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Development of a Sendai virus vector-based AIDS vaccine inducing T cell responses

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References

  • Papers of special note have been highlighted as:
  • * Of interest
  • ** Of considerable interest
  • McMichael A. T cell responses and viral escape. Cell. 1998;93(5):673–676.
  • Richman DD, Wrin T, Little SJ, et al. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci USA. 2003;100(7):4144–4149.
  • Wei X, Decker JM, Wang S, et al. Antibody neutralization and escape by HIV-1. Nature. 2003;422(6929):307–312.
  • Trkola A, Kuster H, Rusert P, et al. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med. 2005;11(6):615–622.
  • Hütter G, Nowak D, Mossner M, et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med. 2009;360(7):692–698.
  • Berzofsky JA, Ahlers JD, Belyakov IM. Strategies for designing and optimizing new generation vaccines. Nat Rev Immunol. 2001;1(3):209–219.
  • Gilbert PB, Peterson ML, Follmann D, et al. Correlation between immunologic responses to a recombinant glycoprotein 120 vaccine and incidence of HIV-1 infection in a phase 3 HIV-1 preventive vaccine trial. J Infect Dis. 2005;191(5):666–677.
  • Pitisuttithum P, Gilbert P, Gurwith M, et al. Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J Infect Dis. 2006;194(12):1661–1671.
  • Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med. 2009;361(23):2209–2220.
  • Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med. 2012;366(14):1275–1286.
  • Tomaras GD, Ferrari G, Shen X, et al. Vaccine-induced plasma IgA specific for the C1 region of the HIV-1 envelope blocks binding and effector function of IgG. Proc Natl Acad Sci USA. 2013;110(22):9019–9024.
  • Kwong PD, Mascola JR, Nabel GJ. Rational design of vaccines to elicit broadly neutralizing antibodies to HIV-1. Cold Spring Harb Perspect Med. 2011;1:a007278.
  • Burton DR, Ahmed RA, Barouch DH, et al. A blueprint for HIV vaccine discovery. Cell Host Microbe. 2012;12:396–407.
  • Koup RA, Safrit JT, Cao Y, et al. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol. 1994;68(7):4650–4655.
  • Borrow P, Lewicki H, Hahn BH, et al. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol. 1994;68(9):6103–6110.
  • Matano T, Shibata R, Siemon C, et al. Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol. 1998;72(1):164–169.
  • Barouch DH, Santra S, Schmitz JE, et al. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science. 2000;290(5491):486–492.
  • Amara RR, Villinger F, Altman JD, et al. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science. 2001;292(5514):69–74.
  • Belyakov IM, Hel Z, Kelsall B, et al. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat Med. 2001;7(12):1320–1326.
  • Matano T, Kano M, Nakamura H, et al. Rapid appearance of secondary immune responses and protection from acute CD4 depletion after a highly pathogenic immunodeficiency virus challenge in macaques vaccinated with a DNA prime/Sendai virus vector boost regimen. J Virol. 2001;75(23):11891–11896.
  • Rose NF, Marx PA, Luckay A, et al. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell. 2001;106(5):539–549.
  • Shiver JW, Fu TM, Chen L, et al. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature. 2002;415(6869):331–335.
  • Horton H, Vogel TU, Carter DK, et al. Immunization of rhesus macaques with a DNA prime/modified vaccinia virus ankara boost regimen induces broad simian immunodeficiency virus (SIV)-specific T-cell responses and reduces initial viral replication but does not prevent disease progression following challenge with pathogenic SIVmac239. J Virol. 2002;76(14):7187–7202.
  • Feinberg MB, Moore JP. AIDS vaccine models: challenging challenge viruses. Nat Med. 2002;8(3):207–210.
  • Matano T, Kobayashi M, Igarashi H, et al. Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J Exp Med. 2004;199(12):1709–1718.

* This is the first report indicating virus control by a T-cell-based vaccine in a macaque AIDS model of SIVmac239 infection.

  • Wilson NA, Reed J, Napoe GS, et al. Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J Virol. 2006;80(12):5875–5885.
  • Liu J, O’Brien KL, Lynch DM, et al. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature. 2009;457:87–91.
  • Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature. 2011;473(7348):523–527.

** This study indicated the potential of CMV vectors to induce durable antigen-specific effector T cells effective against SIV infection.

  • Townsend AR, Rothbard J, Gotch FM, et al. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell. 1986;44(6):959–968.
  • Whitney JB, Ruprecht RM. Live attenuated HIV vaccines: pitfalls and prospects. Curr Opin Infect Dis. 2004;17(1):17–26.
  • Egan MA, Pavlat WA, Tartaglia J, et al. Induction of human immunodeficiency virus type 1 (HIV-1)-specific cytolytic T lymphocyte responses in seronegative adults by a nonreplicating, host-range-restricted canarypox vector (ALVAC) carrying the HIV-1MN.env gene. J Infect Dis. 1995;171(6):1623–1627.
  • Kent SJ, Zhao A, Best SJ, et al. Enhanced T-cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant fowlpox virus. J Virol. 1998;72(12):10180–10188.
  • Hanke T, Samuel RV, Blanchard TJ, et al. Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA prime-modified vaccinia virus Ankara boost vaccination regimen. J Virol. 1999;73(9):7524–7532.
  • Earl PL, Wyatt LS, Montefiori DC, et al. Comparison of vaccine strategies using recombinant env-gag-pol MVA with or without an oligomeric Env protein boost in the SHIV rhesus macaque model. Virology. 2002;294(2):270–281.
  • Mossman SP, Bex F, Berglund P, et al. Protection against lethal simian immunodeficiency virus SIVsmmPBj14 disease by a recombinant Semliki Forest virus gp160 vaccine and by a gp120 subunit vaccine. J Virol. 1996;70(3):1953–1960.
  • Caley IJ, Betts MR, Irlbeck DM, et al. Humoral, mucosal, and cellular immunity in response to a human immunodeficiency virus type 1 immunogen expressed by a Venezuelan equine encephalitis virus vaccine vector. J Virol. 1997;71(4):3031–3038.
  • Xin KQ, Urabe M, Yang J, et al. A novel recombinant adeno-associated virus vaccine induces a long-term humoral immune response to human immunodeficiency virus. Hum Gene Ther. 2001;12(9):1047–1061.
  • Kano M, Matano T, Nakamura H, et al. Elicitation of protective immunity against simian immunodeficiency virus infection by a recombinant Sendai virus expressing the Gag protein. Aids. 2000;14(9):1281–1282.
  • Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet. 2008;372(9653):1881–1893.

* This study reported that a clinical trial of an adenovirus type 5 vector AIDS vaccine failed to show efficacy, rather suggesting a possibility of enhancing HIV infection.

  • Duerr A, Huang Y, Buchbinder S, et al. Extended follow-up confirms early vaccine-enhanced risk of HIV acquisition and demonstrates waning effect over time among participants in a randomized trial of recombinant adenovirus HIV vaccine (Step Study). J Infect Dis. 2012;206(2):258–266.
  • Perreau M, Pantaleo G, Kremer EJ. Activation of a dendritic cell-T cell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells. J Exp Med. 2008;205(12):2717–2725.
  • Li H, Rhee EG, Masek-Hammerman K, et al. Adenovirus serotype 26 utilizes CD46 as primary cellular receptor and only transiently activates T lymphocytes following vaccination of rhesus monkeys. J Virol. 2012;86(19):10862–10865.
  • Baden LR, Liu J, Li H, et al. Induction of HIV-1-specific mucosal immune responses following intramuscular recombinant adenovirus serotype 26 HIV-1 vaccination of humans. J Infect Dis. 2015;211(4):518–528.
  • Keefer MC, Gilmour J, Hayes P, et al. Phase I double blind, placebo-controlled, randomized study of a multigenic HIV-1 adenovirus subtype 35 vector vaccine in healthy uninfected adults. PLoS ONE. 2012;7(8):e41936.
  • Hansen SG, Sacha JB, Hughes CM, et al. Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science. 2013;340(6135):1237874.
  • Slobod KS, Shenep JL, Luján-Zilbermann J, et al. Safety and immunogenicity of intranasal murine parainfluenza virus type 1 (Sendai virus) in healthy human adults. Vaccine. 2004;22:3182–3186.
  • Takeda A, Igarashi H, Nakamura H, et al. Protective efficacy of an AIDS vaccine, a single DNA priming followed by a single booster with a recombinant replication-defective Sendai virus vector, in a macaque AIDS model. J Virol. 2003;77(17):9710–9715.
  • Kawada M, Tsukamoto T, Yamamoto H, et al. Long-term control of simian immunodeficiency virus replication with central memory CD4+ T-cell preservation after nonsterile protection by a cytotoxic T-lymphocyte-based vaccine. J Virol. 2007;81(10):5202–5211.
  • Naruse TK, Chen Z, Yanagida R, et al. Diversity of MHC class I genes in Burmese-origin rhesus macaques. Immunogenetics. 2010;62(9):601–611.
  • Nomura T, Yamamoto H, Shiino T, et al. Association of major histocompatibility complex class I haplotypes with disease progression after simian immunodeficiency virus challenge in burmese rhesus macaques. J Virol. 2012;86(12):6481–6490.
  • Kawada M, Igarashi H, Takeda A, et al. Involvement of multiple epitope-specific cytotoxic T-lymphocyte responses in vaccine-based control of simian immunodeficiency virus replication in rhesus macaques involvement of multiple epitope-specific cytotoxic T-lymphocyte responses in vaccine-based control of simian immunodeficiency virus replication in rhesus macaques. J Virol. 2006;80(4):1949–1958.
  • Kawada M, Tsukamoto T, Yamamoto H, et al. Gag-specific cytotoxic T-lymphocyte-based control of primary simian immunodeficiency virus replication in a vaccine trial. J Virol. 2008;82(20):10199–10206.
  • Hara H, Hara H, Hironaka T, et al. Prevalence of specific neutralizing antibodies against Sendai virus in populations from different geographic areas: Implications for AIDS vaccine development using Sendai virus vectors. Hum Vaccin. 2011;7(6):639–645.
  • Moriya C, Horiba S, Inoue M, et al. Antigen-specific T-cell induction by vaccination with a recombinant Sendai virus vector even in the presence of vector-specific neutralizing antibodies in rhesus macaques. Biochem Biophys Res Commun. 2008;371(4):850–854.
  • Moriya C, Horiba S, Kurihara K, et al. Intranasal Sendai viral vector vaccination is more immunogenic than intramuscular under pre-existing anti-vector antibodies. Vaccine. 2011;29(47):8557–8563.

* This study revealed that intranasal SeV vector vaccination is more immunogenic than intramuscular in the presence of anti-vector NAb responses.

  • Karita E, Anzala O, Gazzard B, et al. Clinical safety and immunogenicity of two HIV vaccines SeV-G (NP) and Ad35-GRIN in HIV uninfected, healthy adult volunteers. AIDS Res Hum Retroviruses. 2014;30(Suppl 1):A85
  • Rolland M, Tovanabutra S, Allan C, et al. Genetic impact of vaccination on breakthrough HIV-1 sequences from STEP trial. Nat Med. 2011;17(3):366–371.
  • Karpenko LI, Bazhan SI, Antonets DV, et al. Novel approaches in polyepitope T-cell vaccine development against HIV-1. Expert Rev Vaccines. 2014;13(1):155–173.
  • Fischer W, Perkins S, Theiler J, et al. Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat Med. 2007;13(1):100–106.
  • Barouch DH, O’Brien KL, Simmons NL, et al. Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat Med. 2010;16(3):319–323.
  • Santra S, Liao HX, Zhang R, et al. Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat Med. 2010;16(3):324–328.
  • Santra S, Muldoon M, Watson S, et al. Breadth of cellular and humoral immune responses elicited in rhesus monkeys by multi-valent mosaic and consensus immunogens. Virology. 2012;428(2):121–127.
  • Létourneau S, Im EJ, Mashishi T, et al. Design and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS One. 2007;2(10):e984.

* This reported conserved elements as a novel HIV vaccine immunogen.

  • Rolland M, Nickle DC, Mullins JI. HIV-1 group M conserved elements vaccine. PLoS Pathog. 2007;3(11):e157.
  • Kulkarni V, Valentin A, Rosati M, et al. HIV-1 conserved elements p24CE DNA vaccine induces humoral immune responses with broad epitope recognition in macaques. PLoS One. 2014;9(10):e111085.
  • Zuñiga R, Lucchetti A, Galvan P, et al. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J Virol. 2006;80(6):3122–3125.
  • Kiepiela P, Ngumbela K, Thobakgale C, et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med. 2007;13(1):46–53.
  • Ishii H, Kawada M, Tsukamoto T, et al. Impact of vaccination on cytotoxic T lymphocyte immunodominance and cooperation against simian immunodeficiency virus replication in rhesus macaques. J Virol. 2012;86(2):738–745.
  • Iwamoto N, Takahashi N, Seki S, et al. Control of simian immunodeficiency virus replication by vaccine-induced Gag- and Vif-specific CD8+ T cells. J Virol. 2014;88(1):425–433.
  • Janssen EM, Lemmens EE, Wolfe T, et al. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature. 2003;421(6925):852–856.
  • Shedlock DJ, Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science. 2003;300(5617):337–339.
  • Sun J, Bevan M. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science. 2003;300(5617):339–342.
  • Vaccari M, Mattapallil J, Song K, et al. Reduced protection from simian immunodeficiency virus SIVmac251 infection afforded by memory CD8+ T cells induced by vaccination during CD4+ T-cell deficiency. J Virol. 2008;82(19):9629–9638.
  • Yi JS, Du M, Zajac AJ. A vital role for interleukin-21 in the control of a chronic viral infection. Science. 2009;324(5934):1572–1576.
  • Elsaesser H, Sauer K, Brooks DG. IL-21 is required to control chronic viral infection. Science. 2009;324(5934):1569–1572.
  • Fröhlich A, Kisielow J, Schmitz I, et al. IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science. 2009;324(5934):1576–1580.
  • Chevalier MF, Jülg B, Pyo A, et al. HIV-1-specific interleukin-21+ CD4+ T cell responses contribute to durable viral control through the modulation of HIV-specific CD8+ T cell function. J Virol. 2011;85(2):733–741.
  • Rosenberg ES, Billingsley JM, Caliendo AM, et al. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science. 1997;278(5342):1447–1450.
  • Schieffer M, Jessen HK, Oster AF, et al. Induction of Gag-specific CD4 T cell responses during acute HIV infection is associated with improved viral control. Virol. 2014;88(13):7357–7366.
  • Malhotra U, Holte S, Dutta S, et al. Role for HLA class II molecules in HIV-1 suppression and cellular immunity following antiretroviral treatment. J Clin Invest. 2001;107(4):505–517.
  • Julg B, Moodley ES, Qi Y, et al. Possession of HLA class II DRB1*1303 associates with reduced viral loads in chronic HIV-1 clade C and B infection. J Infect Dis. 2011;203(6):803–809.
  • Ranasinghe S, Cutler S, Davis I, et al. Association of HLA-DRB1-restricted CD4+ T cell responses with HIV immune control. Nat Med. 2013;19(7):930–933.
  • Soghoian DZ, Jessen H, Flanders M, et al. HIV-specific cytolytic CD4 T cell responses during acute HIV infection predict disease outcome. Sci Transl Med. 2012;4(123):123ra25.
  • Sacha JB, Giraldo-Vela JP, Buechler MB, et al. Gag- and Nef-specific CD4+ T cells recognize and inhibit SIV replication in infected macrophages early after infection. Proc Natl Acad Sci U S A. 2009;106(24):9791–9796.
  • de Souza MS, Ratto-Kim S, Chuenarom W, et al. The Thai phase III trial (RV144) vaccine regimen induces T cell responses that preferentially target epitopes within the V2 region of HIV-1 envelope. J Immunol. 2012;188(10):5166–5176.
  • Veazey RS, Tham IC, Mansfield KG, et al. Identifying the target cell in primary simian immunodeficiency virus (SIV) infection: highly activated memory CD4(+) T cells are rapidly eliminated in early SIV infection in vivo. J Virol. 2000;74(1):57–64.
  • Mattapallil JJ, Douek DC, Hill B, et al. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature. 2005;434(7037):1093–1097.
  • Li Q, Duan L, Estes JD, et al. Peak SIV replication in resting memory CD4+ T cells depletes gut lamina propria CD4+ T cells. Nature. 2005;434(7037):1148–1152.
  • Douek DC, Brenchley JM, Betts MR, et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature. 2002;417(6884):95–98.
  • Benlahrech A, Harris J, Meiser A, et al. Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1. Proc Natl Acad Sci U S A. 2009;106(47):19940–19945.
  • Hutnick NA, Carnathan DG, Dubey SA, et al. Baseline Ad5 serostatus does not predict Ad5 HIV vaccine-induced expansion of adenovirus-specific CD4+ T cells. Nat Med. 2009;15(8):876–878.
  • McElrath MJ, De Rosa SC, Moodie Z, et al. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet. 2008;372(9653):1894–1905.
  • O’Brien KL, Liu J, King SL, et al. Adenovirus-specific immunity after immunization with an Ad5 HIV-1 vaccine candidate in humans. Nat Med. 2009;15(8):873–875.
  • Terahara K, Ishii H, Nomura T, et al. Vaccine-induced CD107a+ CD4+ T cells are resistant to depletion following AIDS virus infection. J Virol. 2014;88(24):14232–14240.

** This study revealed that vaccine-induced CD107a− CD4+ T cells are depleted in the acute phase postinfection, but CD107a+ CD4+ T cells are resistant to the depletion in a macaque AIDS model.

  • Tsukamoto T, Takeda A, Yamamoto T, et al. Impact of cytotoxic-T-lymphocyte memory induction without virus-specific CD4+ T-Cell help on control of a simian immunodeficiency virus challenge in rhesus macaques. J Virol. 2009;83(18):9339–9346.

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