Vaccine-induced gag-specific T cells are associated with reduced viremia after HIV-1 infection

Journal of Infectious Diseases

Volumn 208, Issue 8, 2013, Pages 1231-1239

  Janes, Holly ^a,b   Friedrich, David P ^a   Krambrink, Amy ^a   Smith, Rebecca J ^a   Kallas, Esper G ^e   Horton, Helen ^d   Casimiro, Danilo R ^f   Carrington, Mary ^g,h   Geraghty, Daniel E ^a   Gilbert, Peter B ^a,b   McElrath, M Juliana ^a,b,c   Frahm, Nicole ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b Department of Biostatistics ^*  (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

^f MERCK RESEARCH LABORATORIES   (United States)

^g SAIC FREDERICK INC   (United States)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Gag specific T cells; HIV 1 vaccine; HLA class I alleles; Step study

Indexed keywords

GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS 1 VACCINE MRKAD5; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEF PROTEIN; PLACEBO; POL PROTEIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; DRUG SAFETY; GENE FREQUENCY; HLA TYPING; HOMOZYGOSITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; MAJOR CLINICAL STUDY; MULTICENTER STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; VIRUS GENOME; VIRUS LOAD; VIRUS REPLICATION;

GAG-SPECIFIC T CELLS; HIV-1 VACCINE; HLA CLASS I ALLELES; STEP STUDY;

ADULT; AIDS VACCINES; ALLELES; DOUBLE-BLIND METHOD; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV INFECTIONS; HIV-1; HLA ANTIGENS; HUMANS; MALE; RNA, VIRAL; T-LYMPHOCYTES; VIRAL LOAD; VIREMIA;

EID: 84885028465     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit322     Document Type: Article

References (49)

1. Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Eng J Med 2012; 366:1275-86.
2. Baeten JM, Donnell D, Ndase P, et al. Antiretroviral prophylaxis for HIV prevention in heterosexual men and women. N Eng J Med 2012; 367:399-410.
3. Bailey RC, Moses S, Parker CB, et al. Male circumcision for HIV prevention in young men in Kisumu, Kenya: A randomised controlled trial. Lancet 2007; 369:643-56.
4. Abdool Karim Q, Abdool Karim SS, Frohlich JA, et al. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 2010; 329:1168-74.
5. Grant RM, Lama JR, Anderson PL, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Eng J Med 2010; 363:2587-99.
6. Cohen MS, Chen YQ, McCauley M, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Eng J Med 2011; 365:493-505.
7. Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cellmediated immunity HIV-1 vaccine (the Step Study): A double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008; 372(9653): 1881-93.
8. 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.
9. Fitzgerald DW, Janes H, Robertson M, et al. An Ad5-vectored HIV-1 vaccine elicits cell-mediated immunity but does not affect disease progression in HIV-1-infected male subjects: Results from a randomized placebo-controlled trial (the Step study). J Infect Dis 2011; 203:765-72.
10. Rolland M, Tovanabutra S, de Camp AC, et al. Genetic impact of vaccination on breakthrough HIV-1 sequences from the STEP trial. Nat Med 2011; 17:366-71.
11. Janes H, Frahm N, DeCamp A, 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.
12. 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: 4650-55.
13. Schmitz J, Kuroda M, Santra S, et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999; 277:333-8.
14. Cao J, McNevin J, Malhotra U, McElrath MJ. Evolution of CD8+ T cell immunity and viral escape following acute HIV-1 infection. J Immunol 2003; 171:3837-46.
15. Allen TM, O'Connor DH, Jing P, et al. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 2000; 407:386-90.
16. Goulder PJ, Phillips RE, Colbert RA, et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 1997; 3:212-7.
17. 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; 290:486-92.
18. 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; 292:69-74.
19. Shiver JW, Fu TM, Chen L, et al. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002; 415:331-5.
20. Wilson NA, Keele BF, Reed JS, et al. Vaccine-induced cellular responses control simian immunodeficiency virus replication after heterologous challenge. J Virol 2009; 83:6508-21.
21. Hansen SG, Vieville C, Whizin N, et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 2009; 15:293-9.
22. Betts MR, Ambrozak DR, Douek DC, et al. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: Relationship to viral load in untreated HIV infection. J Virol 2001; 75:11983-91.
23. Ogg GS, Jin X, Bonhoeffer S, et al. Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998; 279:2103-6.
24. Addo MM, Yu XG, Rathod A, et al. Comprehensive epitope analysis of HIV-1-specific T cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J Virol 2003; 77:2081-92.
25. Cao J, McNevin J, Holte S, Fink L, Corey L, McElrath MJ. Comprehensive analysis of human immunodeficiency virus type 1 (HIV-1)-specific gamma interferon-secreting CD8+ T cells in primary HIV-1 infection. J Virol 2003; 77:6867-78.
26. Zuniga 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; 80:3122-5.
27. Ranasinghe S, Flanders M, Cutler S, et al. HIV-specific CD4 T cell responses to different viral proteins have discordant associations with viral load and clinical outcome. J Virol 2012; 86:277-83.
28. 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; 13:46-53.
29. Masemola A, Mashishi T, Khoury G, et al. Hierarchical targeting of subtype C human immunodeficiency virus type 1 proteins by CD8+ T cells: Correlation with viral load. J Virol 2004; 78:3233-43.
30. Steel CM, Ludlam CA, Beatson D, et al. HLA haplotype A1 B8 DR3 as a risk factor for HIV-related disease. Lancet 1988; 1:1185-8.
31. O'Brien SJ, Gao X, Carrington M. HLA and AIDS: A cautionary tale. Trends Mol Med 2001; 7:379-81.
32. Frahm N, Linde CH, Brander C. Identification of HIV-derived, HLA class I restricted CTL epitopes: Insights into TCR repertoire, CTL escape and viral fitness. In: Korber BTM, Brander C, Haynes BF, et al. eds. HIV immunology and HIV/SIV vaccine databases 2004. Los Alamos, NM: Los Alamos National Laboratory, Theoretical Biology and Biophysics, 2006/2007:3-28.
33. Dinges WL, Richardt J, Friedrich D, et al. Virus-specific CD8+ T-cell responses better define HIV disease progression than HLA genotype. J Virol 2010; 84:4461-8.
34. Martinez-Picado J, Prado JG, Fry EE, et al. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J Virol 2006; 80:3617-23.
35. Brockman MA, Schneidewind A, Lahaie M, et al. Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J Virol 2007; 81:12608-18.
36. Schneidewind A, Brockman MA, Yang R, et al. Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J Virol 2007; 81:12382-93.
37. Carrington M, Nelson GW, Martin MP, et al. HLA and HIV-1: Heterozygote advantage and B.*35-Cw.*o4 disadvantage. Science 1999; 283: 1748-52.
38. Kaslow RA, Carrington M, Apple R, et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 1996; 2:405-11.
39. Carrington M, Walker BD. Immunogenetics of spontaneous control of HIV. Annu Rev Med 2012; 63:131-45.
40. Carrington M, O'Brien SJ. The influence of HLA genotype on AIDS. Annu Rev Med 2003; 54:535-51.
41. Mothe BR, Weinfurter J, Wang C, et al. Expression of the major histocompatibility complex class I molecule Mamu-A.*o1 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 2003; 77:2736-40.
42. Yant LJ, Friedrich TC, Johnson RC, et al. The high-frequency major histocompatibility complex class I allele Mamu-B.*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 2006; 80:5074-7.
43. Fellay J, Shianna KV, Ge D, et al. A whole-genome association study of major determinants for host control of HIV-1. Science 2007; 317:944-7.
44. Pereyra F, Jia X, McLaren PJ, et al. The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 2010; 330:1551-7.
45. Fellay J, Frahm N, Shianna KV, et al. Host genetic determinants of T cell responses to the MRKAd5 HIV-1 gag/pol/nef vaccine in the step trial. J Infect Dis 2011; 203:773-9.
46. Gao X, Nelson GW, Karacki P, et al. Effect of a single amino acid change in MHC class I molecules on the rate of progression to AIDS. N Eng J Med 2001; 344:1668-75.
47. Frahm N, DeCamp AC, Friedrich DP, et al. Human adenovirus-specific T cells modulate HIV-specific T cell responses to an Ad5-vectored HIV-1 vaccine. J Clin Invest 2012; 122:359-67.
48. Horton H, Thomas EP, Stucky JA, et al. Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-specific T cells induced by vaccination. J Immunol Methods 2007; 323:39-54.
49. Migueles SA, Rood JE, Berkley AM, et al. Trivalent adenovirus type 5 HIV recombinant vaccine primes for modest cytotoxic capacity that is greatest in humans with protective HLA class I alleles. PLoS Pathog 2011; 7:e1002002.