Adenovirus-based HIV-1 vaccine candidates tested in efficacy trials elicit CD8 + T cells with limited breadth of HIV-1 inhibition

AIDS

Volumn 30, Issue 11, 2016, Pages 1703-1712

  Hayes, Peter J ^a   Cox, Josephine H ^a,f   Coleman, Adam R ^a   Fernandez, Natalia ^a   Bergin, Philip J ^a   Kopycinski, Jakub T ^a   Nitayaphan, Sorachai ^b   Pitisuttihum, Punnee ^c   De Souza, Mark ^d   Duerr, Ann ^e   Morgan, Cecilia ^e   Gilmour, Jill W ^a  

^a CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^b ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^c MAHIDOL UNIVERSITY   (Thailand)

^d THAI RED CROSS AIDS RESEARCH CENTRE   (Thailand)

^e Fred Hutchinson Cancer Research Center   (United States)

^f INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

Author keywords

CD8 positive T lymphocytes; genetic vectors; HIV 1; vaccines

Indexed keywords

ADENOVIRUS VACCINE; BISPECIFIC ANTIBODY; GAG PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; POL PROTEIN; DRUG CARRIER; GAMMA INTERFERON; RECOMBINANT VACCINE;

ADENOVIRUS INFECTION; ANTIVIRAL ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG DESIGN; DRUG DETERMINATION; DRUG EFFICACY; DRUG SCREENING; GENE SEQUENCE; HUMAN; HUMAN ADENOVIRUS 5; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENICITY; IN VITRO STUDY; INFECTION PREVENTION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; VIREMIA; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION; CELL CULTURE; ENZYME LINKED IMMUNOSPOT ASSAY; GENETICS; HUMAN ADENOVIRUS C; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; NORMAL HUMAN; SECRETION (PROCESS); VIROLOGY;

ADENOVIRUSES, HUMAN; AIDS VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DRUG CARRIERS; ENZYME-LINKED IMMUNOSPOT ASSAY; HEALTHY VOLUNTEERS; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-GAMMA; VACCINES, SYNTHETIC;

EID: 84963960472     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000001122     Document Type: Article

References (62)

1. Burton DR, Ahmed R, Barouch DH, Butera ST, Crotty S, Godzik A, et al. A blueprint for HIV vaccine discovery. Cell Host Microbe 2012; 12:396-407.
2. McElrath MJ, Haynes BF. Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 2010; 33:542-554.
3. McMichael AJ, KoffWC. Vaccines that stimulate T cell immunity to HIV-1: the next step. Nat Immunol 2014; 15:319-322.
4. D'Souza MP, Yang OO. Adenovirus vectors as HIV-1 vaccines: where are we? What next?. AIDS 2015; 29:395-400.
5. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, Li D, Gilbert PB, 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; 372:1881-1893.
6. McElrath MJ, De Rosa SC, Moodie Z, Dubey S, Kierstead L, Janes H, et al. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 2008; 372:1894-1905.
7. Gray GE, Allen M, Moodie Z, Churchyard G, Bekker LG, Nchabeleng M, et al. Safety and efficacy of the HVTN 503/ Phambili study of a clade-B-based HIV-1 vaccine in South Africa: a double-blind, randomised, placebo-controlled testof-concept phase 2b study. Lancet Infect Dis 2011; 11:507-515.
8. Hammer SM, Sobieszczyk ME, Janes H, Karuna ST, Mulligan MJ, Grove D, et al. Efficacy trial of a DNA/rAd5 HIV-1 preventive vaccine. N Engl J Med 2013; 369:2083-2092.
9. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361:2209-2220.
10. Priddy FH, Brown D, Kublin J, Monahan K, Wright DP, Lalezari J, et al. Safety and immunogenicity of a replication-incompetent adenovirus type 5 HIV-1 clade B gag/pol/nef vaccine in healthy adults. Clin Infect Dis 2008; 46:1769-1781.
11. Jaoko W, Karita E, Kayitenkore K, Omosa-Manyonyi G, Allen S, Than S, et al. Safety and immunogenicity study of multiclade HIV-1 adenoviral vector vaccine alone or as boost following a multiclade HIV-1 DNA vaccine in Africa. PLoS One 2010; 5:e12873.
12. Churchyard GJ, Morgan C, Adams E, Hural J, Graham BS, Moodie Z, et al. A phase IIA randomized clinical trial of a multiclade HIV-1 DNA prime followed by a multiclade rAd5 HIV-1 vaccine boost in healthy adults (HVTN 204). PLoS One 2011; 6:e21225.
13. Janes H, Friedrich DP, Krambrink A, Smith RJ, Kallas EG, Horton H, et al. Vaccine-induced Gag-specific T cells are associated with reduced viremia after HIV-1 infection. J Infect Dis 2013; 208:1231-1239.
14. Janes H, Frahm N, DeCamp A, Rolland M, Gabriel E, Wolfson J, et al. MRKAd5 HIV-1 Gag/Pol/Nef vaccine-induced T-cell responses inadequately predict distance of breakthrough HIV-1 sequences to the vaccine or viral load. PLoS One 2012; 7:e43396.
15. Nitayaphan S, Pitisuttithum P, Karnasuta C, Eamsila C, de Souza M, Morgan P, et al. Safety and immunogenicity of an HIV subtype B and E prime-boost vaccine combination in HIVnegative Thai adults. J Infect Dis 2004; 190:702-706.
16. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366:1275-1286.
17. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virusspecific CD8R cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 1994; 68:6103-6110.
18. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 1994; 68:4650-4655.
19. Klein MR, van Baalen CA, Holwerda AM, Kerkhof Garde SR, Bende RJ, Keet IP, et al. Kinetics of Gag-specific cytotoxic T lymphocyte responses during the clinical course of HIV-1 infection: a longitudinal analysis of rapid progressors and long-term asymptomatics. J Exp Med 1995; 181:1365-1372.
20. Rinaldo C, Huang XL, Fan ZF, Ding M, Beltz L, Logar A, et al. High levels of antihuman immunodeficiency virus type 1 (HIV-1) memory cytotoxic T-lymphocyte activity and low viral load are associated with lack of disease in HIV-1-infected long-term nonprogressors. J Virol 1995; 69:5838-5842.
21. Harrer T, Harrer E, Kalams SA, Barbosa P, Trocha A, Johnson RP, et al. Cytotoxic T lymphocytes in asymptomatic long-term nonprogressing HIV-1 infection: breadth and specificity of the response and relation to in vivo viral quasispecies in a person with prolonged infection and low viral load. J Immunol 1996; 156:2616-2623.
22. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, Nowak MA, et al. Late escape from an immunodominant cytotoxic Tlymphocyte response associated with progression to AIDS. Nat Med 1997; 3:212-217.
23. Heintel T, Sester M, Rodriguez MM, Krieg C, Sester U, Wagner R, et al. The fraction of perforin expressing HIV-specific CD8 T cells is a marker for disease progression in HIV infection. AIDS 2002; 16:1497-1501.
24. Migueles SA, Laborico AC, Shupert WL, Sabbaghian MS, Rabin R, Hallahan CW, et al. HIV-specific CD8R T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat Immunol 2002; 3:1061-1068.
25. Pantaleo G, Koup RA. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat Med 2004; 10:806-810.
26. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, Abraham J, et al. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8R T cells. Blood 2006; 107:4781-4789.
27. Friedrich TC, Valentine LE, Yant LJ, Rakasz EG, Piaskowski SM, Furlott JR, et al. Subdominant CD8R T cell responses are involved in durable control of AIDS virus replication. J Virol 2007; 81:3465-3476.
28. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, Ganusov VV, et al. The first T cell response to transmitted/ founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 2009; 206:1253-1272.
29. Riou C, Burgers WA, Mlisana K, Koup RA, Roederer M, Abdool Karim SS, et al. Differential impact of magnitude, polyfunctional capacity, and specificity of HIV-specific CD8R T cell responses on HIV set point. J Virol 2014; 88:1819-1824.
30. Smith NMG, Mlcochova P, Watters SA, Aasa-Chapman MMI, Rabin N, Moore S, et al. Proof-of-principle for immune control of global HIV-1 reactivation in vivo. Clin Inf Dis 2015; 61:120-128.
31. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, Whizin N, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011; 473:523-527.
32. Yamamoto T, Johnson MJ, Price DA, Wolinsky DI, Almeida JR, Petrovas C, et al. Virus inhibition activity of effector memory CD8 (R) T cells determines simian immunodeficiency virus load in vaccinated monkeys after vaccine breakthrough infection. J Virol 2012; 86:5877-5884.
33. Fukazawa Y, Park H, Cameron MJ, Lefebvre F, Lum R, Coombes N, et al. Lymph node T cell responses predict the efficacy of live attenuated SIV vaccines. Nat Med 2012; 18:1673-1681.
34. Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, et al. Vaccine-induced CD8 T cells control AIDS virus replication. Nature 2012; 491:129-135.
35. Mendoza D, Migueles SA, Rood JE, Peterson B, Johnson S, Doria-Rose N, et al. Cytotoxic capacity of SIV-specific CD8R T cells against primary autologous targets correlates with immune control in SIV-infected rhesus macaques. PLoS Pathog 2013; 9:e1003195.
36. D'Souza MP, Altfeld M. Measuring HIV-1-specific T cell immunity: how valid are current assays? J Infect Dis 2008; 197:337-339.
37. Bennett MS, Ng HL, Ali A, Yang OO. Cross-clade detection of HIV-1-specific cytotoxic T lymphocytes does not reflect crossclade antiviral activity. J Infect Dis 2008; 197:390-397.
38. Valentine LE, Piaskowski SM, Rakasz EG, Henry NL, Wilson NA, Watkins DI. Recognition of escape variants in ELISPOT does not always predict CD8R T-cell recognition of simian immunodeficiency virus-infected cells expressing the same variant sequences. J Virol 2008; 82:575-581.
39. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, Li H, et al. Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 2009; 206:1273-1289.
40. Yang OO, Walker BD. CD8R T cells in human immunodeficiency virus type I pathogenesis: cytolytic and noncytolytic inhibition of viral replication. Adv Immunol 1997; 66:273-311.
41. Saez-Cirion A, Lacabaratz C, Lambotte O, Versmisse P, Urrutia A, Boufassa F, et al. HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype. Proc Natl Acad Sci USA 2007; 104:6776-6781.
42. Deeks SG, Walker BD. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 2007; 27:406-416.
43. Spentzou A, Bergin P, Gill D, Cheeseman H, Ashraf A, Kaltsidis H, et al. Viral inhibition assay: a CD8 T cell neutralization assay for use in clinical trials of HIV-1 vaccine candidates. J Infect Dis 2010; 201:720-729.
44. Yang H, Wu H, Hancock G, Clutton G, Sande N, Xu X, et al. Antiviral inhibitory capacity of CD8R T cells predicts the rate of CD4R T-cell decline in HIV-1 Infection. J Infect Dis 2012; 206:552-561.
45. Slichter CK, Friedrich DP, Smith RJ, Walsh PN, Mize G, Czartoski JL, et al. Measuring inhibition of HIV replication by ex vivo CD8R T cells. J Immunol Methods 2014; 404:71-80.
46. de Souza MS, Ratto-Kim S, Chuenarom W, Schuetz A, Chantakulkij S, Nuntapinit B, 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; 188:5166-5176.
47. Boaz MJ, Hayes P, Tarragona T, Seamons L, Cooper A, Birungi J, et al. Concordant proficiency in measurement of T-cell immunity in human immunodeficiency virus vaccine clinical trials by peripheral blood mononuclear cell and enzyme-linked immunospot assays in laboratories from three continents. Clin Vaccine Immunol 2009; 16:147-155.
48. Liang X, Fu TM, Xie H, Emini EA, Shiver JW. Development of HIV-1 Nef vaccine components: immunogenicity study of Nef mutants lacking myristoylation and dileucine motif in mice. Vaccine 2002; 20:3413-3421.
49. Wei X, Decker JM, Liu H, Zhang Z, Arani RB, Kilby JM, et al. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 2002; 46:1896-1905.
50. Edmonds TG, Ding H, Yuan X, Wei Q, Smith KS, Conway JA, et al. Replication competent molecular clones of HIV-1 expressing Renilla luciferase facilitate the analysis of antibody inhibition in PBMC. Virology 2010; 408:1-13.
51. Ochsenbauer C, Edmonds TG, Ding H, Keele BF, Decker J, Salazar MG, et al. Generation of transmitted/founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol 2012; 86:2715-2728.
52. Wong JT, Colvin RB. Selective reduction and proliferation of the CD4R and CD8R T cell subsets with bispecific monoclonal antibodies: evidence for inter-T cell-mediated cytolysis. Clin Immunol Immunopathol 1991; 58:236-250.
53. Borthwick N, Ahmed T, Ondondo B, Hayes P, Rose A, Ebrahimsa U, et al. Vaccine-elicited human T cells recognizing conserved protein regions inhibit HIV-1. Mol Ther 2014; 22:464-475.
54. Omosa-Manyonyi G, Mpendo J, Ruzagira E, Kilembe W, Chomba E, Roman F, et al. A phase I double blind, placebo-controlled, randomized study of the safety and immunogenicity of an adjuvanted HIV-1 Gag-Pol-Nef fusion protein and adenovirus 35 Gag-RT-Int-Nef vaccine in healthy HIV-uninfected African adults. PLoS One 2015; 10:e0125954.
55. Mpendo J, Mutua G, Nyombayire J, Ingabire R, Nanvubya A, Anzala O, et al. A phase I double blind, placebo-controlled, randomized study of the safety and immunogenicity of electroporated HIV DNA with or without interleukin 12 in primeboost combinations with an Ad35 HIV vaccine in healthy HIVseronegative African adults. PLoS One 2015; 10:e0134287.
56. Naarding MA, Fernandez N, Kappes JC, Hayes P, Ahmed T, Icyuz M, et al. Development of a luciferase based viral inhibition assay to evaluate vaccine induced CD8 T-cell responses. J Immunol Methods 2014; 409:161-173.
57. Hertz T, Ahmed H, Friedrich DP, Casimiro DR, Self SG, Corey L, et al. HIV-1 vaccine-induced T-cell responses cluster in epitope hotspots that differ from those induced in natural infection with HIV-1. PLoS Pathog 2013; 9:1-14.
58. Li F, Horton H, Gilbert PB, McElrath JM, Corey L, Self SG. HIV-1 CTL-based vaccine immunogen selection: antigen diversity and cellular response features. Curr HIV Res 2007; 5:97-107.
59. Hancock G, Yang H, Yorke E, Wainwright E, Bourne V, Frisbee A, et al. Identification of effective subdominant anti-HIV-1 CD8R T cells within entire postinfection and postvaccination immune responses. PLoS Pathog 2015; 11:e1004658.
60. Freel SA, Lamoreaux L, Chattopadhyay PK, Saunders K, Zarkowsky D, Overman RG, et al. Phenotypic and functional profile of HIV-Inhibitory CD8 T cells elicited by natural infection and heterologous prime/boost vaccination. J Virol 2010; 84:4998-5006.
61. Hansen SG, Piatak M, Ventura AB, Hughes CM, Gilbride RM, Ford JC, et al. Immune clearance of highly pathogenic SIV infection. Nature 2013; 502:100-104.
62. Deng K, Pertea M, Rongvaux A, Wang L, Durand CM, Ghiaur G. Broad CTL response is required to clear latent HIV-1 due to dominance of escape mutations. Nature 2015; 517:381-385.