion protein and envelope (Env) from subtypes A, B, and C. Healthy, uninfected adults were randomized to receive 1 intramuscular injection of placebo (n=6) or vaccine at dose levels of 10(9) (n=10), 10(10) (n=10), or 10(11) (n=10) particle units and were followed for 24 weeks to assess immunogenicity and safety. RESULTS: The vaccine was well tolerated but was associated with more reactogenicity at the highest dose. At week 4, vaccine antigen-specific T cell responses were detected in 28 (93.3%) and 18 (60%) of 30 vaccine recipients for CD4(+) and CD8(+) T cells, respectively, by intracellular cytokine staining assay and in 22 (73%) of 30 vaccine recipients by enzyme-linked immunospot assay. Env-specific antibody responses were detected in 15 (50%) of 30 vaccine recipients by enzyme-linked immunosorbant assay and in 28 (93.3%) of 30 vaccine recipients by immunoprecipitation followed by Western blotting. No neutralizing antibody was detected. CONCLUSIONS: A single injection induced HIV-1 antigen-specific CD4(+) T cell, CD8(+) T cell, and antibody responses in the majority of vaccine recipients. This multiclade rAd5 HIV-1 vaccine is now being evaluated in combination with a multiclade HIV-1 DNA plasmid vaccine.

VRC – conference presentations:

AIDS Vaccines 2007

http://www.hivvaccineenterprise.org/_dwn/Oral_Sessions.pdf

OA08-01
Adenoviral HIV-1 vaccine elicits durable CD8+ and CD4+ HIV specific responses in HIV-1 uninfected adults without pre-existing Ad5 antibodies, HVTN 054

C Morgan2, L Peiperl4, Z Moodie2, D Carter2, S De Rosa2, N Russell1,
B Graham3 and N HIV Vaccine Trials Network2

1 Bill and Melinda Gates Foundation, Seattle, WA, USA; 2 Fred Hutchinson Cancer Research Center, Seattle, WA, USA; 3 NIAID Vaccine Research Center, Bethesda, MD, USA; 4 University of California San Francisco, San Francisco, CA, USA

Objective: To evaluate the safety and immunogenicity of the NIAID Vaccine Research Center adenoviral vector HIV gag-polB/envA/envB/envC vaccine (rAd5-HIV) delivered IM at 2 doses in adults with undetectable levels of preexisting adenovirus type 5 (Ad5) neutralizing antibodies (nAb). Methods: The NIAID HIV Vaccine Trials Network enrolled 48 participants: 20 received 1 dose of 1010 PU rAd5-HIV (T1), 20 1011 PU rAd5-HIV (T2), and 8 placebo (C). Participants were monitored for reactogenicity and adverse events. PBMC were evaluated by IFN-γ ELISpot and CD4/CD8, IFN-γ/IL-2 intracellular cytokine staining (ICS) assays. These assays utilized potential T cell epitope peptide pools for Gag, Pol, and Env, representing peptides present in at least 15% of HIV-1 isolates in the Los Alamos Database. HIV antibody testing was performed using Abbot HIVAB HIV 1/2, BioRad Genetic Systems HIV 1/2 Plus O, and/or bioMerieux Vironostika HIV-1 EIAs. Results: The vaccine appeared safe in participants without prior Ad5 nAb (presented at AIDS Vaccine 2006). IFN-γ ELISpot response rates to any of the 3 antigens at 4 weeks post injection (D28) were 0/7C, 14/16 T1 and 17/20 T2 with magnitudes up to 3200 SFC/106 PBMC to a peptide pool. 53% of vacinees recognized all 3 antigens, 22% recognized 2, 11% recognized 1, and 14% recognized 0. One year post vaccination the IFN-γ ELISpot response rates were 15/22 T1 and 13/20 T2. Response rates to any of the 3 antigens for CD4+ or CD8+ T cells by ICS for IFN-γ and/or IL-2 at D28 were 0/8 C, 17/19 T1, and 17/20 T2 with up to 4.2% of T cells responding to a peptide pool. 0/8 C, 12/19 T1, and 10/20 T2 had HIV-specific CD4+ T cell responses. 0/8 C, 15/18 T1, and 16/20 T2 had HIV-specific CD8+ T cell responses. One year post vaccination, 0/8 C, 18/19 T1, and 15/19 T2 tested positive for vaccine induced HIV antibodies by 1 or more EIA. Conclusion: One dose of this rAd5-HIV vaccine elicited high frequency and magnitude of CD8+ T cell responses to HIV antigens in Ad5 nAb seronegative persons. These responses were discernible for up to one year, perhaps related to the associated CD4+ T cell responses. 75% of vaccinees recognized epitopes in 2 or more antigens. 87% of uninfected vaccinees developed antibodies detected by commercial HIV antibody tests. To date, these are the most potent vaccine induced HIV-1 responses reported in humans.

OA08-03
Safety and immunogenicity of VRC multiclade HIV-1 adenoviral vector vaccine alone or with VRC multiclade HIV-1 DNA plasmid vaccine in African adults

W Jaoko4, K Kayitenkore6, GO Manyonyi3, E Karita6, C Schmidt2, P Fast2, W Komaroff2, A Cooper1, M Boaz1, J Gilmour1, L Dally7, M Ho7, C Smith7 and B Graham5

1 IAVI Core Laboratory, London, United Kingdom (Great Britain); 2 International AIDS Vaccine Initiative (IAVI), New York, NY, USA; 3 Kenya AIDS Vaccine Initiative (KAVI), Nairobi, Kenya; 4 Kenya AIDS Vaccine Initiative (KAVI), University of Nairobi, Nairobi, Kenya; 5 NIH Vaccine Research Centre (VRC), Bethesda, MD, USA; 6 Project San Francisco (PSF), Kigali, Rwanda; 7 The EMMES Corporation, Rockville, MD, USA

Methods: Healthy adults aged 18-50 in Kigali, Rwanda and Nairobi, Kenya were randomized to either i) one intramuscular injection of 1x1010 or 1x1011 particle units of VRC multiclade HIV-1 recombinant adenoviral vector vaccine (rAd5, n=35) or placebo, or ii) 3 doses 4mg VRC multiclade HIV-1 DNA vaccine (DNA) followed by 1 dose rAd5 1x1010 or 1x1011 as boost or placebo (n=79) (vaccine:placebo 3:1). Safety and tolerability were assessed clinically and by routine lab tests. Immunogenicity was evaluated by Ad5-specific neutralization (NT) assay and IFN-γ ELISpot on frozen PBMC with matched peptides reported as spot forming cells (SFC)/million PBMC. Results: The study is ongoing; preliminary safety and group unblinded immunogenicity data are presented. Local reactions were experienced by approx. 75% of volunteers following any rAd5/placebo and almost all volunteers following any DNA/placebo, most events were mild. Systemic symptoms were reported by 67-72% following any rAd5/placebo and 89% of volunteers following any DNA/placebo, most events were mild. 342 adverse events, mostly mild, were reported within 28 days of any vaccination. There were no vaccine related serious adverse events. Immune responses by ELISpot were detected in 6/13 (46%) and 7/13 (54%) recipients of rAd5 1010 and rAd5 1011 respectively, and in 0/9 placebo recipients. Median SFC were 85 and 77 per million PBMC respectively (range 39-297). Following 3 DNA/placebo there were 27/55 (49%) vaccinees and 1/20 placebo recipients with positive IFN-y ELISpot responses. Median SFC were 92 (range 44-598). Following rAd5 1010 and rAd5 1011 boost, there were 18/25 (72%) and 18/26 (69%) responders respectively. Median SFC were 106 and 105 (range 41-1707). At baseline, 74% of all volunteers had detectable Ad5 NT antibodies (Ab). In either DNA prime/rAd5 boost arms the impact of Ad5 NT Ab on immunogenicity amongst vaccine recipients was modest. In rAd5 alone arms numbers were too small to assess effect. Conclusion: Vaccination with rAd5 either alone or as boost in combination with corresponding DNA vaccine appears safe and well tolerated. Data from African volunteers indicates good immunogenicity of DNA prime/rAd5 boost regimen, appears equivalent at the different rAd5 boost doses and only modestly affected by baseline Ad5 NT Ab. Future trials will focus on larger sample sizes and those at risk for HIV.

OA08-04
A phase IIA trial to evaluate a multiclade HIV-1 DNA vaccine followed by a multiclade rAd5 HIV-1 vaccine boost in HIV-1 uninfected adults (HVTN 204)

MC Keefer7, C Morgan3, G Churchyard1, E Adams2, J Hural3, B Graham5, Z Moodie3, G Gray8, L Bekker6, L Baden4 and M McElrath3

1 Aurum Institute for Health Research, Klerksdorp, South Africa; 2 Division of AIDS, NIAID, Bethesda, MD, USA; 3 Fred Hutchinson Cancer Research Center, Seattle, WA, USA; 4 Harvard University Medical School, Boston, MA, USA; 5 NIAID Vaccine Research Center, Bethesda, MD, USA; 6 University of Cape Town, Cape Town, South Africa; 7 University of Rochester School of Medicine and Dentistry, Rochester, NY, USA; 8 University of Witwatersrand, Johannesburg, South Africa

Background: The NIAID HIV Vaccine Trials Network (HVTN) has undertaken a prospective, randomized, double-blind, placebo-controlled phase IIA clinical trial of the NIAID Vaccine Research Center’s (VRC) 6-plasmid candidate DNA HIV-1 (envA, envB, envC, gagB, polB, nefB) (DNA-HIV) and rAd5 HIV- 1 (envA, envB, envC, gagB, polB) vaccine (Ad5-HIV) in healthy uninfected people in diverse geographic locations. Methods: A total of 480 participants (ppts) were enrolled irrespective of their baseline Ad5 titer; 240 in the Americas (US, Brazil, Jamaica & Haiti) and 240 in South Africa. Half in each region received DNA-HIV (4 mg IM by Biojector) at 0, 1 and 2 months, followed by Ad5-HIV (1010 PU IM by needle/syringe) at 6 months; the other half received placebo injections on the same schedule. Ppts were monitored for reactogenicity and adverse events throughout the 12- month trial; sera and PBMCs were evaluated by humoral (binding/neutralizing antibody) and cellular (bulk IFN-γ ELISpot and IFN-γ /IL-2 intracellular cytokine staining, using global Potential T cell Epitope [PTE] peptide pools) immune assays. Results: At the US sites, the 180 allotted ppts completed enrollment on 7 Apr 06 while enrollment was completed in South Africa on 18 Dec 06 and in the Caribbean/South American region on 20 Mar 07. Preliminary blinded safety and immunogenicity results are available for the US cohort. Both vaccines were well-tolerated. DNA-HIV/placebo caused more local reactions; moderate pain in 10% of participants after 1st vaccination, decreasing with subsequent injections, while Ad5-HIV/placebo caused more systemic reactions; selflimited moderate malaise and/or fatigue in 9.3%. At days 0 and 210 (6 weeks after the rAd5-HIV boost), IFN-γ ELISpot assays were positive in 1.6% and 37.8% of study ppts (half of whom received placebo), respectively. Of those that were positive, responses to Env and Gag peptides were most frequent, seen in 73.2% and 80.4% of responders, respectively. Conclusion: These preliminary interim data indicate acceptable safety and suggest that IFN-γ ELISpot responses using the PTE peptide pools could be positive in up to 75% of vaccine recipients. If further study data confirm these findings and results are favorable from other related protocols, evaluation of this regimen in a phase IIB efficacy trial will be proposed, and would be conducted by the Partnership for AIDS Vaccine Evaluation (PAVE) in distinct regions with diverse HIV-1 epidemics.

http://www.hivvaccineenterprise.org/_dwn/Poster_Sessions.pdf

P06-16
DNA prime followed by adenoviral vector boost elicits HIV-1 specific CD8+ T cell responses in healthy HIV-1 uninfected adults (HVTN 052 and 057)

C Morgan2, L Peiperl4, M McElrath2, Z Moodie2, S De Rosa2, D Carter2, N Russell1, B Graham3 and N HIV Vaccine Trials Network2

1 Bill and Melinda Gates Foundation, Seattle, WA, USA; 2 Fred Hutchinson Cancer Research Center, Seattle, WA, USA; 3 NIAID Vaccine Research Center, Bethesda, MD, USA; 4 University of California San Francisco, San Francisco, CA, USA

Objective: To evaluate the safety and immunogenicity of 2 or 3 doses of a 4-plasmid DNA (envA, envB, envC, gagB-polB-nefB) HIV-1 prime (DNA) followed by a recombinant adenoviral vector (envA, envB, envC, gagB-polB) HIV-1 boost (rAd5) in healthy, HIV-1 uninfected adults. Methods: The NIAID HIV Vaccine Trials Network enrolled 180 participants (ppts) in HVTN 052 where ppts received 4mg DNA x 3 at 0, 1 and 2 mos (N=60; T1), 4mg DNA x 2 at 0, 2 mos (N=60; T2) or placebo (N=10; C). Seventy of these ppts rolled over into HVTN 057 and received 1 dose of 1010PU rAd5 6-9 mos after completing the DNA prime (N=30 in T1 and T2, N=10 in C). Ppts were monitored for reactogenicity and adverse events. PBMC were collected and shipped overnight prior to cryopreservation. PBMC were evaluated by IFN-γ ELISpot and CD4/CD8, IFN-γ/IL-2 intracellular cytokine staining (ICS) assays. These assays utilized global potential T cell epitope peptide pools for Gag, Pol, and Env, representing peptides present in at least 15% of HIV-1 clades A, B, C and non-A,B,C isolates in the Los Alamos Database. Results: There were no notable untoward safety events attributable to vaccine (presented at AIDS Vaccine 2005). The response rates to any of the 3 HIV antigens by IFN-γ ELISpot 2 weeks after the last DNA prime were 2/52 (4%) C, 28/56 (50%) T1, and 12/53 (23%) T2. By ICS the response rates to any of the 3 antigens by CD4+ or CD8+ T cells and IFN-γ and/or IL-2 secretion were 1/10 (10%) C, 11/30 (37%) T1, and 9/29 (31%) T2. 1/10 (10%) C, 8/27 (30%) T1, and 8/28 (29%) T2 were CD4+. 0/9 (0%) C, 4/30 (13%) T1, and 1/29 (3%) T2 were CD8+. Four weeks after the boost, the response rates by IFN-γ ELISpot were 0/8 (0%) C, 7/12 (58%) T1, and 10/21 (48%) T2. ICS assays were positive in 1/10 (10%) C, 12/25 (48%) T1, and 9/28 (32%) T2. 1/10 (0%) C, 4/23 (17%) T1, and 4/28 (14%) T2 were CD4+. 0/10 (0%) C, 11/25 (44%) T1, and 8/28 (29%) T2 were CD8+. The rAd5 boost elicited more responses to Gag and Pol than DNA alone. Conclusion: The DNA vaccine primarily elicited CD4+ HIV-specific T cells while the rAd5 boost elicited primarily CD8+ responses and broadened the responses to Gag and Pol. The 3rd dose of DNA may have skewed the response more towards a CD8+ response. We anticipate that the response frequencies will increase in future protocols with the evaluation of PBMC cryopreserved on the same day as venipuncture.

P06-19
Evaluation of candidate DNA HIV-1 vaccine delivery by biojector or needle and syringe in healthy adults (VRC 008)

BS Graham, JE Martin, I Gordon, M Nason, M Enama, R Koup, M Roederer, P Gomez, J Mascola and G Nabel

Vaccine Research Center, NIAID, NIH, Bethesda, MD, USA

Objective: To compare safety and immunogenicity of the NIAID Vaccine Research Center (VRC) candidate DNA HIV-1 vaccine delivered by either needle-free injection device Biojector or needle & syringe (N/S), and its ability to prime for a response to boosting with the VRC candidate recombinant replication-defective adenoviral serotype 5 HIV-1 vaccine vector (rAd5) given at a dose of 1010 or 1011 particle units (PU) in volunteers with either high or low preexisting Ad5 antibody. Methods: 40 healthy adults age 18-50 were randomized to receive 3 injections of 4 mg of the VRC multiclade DNA IM at 0, 1, and 2 months by Biojector or N/S. All subjects received rAd5 at month 6 IM by N/S at either 1010 or 1011 PU. Equal numbers in each subgroup had low (≤500) or high (>500) reciprocal titers of preexisting Ad5 95% neutralizing antibody. Cryopreserved PBMCs were evaluated by ELISpot and intracellular cytokine staining (ICS). Results: 120 DNA and 39 rAd5 injections were given; 36 subjects had a 4 week sample collected after the boost. The vaccine regimen was well tolerated for each delivery approach and dose level. Biojector resulted in occasional bruising, and routinely caused small papules or scabs (less than 1 X 1 cm) at the injection site. The lesions were observed by clinician exam after 38/60 (63%) Biojector injections, but were reported by subject diary cards in only 11/60 (18%). Lesions were never pustular or vesicular and resolved without treatment. Neither clinicians nor subjects reported any papules or scabs after any of the 60 DNA N/S injections. IFN-γ ELISpot response rates for any peptide pool at 4 weeks post rAd5 boost were 17/19 (89%) for Biojector and 13/17 (76%) for N/S delivery. The cumulative median ELISpot response (sum of highest Env+Gag+Pol+Nef responses) was 3-fold higher in the Biojector recipients than those receiving N/S. Response rates and magnitude for CD8+ T cells by ICS were similar to the patterns seen for ELISpot, but CD4+ T cell response frequencies and magnitudes by ICS were the same with use of either delivery method. Conclusion: Biojector delivery of DNA results in slightly greater local reactogenicity than N/S, but is associated with improved ELISpot and CD8+ T cell responses post boosting with rAd5. These data support continued evaluation of Biojector for DNA vaccine delivery and exploration of alternative delivery approaches to improve vaccine-induced immune responses.

P06-20
Functional profiles and epitope specificities of HIVspecific T cells induced by Ad5 HIV vaccination in Ad5- naïve, HIV-uninfected participants

H Horton1, DP Friedrich1, EC Jalbert1, SC DeRosa1, L Peiperl2, G Nabel3 and JM McElrath1

1 Fred Hutchinson Cancer Research Center, Seattle, WA, USA; 2 San Francisco Department of Public Health, San Francisco, CA, USA; 3 Vaccine Research Center, Bethesda, MD, USA

Background: We recently reported that in natural infection, the functional capabilities of HIV-specific T cells differ depending on their epitope specificities and MHC restriction. To determine if this response pattern occurs following vaccination in immunocompetent persons, we analyzed epitope specificities and functional capabilities of T cells induced by a single dose (either 1010 or 1011 PU) recombinant adenoviral vector expressing Clade B Gag/Pol and Clades A,B,C Env in 48 healthy HIV-1-uninfected adults with undetectable preexisting Ad5 neutralizing antibodies. Methods: HIV-specific vaccine-induced T cell responses were de-convoluted by IFN-γ ELISpot to determine the 9-15mer peptide recognized. In addition, functional profiling of responses was performed, including examining cytokine secretion (IFN-γ, IL-2 and TNF-α), degranulation (CD107a) and proliferation (CFSE dilution) in response to cognate epitopes. Results: A total of 66 epitopic peptides were recognized in 30 participants: 39 distinct epitopes in pol, 8 in gag and 19 in env. A median of 3 epitopes were recognized per participant (mean = 4; range 1-22). The sum of epitopespecific T cell magnitudes per individual ranged from 71-20,778 SFC/106 PBMC (median= 972; mean = 1,778). Forty-six CD8+ T cell responses were mapped to the optimal epitope in 21 individuals. Eight of these individuals (38%) possessed T cells that recognized multiple variants of 14 different epitopes. Since each volunteer was HLA typed we can infer that these epitopes were restricted by 12 different MHC alleles. Responses restricted by HLA-B27 (present at 10% in this population), -B57 (6%), -B14 (15%) and B35 (15%) were dominant (86-100% individuals expressing these alleles possessed vaccine-induced responses restricted by them). However, responses restricted by HLA-A02 and -B07 were seen very infrequently despite these alleles being present at high frequency in these subjects (A02: 48%; B07: 21%). Conclusion: Our findings indicate that immunocompetent vaccinees mount broad high magnitude CD8+ T cell responses to this candidate vaccine. Furthermore, a substantial proportion of vaccine-induced CD8+ T cells recognize multiple epitope variants present in circulating viral sequences. Finally, this study suggests that CD8+ T cell responses induced in individuals with low pre-existing Ad5 neutralizing antibody can be predicted based on HLA and that certain HLA alleles dominate vaccine-induced responses.

http://www.hivvaccineenterprise.org/_dwn/Late_Breaker_Abstracts.pdf

P06-43
Cellular immune responses in HIV-1 uninfected adult Tanzanian volunteers enrolled in a phase I/II multiclade HIV-1 DNA plasmid vaccine

A Schuetz4, A Haule3, A Mwalongo3, C Kiwole3, K Schindler3, M Schunk3, A Kroidl3, M Hoelscher2, L Maganga3, L Maboko3, M Robb5, N Michael5, B Graham6, J Cox5 and M de Souza1

1 Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; 2 Department of Infectious Diseases and Tropical Medicine, Munich, Germany; 3 Mbeya Medical Research Programme, Mbeya, Tanzania, United Republic of; 4 USMHRP / Henry M. Jackson Foundation, Mbeya, Tanzania, United Republic of; 5 USMHRP / Henry M. Jackson Foundation, Rockville, MD, USA; 6 Vaccine Research Center / NIH, Bethesda, MD, USA

Objective: To determine the frequency of T cell responses in Tanzanian seronegative participants in a multiclade phase I/II HIV-1 DNA plasmid vaccine / Adenovirus-5 vector boost vaccine trial. Methods: Sixty participants were enrolled in a phase I/II randomised, double- blind, placebo controlled trial to assess the safety and immunogenicity of a multiclade (A, B and C) HIV-1 DNA plasmid vaccine, boosted with a clade- matched HIV-1 recombinant Adenovirus-5 vector (Vaccine Research Center, NIH, USA). The vaccine:placebo ratio was 1:1. DNA was administered at weeks 0, 4 and 8 and the adenovirus boost at week 24. Cellular immunogenicity assays were conducted on a random subset of participants using an interferon-gamma (IFN- γ) ELISpot assay with freshly isolated peripheral blood mononuclear cells (PBMC). Assays were conducted at weeks 0, 6, 10, 26 and 30 to HIV-1 Env (clades A and B), Pol and Nef (clade B) peptide pools. A positive IFN- γ ELISpot response was defined as at least 55 SFC/106 PBMC and 4 times the media treated wells. Results: Forty of the 60 participants were tested by IFN- γ ELISpot. All results are blinded and include placebo controls. There were no positive IFN- γ ELISpot responses to HIV peptides prior to immunization. Positive immune responses were initially observed in volunteers at 2 weeks following the second injection against Env (5/40) and Pol (1/40). Point prevalence two weeks following the third DNA injection was 23% (9/40), with all responding against Env, 5% (2/40) against Pol and 13% (5/40) against Nef. Two weeks after the adenoviral boost 35% (14/40) of subjects demonstrated a HIV- specific immune response, all against Env, 5% (2/40) against Pol and 3% (1/40) against Nef. However, six weeks after the adenoviral boost 10/39 (26%) participants reacted against Env, 1/39 (3%) against Pol and 1/39 against Nef (3%). The cumulative frequency of positive responses 6 weeks following the completion of immunization is 16/40 (40%), with 15/40 (38 %) reacting against Env, 3/40 (8%) against Pol and 5/40 (13%) against Nef. Twelve of the 16 (75%) positive responders were positive at more than one time-point. Conclusion: This multiclade DNA/adenovirus vaccine combination induced HIV-specific cellular immune responses as measured by IFN- ELIspot assay, and these responses were sustained in a large number of study participants.

P06-44
Cellular immune responses in HIV-1 uninfected Ugandans enrolled in a phase II multiclade HIV-1 DNA plasmid/adenovirus-5 vector boost vaccine trial

L Eller1, M Eller1, P Naluyima1, D Kyabaggu1, M Robb2, H Kibuuka1, F Wabwire-Mangen1, B Graham3, N Michael2, M deSouza2 and J Cox2

1 Makerere University Walter Reed Project, Kampala, Uganda; 2 U.S. Military HIV Research Program, Rockville, MD, USA; 3 Vaccine Research Center, NIH, Bethesda, MD, USA

Objective: To determine the frequency of cellular immune responses by intracellular cytokine staining (ICS) in freshly isolated peripheral blood mononuclear cells (PBMC) derived from Ugandan HIV seronegative recipients of a multiclade HIV-1 DNA/ Adenovirus-5 (Ad5) vector vaccine combination. Methods: Sixty adult volunteers were enrolled in a randomized, double blind, placebo controlled trial to assess the safety and immunogenicity of multiclade (A,B,C) HIV-1 DNA plasmid vaccine (VRC-HIVDNA016-00-VP) boosted with HIV-1 recombinant Ad5 vector (VRC-HIVADV014-00-VP) vaccine (Vaccine Research Center, NIH Bethesda). The ratio of vaccine to placebo recipients was 1:1. DNA vaccine was administered at weeks 0, 4 and 8, with Ad5 boosting at week 24. A standard intracellular cytokine staining assay (ICS) was performed at weeks 0, 6, 10, 26 and 30 on fresh PBMC stimulated with HIV Env (clades A and B), Pol and Nef (clade B) peptide pools and analyzed for interferon-gamma (IFN-g) and interleukin 2 (IL-2) using 4-color flow cytometry. A positive response was defined as greater than or equal to 0.05 (corrected for unstimulated background) and greater than 3 times background. All assays were conducted on blinded samples. Results: Reactivity to HIV peptides was detectable in 8% (5/60) of volunteers prior to immunization. To date, cumulative positive ICS responses to HIV peptides have been observed in 58% (35/60) of volunteers in this blinded study that includes placebo controls. Cytokine production was measured in both CD4 (53%; 32/60 volunteers) and CD8 (38%; 23/60 volunteers) T cells. ICS responses were seen following the second immunization in some volunteers. 74% (26/35) of ICS responders were positive at multiple timepoints and 71% (25/35) had responses to multiple peptide pools. 77% (27/35) had responses to clade A Env, 60% (21/35) to clade B Env, 29% (10/35) to Pol, and 43% (15/35) to Nef. Conclusion: A multiclade HIV-1 DNA vaccine boosted with Ad5 vector induced CD4 and CD8 T cell immune responses to a wide range of HIV antigens. The response rate in this urban Ugandan population looks similar to that seen in the U.S. and other trials of the Vaccine Research Center’s DNA/Ad5 vaccine. The results of this trial will help with the decision to undertake phase IIb trials of this vaccine in East Africa.

P06-47
Safety and immunogenicity of the NIAID VRC multiclade HIV-1 DNA plasmid/multiclade rAd5 vector vaccine boost (HVTN 204) in South African participants

G Churchyard1, M Keefer8, C Morgan3, E Adams6, J Hural3, Z Moodie3, B Graham5, L Gu3, M McElrath3, L Bekker2, G Gray7, E Vardas7 and HIV Vaccine Trials Network4

1 Aurum Institute for Health Research, Marshalltown, St. Helena; 2 Desmond Tutu HIV Foundation, University of Cape Town, Cape Town, South Africa; 3 Fred Hutchinson Cancer Research Center, Seattle, WA, USA; 4 NIAID HIV Vaccine Trials Network, Seattle, WA, USA; 5 NIAID Vaccine Research Center, Bethesda, MD, USA; 6 NIAID, Division of AIDS, Bethesda, MD, USA; 7 Perinatal HIV Research Unit, University of the Witwatersrand, Soweto, South Africa; 8 University of Rochester Medical Center, Rochester, NY, USA

Background: Results from primate and humans studies suggest that prior immunity to adenovirus, particularly high-titer neutralizing Ad5 antibody (NAb), reduces the immune response to recombinant Ad5 HIV vaccines and may be associated with less reactogenicity. South African (SA) participants (ppts) have higher neutralizing Ad5 titers than United States (US) ppts (Ad5 NAb titers>1:1000 [Merck assay]: SA; 23.1% vs US; 12.2%). A multi- country, randomized, double-blind, placebo-controlled phase IIA clinical trial of the NIAID Vaccine Research Center’s 6-plasmid candidate DNA HIV-1 (envA, envB, envC, gagB, polB, nefB) (DNA-HIV) given IM by biojector at 0,1 and 2 months, and boosted with rAd5 HIV-1 (envA, envB, envC, gagB, polB) vaccine (Ad5-HIV) given IM at 6 months was conducted in healthy uninfected ppts. Preliminary safety and immunogenicity data for SA ppts are described. Methods: 240 SA ppts were enrolled irrespective of their baseline Ad5 titer. Half received placebo. Ppts were monitored for reactogenicity and adverse events. PBMCs were evaluated by IFN- γ ELISpot, using global Potential T cell Epitope peptide pools 6 weeks after the Ad5-HIV boost. Results: Median (range) age: 24 (18-47) years. 45% Male, 98% black. The proportion receiving vaccinations with product/placebo at 0, 1, 2 and 6 months were 100%, 96%, 93% and 88% respectively. Compared to placebo, DNA-HIV caused more local reactions (≥ mild), decreasing with subsequent injections (DNA-HIV; 70%, 47.7%, 43.2%; placebo: 42.5%, 31.3%, 33.6%), but not more systemic reactions. Ad5-HIV caused more local (≥ mild) reactions than placebo (40.6% vs 20.8%) and a similar rate of systemic reactions (3.1% vs 2.8%). Preliminary IFN- γ ELISpot data suggest acceptable responses. Conclusion: Both vaccines were well tolerated. Ad5-HIV associated systemic reactions are lower than that observed in US ppts. Preliminary IFN- γ ELISpot data suggest that the product is comparably immunogenic in South African ppts compared to US ppts.

AIDS Vaccines 2005

Safety and Immunogenicity of a Multiclade HIV-1 Recombinant Adenovirus Vaccine Boost in Prior Recipients of a Multiclade HIV-1 DNA Vaccine

Barney S. Graham, Mario Roederer, Richard A. Koup, Robert Bailer, Phillip L. Gomez, Martha Nason, Julie E. Martin, Mary E. Enama, John Mascola, Gary J. Nabel, for The VRC Clinical Trials Core, The VRC Vector Core, The VRC Vaccine Production Program and The VRC Immunology Core Lab. Vaccine Research Center, NIAID, NIH, DHHS, Bethesda, MD

Induction of HIV-1-specific T cell and antibody responses to diverse subtypes is a major goal of current vaccine efforts. We have developed a heterologous DNA prime-recombinant adenovirus vector boost approach, priming subjects with 3 doses of a 4-plasmid DNA expressing clade B gag/pol/nef and clades A, B, and C envelope constructs and boosting with 4 recombinant adenovirus serotype 5 vectors (rAd5) expressing matching genes except for the absence of nef. Subjects received 4 mg (N=4) or 8 mg (N=4) of DNA. All subjects were boosted with 1010 PU of rAd5 at a boost interval ranging from 79 to 104 weeks. Three subjects had moderate systemic symptoms, including myalgia and 1 had mild fever within 24 hours following rAd5. CD4 and CD8 T cell responses were measured by IFN-gamma ELISpot and intracellular cytokine staining for IL- 2 or IFN-gamma. Preliminary analysis showed that 6 of 8 subjects had >3-fold increase (range 3-21) in Env-specific ELISpot responses, and all subjects had robust antibody responses after rAd5 boosting. Both T cell and antibody responses were up to 30-fold higher than seen previously in rAd5 only recipients. Priming with the VRC DNA vaccine followed by the rAd5 vector was well tolerated in this small cohort of subjects. With a 20-26 month interval between prime and boost, significant T cell and antibody responses are induced by the rAd5 that exceed the highest values seen to date in subjects immunized with rAd5 alone.

Keystone Meeting 2006 (from the GenVec website) Speaker Abstract 029
Update on VRC Clinical Trials
Barney S. Graham, M.D., Ph.D.
Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892

The Vaccine Research Center (VRC) in the National Institute of Allergy and Infectious Diseases (vrc.nih.gov) is devoted to developing a vaccine for HIV. The program is mission-oriented and develops vaccine candidates for viral diseases from basic research through production and analysis of Phase I clinical trials. The initial VRC HIV vaccine candidate is based on gene delivery of vaccine antigens (clade B Gag, Pol, and Nef, and clades A, B, and C Envelope) using a combination of plasmid DNA for priming and replication-defective recombinant adenoviral vectors (rAd5) for boosting. CD4+ and CD8+ T cell responses are measured by peptide pool stimulation of PBMCs followed by IFN-(ELISpot and flow cytometric detection of intracellular IL-2 or IFN-(production. The vaccine is designed to induce T cell responses against multiple HIV proteins to diminish immune escape, and includes sequences from multiple clades to be relevant for large portion of the global epidemic. Several Phase I studies have evaluated plasmid DNA vaccine candidates, rAd5 vectors, or a combined prime-boost regimen delivered by needless injection device or needle syringe. Both DNA and rAd5 vaccines are immunogenic alone, and the combined prime-boost schedule induces HIV-specific T cell responses up to 5-10 fold higher and antibody responses several orders of magnitude higher than either modality alone. The product has now advanced into Phase II evaluation in collaboration with the HIV Vaccine Trials Network (HVTN), the U.S. Military HIV Research Program (USMHRP), and the International AIDS Vaccine Initiative (IAVI) at sites in the Americas, Caribbean, South Africa, and East Africa.

Measuring T cell Responses: Apples, Orange Pies & Interferon Gamma

As mentioned in a prior post, one of the key questions that the HIV vaccine field has to wrestle with is: what is the best method for measuring vaccine-induced HIV-specific CD4 and CD8 T cell responses? The failure of the Merck vaccine - the first T cell-based HIV vaccine to be tested for efficacy - has shone a harsh light on this question, because the construct appeared to induce reasonable T cell responses according to the most commonly used tests.

To start at the beginning, there are several important features of the T cell response:

  • Specificity: this refers to the specific parts of a pathogen that T cells are targeting. T cells recognize small slices of proteins from pathogens called epitopes via molecular docking bays on their surface called T cell receptors (TCRs).
  • Breadth: refers to how many different epitopes from a given pathogen that the T cell response is targeting (narrow=few epitopes, broad=many).
  • Function: the ability of responding T cells to perform specific functions e.g. proliferation (the ability of the T cell to copy itself), production of immune system proteins called cytokines (e.g. interferon gamma, IL-2 and TNF-alpha) and chemokines (e.g. MIP-1beta). Other functional measures are also possible such as the measurement of the ability of HIV-specific CD8 T cells to kill HIV-infected cells in a lab dish, some studies use surrogate measures of cell-killing ability (e.g. the expression of a molecule called CD107a).
  • Phenotype: A term that refers to the fact that T cells can belong to different subsets which immunologists define based on particular functional properties and expression of cell surface markers. It’s worth noting that these definitions can be a little fuzzy, and that T cells can also transition back and forth between different phenotypes depending on whether they are actively responding to something and where they are in the body (e.g. the blood vs. body tissues). Two broad subsets of memory T cells with differing properties are “central memory” T cells, which circulate in a resting state but have a prodigious ability to proliferate if they encounter the pathogen that they recognize, and “effector memory” T cells which circulate in a more activated state which is associated with rapid production of the cytokine interferon gamma but a poor ability to proliferate. Sometimes immunologists also refer to additional categories such as “transitional effector memory“ T cells (cells transitioning from central memory to effector memory subsequent to activation) and simply “effector” T cells which are so battle weary (or “terminally differentiated” in immunological parlance) that they cannot return to a resting central memory state.

For vaccine researchers, the goal is to try and understand what an ideal HIV-specific T cell response should look like, based on each of these features; e.g. which epitopes should be targeted? How broad should the response be? What are the ideal functional properties? Should the response be biased toward a particular phenotype (e.g. central vs. effector memory)?

In the run-up to the Merck trial, the leading assay for studying T cell responses was the relatively new interferon gamma (IFNg) ELISpot (Enzyme-Linked ImmunoSpot). This test quantitates T cell responses to a given epitope (or mixture of epitopes) based on their ability to make just this one cytokine. Merck and researchers from the HVTN (along with many other immunologists working in the vaccine field) put a great deal of effort into standardizing the IFNg ELISpot in order to try and ensure that results were reproducible and could be compared across trials of different candidates. Several of the large coordinating bodies in HIV vaccine research – including the Global HIV/AIDS Vaccine Enterprise and US government-sponsored Partnership for AIDS Vaccine Evaluation (PAVE) – also sponsored overlapping processes aiming to promote standardization of immunogenicity assays.

However, at the same time as these efforts were underway, researchers using a different assay called intracellular cytokine staining (ICS) showed that IFNg-producing T cells do not reflect the entire memory T cell response generated by vaccination; in fact, in Stephen De Rosa’s initial study using various licensed vaccines, IFNg-producing T cells were often in the minority compared to T cells producing other cytokines and chemokines such as IL-2. De Rosa’s work began a trend toward evaluating multiple parameters involved in T cell function, a trend that was accelerated by data showing that, in people with HIV infection, the presence of so-called “polyfunctional” CD4 and CD8 T cell responses targeting HIV is associated with control of viral load and long-term non-progression. Researchers at the NIH’s Vaccine Research Center, who are blessed to possess one of the largest multi-parameter flow cytometers in the land (a device which allows multiple different facets of a cell’s function to be analyzed simultaneously), pioneered these studies of polyfunctional T cells and thus, unsurprisingly, began to use this approach to analyze the T cell responses induced by their HIV vaccine candidate. The VRC have focused on five main T cell functions: the production of the cytokines IL-2, TNF-alpha, IFNg and the chemokine MIP-1beta, and expression of the CD107a molecule mentioned earlier. The VRC now typically present the spectrum of T cell functions they detect amongst a particular antigen-specific population in the form of pie charts, divided into the proportion of T cells elaborating a particular number of functions (e.g. blue for 1, green for 2, etc.).

The upshot of these developments is that anyone attempting to directly compare the immunogenicity of the Merck HIV vaccine and the VRC’s candidate has their work cut out (as Jerry Sadoff, a member of the AIDS Vaccine Research Subcommittee complained at their December 12 meeting). The Merck data presented and published to date primarily includes information derived from the IFNg ELISpot (with some additional ICS data regarding IL-2), while the VRC have presented ICS data addressing multiple functions as well as some IFNg ELISpot data. In both cases, there are no published data addressing the immunogenicity of the exact vaccine regimens selected for use in the efficacy trials in a systematic and detailed way; Merck has published data from a scattering of individuals who received the prototype Ad5 construct (encoding only gag) at various doses, some also after receiving a DNA priming immunization (which Merck decided not to use). The VRC has published data from the phase I trials of the DNA and Ad5 components of their regimen in separate papers in the same issue of the Journal of Infectious Diseases, but data from individuals who have received the full DNA prime/Ad5 boost immunization series is limited and has only been presented at meetings. In order to inform the HIV vaccine field – and particularly to assist those making decisions about PAVE100 - one immediate priority should be the publication of detailed information regarding the T cell responses induced by the Merck & VRC candidates that addresses their specificity, breadth, function & phenotype.

As if things weren’t complicated enough, CD8 T cell aficionado Otto Yang has recently highlighted another important issue relating to immunogenicity assays in a paper forthcoming in JID. Yang points out that the best test for CD8 T cells may be one that directly measures their ability to kill HIV-infected cells in a lab dish. In his JID paper, Yang uses such a test to show that CD8 T cells that appear to recognize HIV variants from different clades (when evaluated using IFNg ELISpot) may actually not be able to kill cells infected with those same variants. Yang argues that more direct measures of CD8 T cell efficacy should be used in vaccine evaluation, a point echoed by David Watkins in a recent article in the IAVI Report. Watkins suggests that, in some cases, using IFNg ELISpot may be equivalent to measuring non-neutralizing antibodies, while direct measures of CD8 T cell killing are more akin to a neutralization assay. Patricia D’Souza and Marcus Altfeld make a similar point in the JID commentary that accompanies Otto Yang’s report: “The accurate assessment of the antiviral activity of HIV-1-specific CD8 T cells is a crucial step toward identifying the immune correlates of vaccine efficacy. There is a tendency to consider CD8 lymphocyte responses as equivalent, perhaps in the same way that the Env-specific antibodies were once thought to be equally effective in mediating antiviral activity. It is possible that there is a hierarchy of efficacious CD8+ lymphocyte responses in which the most effective CD8 lymphocytes may be an analogue of a potent and broad neutralizing antibody.” However, assays for measuring CD8 T cell killing also vary and so – if the field does follow this path – another effort to identify, select and standardize the best method will be necessary.

Recently published papers, commentaries & opinion pieces:

The Journal of Infectious Diseases 2008;197:000–000
DOI: 10.1086/525288
EDITORIAL COMMENTARY

Measuring HIV‐1–Specific T Cell Immunity: How Valid Are Current Assays?
M. Patricia D’Souza1 and Marcus Altfeld2

1Vaccine Clinical Research Branch, Division of AIDS, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland; 2Partners AIDS Research Center, Massachusetts General Hospital, Charlestown, and Division of AIDS, Harvard Medical School, Boston

The Journal of Infectious Diseases 2008;197:000–000
DOI: 10.1086/525281
MAJOR ARTICLE

Cross-Clade Detection of HIV-1–Specific Cytotoxic T Lymphocytes Does Not Reflect Cross-Clade Antiviral Activity
Michael S. Bennett,1,3, Hwee L. Ng,2,3, Ayub Ali,2,3 and Otto O. Yang1,2,3

1Department of Microbiology, Immunology, and Molecular Genetics and 2Division of Infectious Diseases, Department of Medicine, David Geffen School of Medicine, and 3UCLA AIDS Institute, University of California, Los Angeles

Presented in part: First Annual Ugandan AIDS Conference, Kampala, Uganda, 7 December 2006.

(See the editorial commentary by D'Souza and Altfeld, on pages XXX–XX.)

The genetic divergence of human immunodeficiency virus (HIV)–1 into distinct clades is a serious consideration for cytotoxic T lymphocyte (CTL)–based vaccine development. Demonstrations that CTLs can cross‐recognize epitope sequences from different clades has been proposed as offering hope for a single vaccine. Cross‐clade CTL data, however, have been generated by assessing recognition of exogenous peptides. The present study compares HIV-1–specific CTL cross-clade epitope recognition of exogenously loaded peptides with suppression of HIV‐1–infected cells. Despite apparently broad cross-clade reactivity of CTLs against the former, CTL suppression of HIV-1 strains with corresponding epitope sequences is significantly impaired. The functional avidity of CTLs for nonautologous clade epitope sequences is diminished, suggesting that CTLs can fail to recognize levels of infected endogenously derived cell-surface epitopes despite recognizing supraphysiologic exogenously added epitopes. These data strongly support clade-specific antiviral activity of CTLs and call into question the validity of standard methods for assessing cross-clade CTL activity or CTL antiviral activity in general.

AIDS:Volume 22(3)30 January 2008p 325-331
[OPINION]

Aiming for successful vaccine-induced HIV-1-specific cytotoxic T lymphocytes
Yang, Otto O

From the Division of Infectious Diseases, Department of Medicine and Department of Microbiology, Immunology, and Molecular Genetics, UCLA AIDS Institute, David Geffen School of Medicine at UCLA, Los Angeles, California, 90095, USA.

JVI Accepts, published online ahead of print on 7 November 2007
J. Virology doi:10.1128/JVI.01634-07
REVIEW

HIV-1 Vaccine Development: Recent Advances in the CTL Platform "Spotty Business"
Kimberly A. Schoenly and David B. Weiner

The Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine

The Journal of Experimental Medicine, Vol. 205, No. 1, 7-12
Published online 14 January 2008
doi:10.1084/jem.20072681
COMMENTARY

The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development?
Rafick-Pierre Sekaly

R.-P. Sekaly is at Université de Montréal, CR-CHUM, Institut National de la Santé et de la Recherche Médicale U743, Montréal, Québec H2X1P1, Canada

The world of human immunodeficiency virus (HIV) vaccines has suffered a baffling setback. The first trial of a vaccine designed to elicit strong cellular immunity has shown no protection against infection. More alarmingly, the vaccine appeared to increase the rate of HIV infection in individuals with prior immunity against the adenovirus vector used in the vaccine. A new study in this issue suggests that a different vaccine approach—using a DNA prime/poxvirus boost strategy—induces polyfunctional immune responses to an HIV immunogen. The disappointing results of the recent vaccine trial suggest that a more thorough assessment of vaccine-induced immune responses is urgently needed, and that more emphasis should be placed on primate models before efficacy trials are undertaken.

Probing HIV's Dependence on Host Proteins

An important new study has just been published in Science Express, the advance online section of the widely read journal Science. Abraham Brass and colleagues report results obtained using a genome-wide screen for host proteins necessary for HIV replication. The researchers used an approach that involves blocking the activity of known human genes using small slices of RNA called small interfering RNAs (siRNAs). A staggering 21,121 pools of four siRNAs per gene were employed in the study, ultimately revealing 273 host proteins that appear necessary for efficient HIV replication (the researchers have dubbed them "HIV dependency factors" or HDFs).

Thirty-six HDFs comprise previously reported factors such as the CD4 and CXCR4 proteins, but the others are novel, including proteins involved in transporting materials into a cell's nucleus, glycosylation (addition of sugar molecules to proteins) and degradation of cellular proteins (autophagy). One identified protein, ZNRD1, was also implicated in a recent study of genomic associations with viral load set point in people with HIV (mutations in the gene for ZNRD1 were associated with slow progression). So much data was generated that much of it is not in the paper but in the supplemental online material that accompanies it. The authors also offer a busy schematic that gives a sense of the complex theater of virus-host interactions that they have raised the curtain on (click on the thumbnail for a larger image):
Brassimage



CREDIT: A. L. BRASS ET AL., SCIENCE

In an accompanying news story by Jon Cohen, a number of leading HIV researchers praise the paper and note that it offers a dazzling array of potential new leads for scientists looking to better understand the HIV life cycle, and how to inhibit it.

Published Online January 10, 2008
Science DOI: 10.1126/science.1152725

Submitted on November 7, 2007
Accepted on December 21, 2007

Identification of Host Proteins Required for HIV Infection Through a Functional Genomic Screen

Abraham L. Brass 1, Derek M. Dykxhoorn 2{dagger}, Yair Benita 3{dagger}, Nan Yan 2, Alan Engelman 4, Ramnik J. Xavier 5, Judy Lieberman 2, Stephen J. Elledge 6*

1 Department of Genetics, Center for Genetics and Genomics, Brigham and Women’s Hospital, Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA.; Gastrointestinal Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.
2 Immune Disease Institute and Department of Pediatrics, Harvard Medical School, Boston, MA 02115, USA.
3 Center for Computational and Integrative Biology, Harvard Medical School, Boston, MA 02114, USA.
4 Dana-Farber Cancer Institute, Division of AIDS, Harvard Medical School, Boston, MA 02115, USA.
5 Gastrointestinal Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA.; Center for Computational and Integrative Biology, Harvard Medical School, Boston, MA 02114, USA.
6 Department of Genetics, Center for Genetics and Genomics, Brigham and Women’s Hospital, Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA.

{dagger}These authors contributed equally to this work.

HIV-1 exploits multiple host proteins during infection. We performed a large-scale siRNA screen to identify host factors required by HIV-1 and identified over 250 HIV-dependency factors (HDFs). These proteins participate in a broad array of cellular functions and implicate new pathways in the viral life cycle. Further analysis revealed previously unknown roles for retrograde Golgi transport proteins (Rab6 and Vps53) in viral entry, a karyopherin (TNPO3) in viral integration, and the Mediator complex (Med28) in viral transcription. Transcriptional analysis revealed that HDF genes were enriched for high expression in immune cells suggesting that viruses evolve in host cells that optimally perform the functions required for their life cycle. This effort illustrates the power with which RNA interference and forward genetics can be used to expose the dependencies of human pathogens such as HIV, and in so doing identify potential targets for therapy.

Multiple Roles of CCR5 in Infectious Diseases

Three free access papers from the online first section of the Journal of Infectious Diseases. The articles highlight the role of CCR5 - better known as a co-receptor for HIV entry into cells - in T cell trafficking to sites of infection and suggest that studies are needed to evaluate the effects of pharmacological inhibition of CCR5 in these settings.

A Moving Target: The Multiple Roles of CCR5 in Infectious Diseases
Robyn S. Klein

Genetic Deficiency of Chemokine Receptor CCR5 Is a Strong Risk Factor for Symptomatic West Nile Virus Infection: A Meta‐Analysis of 4 Cohorts in the US Epidemic
Jean K. Lim, Christine Y. Louie, Carol Glaser, Cynthia Jean, Bernard Johnson, Hope Johnson, David H. McDermott, and Philip M. Murphy

A Deletion in the Chemokine Receptor 5 (CCR5) Gene Is Associated with Tickborne Encephalitis
Elin Kindberg, Auksė Mickienė, Cecilia Ax, Britt Åkerlind, Sirkka Vene, Lars Lindquist, Åke Lundkvist, and Lennart Svensson

Adenovirus-Specific T Cell Immunity

One of the yawning information gaps highlighted by the Merck HIV vaccine trial is the absence of data regarding the impact of vaccination on adenovirus-specific T cell immune responses. Although it was logical for researchers to focus on the HIV-specific T cell responses induced by the vaccine, in retrospect it was an oversight to not pay attention to the effect of the vector on adenovirus-specific T cells, particularly CD4 T cells which are potential targets for HIV infection.

The literature on adenovirus-specific T cell immunity is relatively sparse, but the published data indicates:

  • Adenovirus-specific T cell responses are detectable in the majority of individuals studied
  • Responses are biased toward CD4 T cells with an effector memory phenotype
  • Adenovirus-specific CD4 T cell responses are generally of a high magnitude but wane with age
  • Adenovirus-specific CD4 T cells recognize epitopes that are conserved across adenovirus serotypes, including epitopes that are present even in Ad5 vectors with multiple gene deletions

Taken together, the published data certainly suggests that studies of the impact of Merck’s Ad5 vector on adenovirus-specific CD4 T cells should be a priority in the ongoing effort to understand the outcome of the Merck HIV vaccine trial.

J. Virol. 2008 Jan;82(1):546-54. Epub 2007 Oct 17.

Identification of hexon-specific CD4 and CD8 T-cell epitopes for vaccine and immunotherapy.

Leen AM, Christin A, Khalil M, Weiss H, Gee AP, Brenner MK, Heslop HE, Rooney CM, Bollard CM.

Center for Cell and Gene Therapy, Baylor College of Medicine, 6621 Fannin Street, MC 3-3320, Houston, TX 77030, USA.

Adenoviral infections in the immunocompromised host are associated with significant morbidity and mortality. Although the adoptive transfer of adenovirus-specific T cells may prevent and treat such infections, the T-cell immune response to the multiplicity of adenovirus serotypes and subspecies that infect humans has not been well characterized, impeding the development of such approaches. We have, therefore, analyzed the specificities of T-cell responses to the viral capsid hexon antigen, since this structure is highly conserved in human pathogens. We screened 25 human cytotoxic T-cell lines with adenovirus specificity to extensively characterize their responses to adenoviral hexon and to identify a panel of novel CD4(+) and CD8(+) T-cell epitopes. Using a peptide library spanning the entire sequence of the hexon protein, we confirmed the responsiveness of these cytotoxic T-cell lines to seven peptides described previously and also identified 33 new CD4- or CD8-restricted hexon epitopes. Importantly, the majority of these epitopes were shared among different adenovirus subspecies, suggesting that T cells with such specificities could recognize and be protective against multiple serotypes, simplifying the task of effective adoptive transfer or vaccine-based immunotherapy for treating infection by this virus.

J Gen Virol. 2007 Sep;88(Pt 9):2417-25.

The CD4+ T-cell response to adenovirus is focused against conserved residues within the hexon protein.

Onion D, Crompton LJ, Milligan DW, Moss PA, Lee SP, Mautner V.

CRUK Institute for Cancer Studies, University of Birmingham, Birmingham B15 2TT, UK.

Adenovirus is a significant pathogen in immunocompromised patients and is widely utilized as a gene delivery vector, so a detailed understanding of the human immune response to adenovirus infection is critical. This study characterized the adenovirus-specific CD4(+) T-cell response of healthy donors by incubation with whole virus or with individual hexon and fiber proteins. Adenovirus-specific CD4(+) T cells averaged 0.26 % of the CD4(+) T-cell pool and were detectable in all donors. T cells recognizing the highly conserved hexon protein accounted for 0.09 %, whereas no response was observed against the fiber protein. A panel of hexon-specific CD4(+) T-cell clones was generated and shown to lyse targets infected with adenovirus from different serotypes and species. Three CD4 T-cell epitopes are described, which map to highly conserved regions of the hexon protein.

Br J Haematol. 2007 Jan;136(1):117-26. Epub 2006 Nov 8.

Capture and generation of adenovirus specific T cells for adoptive immunotherapy.

Chatziandreou I, Gilmour KC, McNicol AM, Costabile M, Sinclair J, Cubitt D, Campbell JD, Kinnon C, Qasim W, Gaspar HB.

Molecular Immunology Unit, Institute of Child Health, University College London, London, UK.

Adenoviral infections represent a major cause of morbidity and mortality following haematopoietic stem cell transplantation. Current anti-viral agents are virostatic and it is evident that elimination of adenovirus (ADV) infection is only achieved by recovery of cellular immunity. Using an interferon-gamma (IFN-gamma) secretion and capture assay to isolate ADV-specific T cells, followed by a 2 week expansion and restimulation protocol, we generated ADV T cells that may be used for cellular immunotherapy. In contrast to virus-specific T cells for cytomegalovirus or Epstein-Barr virus, the ADV response was dominated by CD4(+) T cells and the majority of captured cells exhibited an effector/memory immunophenotype. Highly specific antigen responses were demonstrated by intracellular IFN-gamma expression and cytotoxicity assays when the expanded cells underwent restimulation with ADV-pulsed target cells. Although T cells were initially generated in response to ADV species C, the expanded populations also showed strong activity against ADV species B, suggesting cross-reactivity across ADV species; a finding that has important clinical consequences in the paediatric setting, where the majority of infections are caused by ADV type B and C. The protocols can be readily translated to generate ADV-specific T cells suitable for clinical use and offer an effective immunotherapeutic strategy to control ADV infection.

Int Immunol. 2006 Nov;18(11):1521-9. Epub 2006 Sep 5.

Novel pan-DR-binding T cell epitopes of adenovirus induce pro-inflammatory cytokines and chemokines in healthy donors.

Haveman LM, Bierings M, Legger E, Klein MR, de Jager W, Otten HG, Albani S, Kuis W, Sette A, Prakken BJ.

Department of Pediatric Immunology and Hematology, Wilhelmina Children's Hospital, University Medical Center, KC.03.063.0, Lundlaan 6, Postbus 85090, 3508 AB, Utrecht, The Netherlands.

Adenovirus can cause fatal infections in the immunocompromised host. To date, no effective anti-viral therapy is available. Adoptive therapy with adenovirus-specific T cells could be a promising treatment, but requires the identification of such T cells. Aim of this study was to identify conserved adenoviral T cell epitopes recognized in a majority of healthy individuals. By using a computer algorithm designed to predict pan-HLA-DR-binding T cell epitopes, we selected 19 peptides of adenovirus serotype 5. PBMCs from 26 healthy subjects were isolated and incubated with these peptides to test epitope-specific T cell proliferation. Six epitopes derived from E1B protein, hexon protein (two epitopes), DNA polymerase, E3A glycoprotein and fiber protein induced a proliferative T cell response in the majority of healthy controls. In vitro MHC binding assays confirmed the potential capacity of the adenovirus epitopes to bind multiple MHC alleles. The cytokine and chemokine profile induced by these epitopes was determined with a multiplex immunoassay and revealed a predominant pro-inflammatory pattern. Based on the broad recognition and the induced cytokine and chemokine profile, the detected epitopes can be regarded as potential candidates to select adenovirus-specific T cells for immune intervention in the immunocompromised host.

J Virol. 2003 Jun;77(11):6562-6. (free access to full text)

Extensive cross-reactivity of CD4+ adenovirus-specific T cells: implications for immunotherapy and gene therapy.

Heemskerk B, Veltrop-Duits LA, van Vreeswijk T, ten Dam MM, Heidt S, Toes RE, van Tol MJ, Schilham MW.

Department of Pediatrics, Leiden University Medical Center, The Netherlands.

Adenovirus (Ad)-specific T-cell responses in healthy adult donors were investigated. Ad5, inactivated by methylene blue plus visible light, induced proliferation and gamma interferon (IFN-gamma) production in peripheral blood mononuclear cells of the majority of donors. Responding T cells were CD4(+) and produced IFN-gamma upon restimulation with infectious Ad5 and Ads of different subgroups. T-cell clones showed distinct cross-reactivity patterns recognizing Ad serotypes from either one subgroup (C), two subgroups (B and C), or three subgroups (A, B, and C). This cross-reactivity of Ad-specific T cells has relevance both for Ad-based gene therapy protocols, as well as for the feasibility of T-cell-mediated adoptive immunotherapy in recipients of an allogeneic stem cell transplantation.

Hum Gene Ther. 2002 Jul 1;13(10):1167-78.

The adenovirus capsid protein hexon contains a highly conserved human CD4+ T-cell epitope.

Olive M, Eisenlohr L, Flomenberg N, Hsu S, Flomenberg P.

Center of Human Virology and Department of Medicine, Thomas Jefferson University, Philadelphia, PA 19107, USA.

The immunogenicity of adenovirus vectors remains a major obstacle to their safe and efficacious use for gene therapy. In order to identify T-cell epitopes directly from adenoviruses, four viral protein sequences were screened for the well-characterized 9-mer HLA-A2 binding motif. Peripheral blood mononuclear cells (PBMC) from healthy adults were tested for responses to 17 selected viral peptides using a short-term interferon-gamma ELISPOT assay. Memory T-cell responses were identified to a single peptide derived from the major capsid protein hexon in 5 of 6 HLA-A2-positive donors. Unexpectedly, responses to this hexon peptide were also detected in 4 of 6 HLA-A2-negative donors, and responder cells were identified as CD4(+) T cells by immunomagnetic depletion experiments. A longer 15-mer peptide, H910-924, was identified as the optimal CD4(+) T-cell epitope. This hexon epitope induces strong proliferative T-cell responses that can be blocked by a monoclonal antibody against HLA-DR, and molecular HLA typing of donors suggests that the peptide response is restricted by multiple HLA-DR alleles. Additionally, quantitative analysis of responses to H910-924 and whole adenovirus reveals that the frequency of circulating CD4(+) T cells specific for this single hexon epitope (mean = 61 per 10(6) PBMC) represents up to one third of the total adenovirus-specific T-cell response. Finally, comparison of hexon sequences from over 20 different human adenovirus serotypes indicates that H910-924 is highly conserved. In most individuals, therefore, T-cell responses to this hexon epitope will be induced by all adenovirus vectors, including "gutted" vectors packaged with capsid proteins and vectors based on different serotypes.

J Infect Dis. 2002 May 15;185(10):1379-87. Epub 2002 Apr 30. (free access to full text)

Age-related decrease in adenovirus-specific T cell responses.

Sester M, Sester U, Alarcon Salvador S, Heine G, Lipfert S, Girndt M, Gärtner B, Köhler H.

Medical Department IV, Institute of Medical Microbiology and Hygiene, University of the Saarland, Homburg, Germany.

Infections with persistent viruses, such as cytomegalovirus (CMV) or adenovirus, are not, in general, clinically apparent but may cause serious complications in the immunocompromised host. As has been shown for CMV, the cellular arm of the immune response is essential in controlling viral replication. However, cellular immunity toward adenoviruses has not been well characterized in humans. The aim of the present study was the quantitative and functional analysis of adenovirus-specific T cell responses from 171 healthy individuals and 59 long-term renal transplant recipients by use of flow-cytometric, as well as standard proliferation and enzyme-linked immunosorbant, assays. Adenovirus-specific immunity is dominated by CD4 T cells with memory/effector phenotype. Of interest, the frequency of adenovirus-specific T cells decreases significantly with age. This age-related decline indicates the eventual elimination of adenoviruses within a lifetime that may explain the well-known clinical observation of a predominant incidence of adenoviral complications in children and young adults, compared with older adults, after transplantation.

Viral Immunol. 2001;14(4):403-13.

Quantitative analysis of adenovirus-specific CD4+ T-cell responses from healthy adults.

Olive M, Eisenlohr LC, Flomenberg P.

Department of Medicine, Center for Human Virology, Thomas Jefferson University, Philadelphia, Pennsylvania 19107, USA.

Although nearly all adults are seropositive for adenoviruses, little is known about the cellular immune responses to these ubiquitous pathogens. We have previously identified adenovirus-specific proliferative T-cell responses in peripheral blood mononuclear cells (PBMC) from healthy adults. In this study, memory T-cell responses to adenovirus were further evaluated in healthy adult donors using a short term, quantitative enzyme-linked immunospot assay (ELISPOT) assay. Adenovirus antigen induced specific secretion of interferon-gamma (IFN-gamma) from PBMC within 12 hours of incubation. PBMC from 20 of 22 healthy donors (90.9%) expressed IFN-y in response to adenovirus. Responder cells were identified as CD4+ T cells by immunomagnetic depletion methods. Interleukin-4 (IL-4) secretion was not detected, consistent with a TH1 response. There was a 10-fold variation in the frequencies of adenovirus-specific CD4+ T cells between donors (range, 34 to 294; median, 122 per million PBMC). Adenovirus-specific T cell frequencies remained stable over periods up to 2 years among individual donors, but there was an inverse correlation between frequency and donor age. These quantitative data suggest that most adults retain adenovirus-specific cellular memory after childhood exposure. This assay may be useful for the evaluation of adenovirus-specific CD4+ T-cell responses in patients treated with adenovirus gene therapy vectors and the identification of major T-cell epitopes.