Longitudinal analysis of an HLA-B*51-restricted epitope in integrase reveals immune escape in early HIV-1 infection

AIDS

Volumn 27, Issue 3, 2013, Pages 313-323

  Yager, Nicole ^a   Robinson, Nicola ^a   Brown, Helen ^a   Flanagan, Peter ^a   Frater, John ^a,b   Fidler, Sarah ^c   Weber, Jonathan ^c   Phillips, Rodney ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

cytotoxic T lymphocyte escape; early HIV 1 infection; HLA B51; integrase; longitudinal; vaccine

Indexed keywords

GAMMA INTERFERON; HLA B51 ANTIGEN; INTEGRASE;

ADULT; ARTICLE; CELL FUNCTION; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE ESCAPE; DNA POLYMORPHISM; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GENE SEQUENCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS LOAD;

DISEASE PROGRESSION; EPITOPES, T-LYMPHOCYTE; EVOLUTION, MOLECULAR; FEMALE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HLA-B51 ANTIGEN; HUMANS; INTEGRASES; INTERFERON-GAMMA; LONGITUDINAL STUDIES; MALE; MOLECULAR SEQUENCE DATA; MUTATION; RNA, VIRAL; T-LYMPHOCYTES, CYTOTOXIC; VIRAL LOAD;

EID: 84872359940     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32835b8cf5     Document Type: Article

References (33)

1. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB. Virus-specific CD8R cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 1994; 68:6103-6110.
2. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W, 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; 68:4650-4655.
3. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, et al. Control of viremia in simian immunodeficiency virus infection by CD8R lymphocytes. Science 1999; 283:857-860.
4. Harrer T, Harrer E, Kalams SA, Elbeik T, Staprans SI, Feinberg MB, et al. Strong cytotoxic T cell and weak neutralizing antibody responses in a subset of persons with stable non-progressing HIV type 1 infection. AIDS Res Hum Retroviruses 1996; 12:585-592.
5. 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 longterm nonprogressors. J Virol 1995; 69:5838-5842.
6. Rowland-Jones S, Sutton J, Ariyoshi K, Dong T, Gotch F, McA-dam S, et al. HIV-specific cytotoxic T-cells in HIV-exposed but uninfected Gambian women. Nat Med 1995; 1:59-64.
7. Phillips RE, Rowland-Jones S, Nixon DF, Gotch FM, Edwards JP, Ogunlesi AO, et al. Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 1991; 354:453-459.
8. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, Meyers H, et al. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 1997; 3:205-211.
9. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, Nowak MA, et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 1997; 3:212-217.
10. Kent SJ, Fernandez CS, Dale CJ, Davenport MP. Reversion of immune escape HIV variants upon transmission: insights into effective viral immunity. Trends Microbiol 2005; 13:243-246.
11. Kaslow RA, Carrington M, Apple R, Park L, Munoz A, Saah AJ, et al. Influence of combinations of human major histocompat-ibility complex genes on the course of HIV-1 infection. Nat Med 1996; 2:405-411.
12. O'Brien SJ, Gao X, Carrington M. HLA and AIDS: a cautionary tale. Trends Mol Med 2001; 7:379-381.
13. Zhang Y, Peng Y, Yan H, Xu K, Saito M, Wu H, et al. Multilayered defense in HLA-B51-associated HIV viral control. J Immunol 2011; 187:684-691.
14. Tomiyama H, Sakaguchi T, Miwa K, Oka S, Iwamoto A, Kaneko Y, et al. Identification of multiple HIV-1 CTL epitopes presented by HLA-BM5101 molecules. Hum Immunol 1999; 60:177-186.
15. Yusim K, Korber BTM, Brander C, Haynes BF, Koup R, Moore JP, et al. HIV molecular immunology. New Mexico: Los Alamos National Laboratory, Theoretical Biology and Biophysics; 2009.
16. Leslie A, Kavanagh D, Honeyborne I, Pfafferott K, Edwards C, Pillay T, et al. Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J Exp Med 2005; 201:891-902.
17. Mellors JW, Kingsley LA, Rinaldo CR Jr, Todd JA, Hoo BS, Kokka RP, et al. QuantitationofHIV-1 RNAinplasma predicts outcome after seroconversion. Ann Intern Med 1995; 122:573-579.
18. Mellors JW, Rinaldo CR Jr, Gupta P, White RM, Todd JA, Kingsley LA. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 1996; 272:1167-1170.
19. Fidler S, Oxenius A, Brady M, Clarke J, Cropley I, Babiker A, et al. Virological and immunological effects of short-course antiretroviral therapy in primary HIV infection. AIDS 2002; 16:2049-2054.
20. Duda A, Lee-Turner L, Fox J, Robinson N, Dustan S, Kaye S, et al. HLA-associated clinical progression correlates with epitope reversion rates in early human immunodeficiency virus infection. J Virol 2009; 83:1228-1239.
21. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003; 52:696-704.
22. Varela-Rohena A, Molloy PE, Dunn SM, Li Y, Suhoski MM, Carroll RG, et al. Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 2008; 14:1390-1395.
23. Miura T, Brockman MA, Brumme ZL, Brumme CJ, Pereyra F, Trocha A, et al. HLA-associated alterations in replication-capacity of chimeric NL4-3 viruses carrying gag-protease from elite controllers of human immunodeficiency virus type 1. J Virol 2009; 83:140-149.
24. Brumme ZL, Li C, Miura T, Sela J, Rosato PC, Brumme CJ, et al. Reduced replication capacity of NL4-3 recombinant viruses encoding reverse transcriptase-integrase sequences from HIV-1 elite controllers. J Acquir Immune Defic Syndr 2011; 56:100-108.
25. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, Addo M, et al. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009; 458:641-645.
26. Bhattacharya T, Daniels M, Heckerman D, Foley B, Frahm N, Kadie C, et al. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science 2007; 315:1583-1586.
27. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, Bornstein E, et al. Superior control of HIV-1 replication by CD8R T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 2007; 204:2473-2485.
28. Payne RP, Kloverpris H, Sacha JB, Brumme Z, Brumme C, Buus S, et al. Efficacious early antiviral activity of HIV Gag-and Pol-specific HLA-B 2705-restricted CD8R T cells. J Virol 2010; 84:10543-10557.
29. Fidler S, SPARTAC Trial Investigators. The effect of short-course antiretroviral therapy in primary HIV infection: final results from an international randomised controlled trial; SPARTAC [abstract]. In: IAS 2011; Rome, Italy; 2011; WELBX06.
30. Propato A, Schiaffella E, Vicenzi E, Francavilla V, Baloni L, Paroli M, et al. Spreading of HIV-specific CD8R T-cell repertoire in long-term nonprogressors and its role in the control of viral load and disease activity. Hum Immunol 2001; 62:561-576.
31. Leslie A, Price DA, Mkhize P, Bishop K, Rathod A, Day C, et al. Differential selection pressure exerted on HIV by CTL targeting identical epitopes but restricted by distinct HLA alleles from the same HLA supertype. J Immunol 2006; 177:4699-4708.
32. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honey-borne I, Moodley E, et al. CD8R T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007; 13:46-53.
33. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 2004; 10:282-289.