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

Expert Review of Vaccines

Volumn 15, Issue 1, 2016, Pages 119-127

  Seki, Sayuri ^a   Matano, Tetsuro ^a,b  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

AIDS vaccine; CTL; HIV; Sendai virus; SIV

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; SENDAI VIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS VECTOR; DRUG CARRIER; RECOMBINANT VACCINE;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION CONTROL; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; SENDAI VIRUS; VACCINATION; DRUG DEVELOPMENT; GENE VECTOR; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; PROCEDURES; TRENDS;

AIDS VACCINES; CD8-POSITIVE T-LYMPHOCYTES; DRUG CARRIERS; DRUG DISCOVERY; GENETIC VECTORS; HUMANS; SENDAI VIRUS; VACCINES, SYNTHETIC;

EID: 84951568347     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/14760584.2016.1105747     Document Type: Review

References (98)

1. Papers of special note have been highlighted as
2. ∗ Of interest
3. ∗ Of considerable interest
4. McMichael A. T cell responses and viral escape. Cell. 1998; 93 (5): 673-676.
5. 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.
6. Wei X, Decker JM, Wang S., et al. Antibody neutralization and escape by HIV-1. Nature. 2003; 422 (6929): 307-312.
7. 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.
8. 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.
9. Berzofsky JA, Ahlers JD, Belyakov IM. Strategies for designing and optimizing new generation vaccines. Nat Rev Immunol. 2001; 1 (3): 209-219.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. Burton DR, Ahmed RA, Barouch DH., et al. A blueprint for HIV vaccine discovery. Cell Host Microbe. 2012; 12: 396-407.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. Feinberg MB, Moore JP. AIDS vaccine models: challenging challenge viruses. Nat Med. 2002; 8 (3): 207-210.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. Whitney JB, Ruprecht RM. Live attenuated HIV vaccines: pitfalls and prospects. Curr Opin Infect Dis. 2004; 17 (1): 17-26.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. Hansen SG, Sacha JB, Hughes CM., et al. Cytomegalovirus vectors violate CD8+ T cell epitope recognition paradigms. Science. 2013; 340 (6135): 1237874.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. 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.
67. Rolland M, Nickle DC, Mullins JI. HIV-1 group M conserved elements vaccine. PLoS Pathog. 2007; 3 (11): e157.
68. 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.
69. 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.
70. 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.
71. 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.
72. 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.
73. 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.
74. Shedlock DJ, Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science. 2003; 300 (5617): 337-339.
75. Sun J, Bevan M. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science. 2003; 300 (5617): 339-342.
76. 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.
77. 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.
78. Elsaesser H, Sauer K, Brooks DG. IL-21 is required to control chronic viral infection. Science. 2009; 324 (5934): 1569-1572.
79. 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.
80. 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.
81. + T cell responses associated with control of viremia. Science. 1997; 278 (5342): 1447-1450.
82. 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.
83. 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.
84. 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.
85. + T cell responses with HIV immune control. Nat Med. 2013; 19 (7): 930-933.
86. 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.
87. 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.
88. 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.
89. 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.
90. 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.
91. 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.
92. Douek DC, Brenchley JM, Betts MR., et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature. 2002; 417 (6884): 95-98.
93. 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.
94. 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.
95. 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.
96. 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.
97. 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.
98. 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.