Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients

Journal of Experimental Medicine

Volumn 205, Issue 5, 2008, Pages 1009-1017

  Goepfert, Paul A ^a,b   Lumm, Wendy ^d   Farmer, Paul ^d   Matthews, Philippa ^e   Prendergast, Andrew ^e   Carlson, Jonathan M ^f,g   Derdeyn, Cynthia A ^d,h   Tang, Jianming ^a,b   Kaslow, Richard A ^c   Bansal, Anju ^a   Yusim, Karina ⁱ   Heckerman, David ^f   Mulenga, Joseph ^j   Allen, Susan ^d   Goulder, Philip J R ^e,k,l   Hunter, Eric ^d,h  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d EMORY UNIVERSITY   (United States)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f MICROSOFT RESEARCH   (United States)

^g University of Washington   (United States)

^h EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ LOS ALAMOS NATIONAL LABORATORY   (United States)

^j Zambia Emory HIV Research Project   (Zambia)

^k UNIVERSITY OF KWAZULU NATAL   (South Africa)

^l MASSACHUSETTS GENERAL HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

ALLELE; ARTICLE; CYTOTOXIC T LYMPHOCYTE; DONOR SELECTION; GENE MUTATION; GENETIC POLYMORPHISM; HLA SYSTEM; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IN VIVO STUDY; LEUKOCYTE; MAJOR CLINICAL STUDY; PATHOGENESIS; PRIORITY JOURNAL; VIRUS LOAD; VIRUS TRANSMISSION;

AMINO ACID SEQUENCE; BASE SEQUENCE; GENE PRODUCTS, GAG; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV-1; HLA-B ANTIGENS; HUMANS; MUTATION; POLYMORPHISM, GENETIC; SOUTH AFRICA; VIRAL LOAD; ZAMBIA;

EID: 43549109265     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20072457     Document Type: Article

References (34)

1. Goulder, P.J., and D.I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
2. + elite suppressors despite CTL escape mutations. J. Exp. Med. 203:1357-1369.
3. Goulder, P.J., R.E. Phillips, R.A. Colbert, S. McAdam, G. Ogg, M.A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, et al. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
4. Edwards, B.H., A. Bansal, S. Sabbaj, J. Bakari, M.J. Mulligan, and P.A. Goepfert. 2002. Magnitude of functional CD8+ T-cell responses to the gag protein of human immunodeficiency virus type 1 correlates inversely with viral load in plasma. J. Virol. 76:2298-2305.
5. Ramduth, D., P. Chetty, N.C. Mngquandaniso, N. Nene, J.D. Harlow, I. Honeyborne, N. Ntumba, S. Gappoo, C. Henry, P. Jeena, et al. 2005. Differential immunogenicity of HIV-1 clade C proteins in eliciting CD8+ and CD4+ cell responses. J. Infect. Dis. 192:1588-1596.
6. Kiepiela, P., K. Ngumbela, C. Thobakgale, D. Ramduth, I. Honeyborne, E. Moodley, S. Reddy, C. de Pierres, Z. Mncube, N. Mkhwanazi, et al. 2007. CD8(+) T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
7. Kaslow, R.A., M. Carrington, R. Apple, L. Park, A. Munoz, A.J. Saah, J.J. Goedert, C. Winkler, S.J. O'Brien, C. Rinaldo, et al. 1996. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2:405-411.
8. Altfeld, M., E.T. Kalife, Y. Qi, H. Streeck, M. Lichterfeld, M.N. Johnston, N. Burgett, M.E. Swartz, A. Yang, G. Alter, et al. 2006. HLA Alleles Associated with Delayed Progression to AIDS Contribute Strongly to the Initial CD8(+) T Cell Response against HIV-1. PLoS Med. 3:e403.
9. Migueles, S.A., A.C. Laborico, W.L. Shupert, M.S. Sabbaghian, R. Rabin, C.W. Hallahan, D. Van Baarle, S. Kostense, F. Miedema, M. McLaughlin, et al. 2002. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
10. + T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204:2473-2485.
11. Crawford, H., J.G. Prado, A. Leslie, S. Hue, I. Honeyborne, S. Reddy, M. van der Stok, Z. Mncube, C. Brander, C. Rousseau, et al. 2007. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLA-B*5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 81:8346-8351.
12. Leslie, A.J., K.J. Pfafferott, P. Chetty, R. Draenert, M.M. Addo, M. Feeney, Y. Tang, E.C. Holmes, T. Allen, J.G. Prado, et al. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10:282-289.
13. Brockman, M.A., A. Schneidewind, M. Lahaie, A. Schmidt, T. Miura, I. Desouza, F. Ryvkin, C.A. Derdeyn, S. Allen, E. Hunter, et al. 2007. 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. 81:12608-12618.
14. Schneidewind, A., M.A. Brockman, R. Yang, R.I. Adam, B. Li, S. Le Gall, C.R. Rinaldo, S.L. Craggs, R.L. Allgaier, K.A. Power, et al. 2007. 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. 81:12382-12393.
15. Leslie, A., D. Kavanagh, I. Honeyborne, K. Pfafferott, C. Edwards, T. Pillay, L. Hilton, C. Thobakgale, D. Ramduth, R. Draenert, et al. 2005. Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J. Exp. Med. 201:891-902.
16. Bhattacharya, T., M. Daniels, D. Heckerman, B. Foley, N. Frahm, C. Kadie, J. Carlson, K. Yusim, B. McMahon, B. Gaschen, et al. 2007. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science. 315:1583-1586.
17. Brumme, Z.L., C.J. Brumme, D. Heckerman, B.T. Korber, M. Daniels, J. Carlson, C. Kadie, T. Bhattacharya, C. Chui, J. Szinger, et al. 2007. Evidence of Differential HLA Class I-Mediated Viral Evolution in Functional and Accessory/Regulatory Genes of HIV-1. PLoS Pathog. 3:e94.
18. Bansal, A., E. Gough, S. Sabbaj, D. Ritter, K. Yusim, G. Sfakianos, G. Aldrovandi, R.A. Kaslow, C.M. Wilson, M.J. Mulligan, et al. 2005. CD8 T-cell responses in early HIV-1 infection are skewed towards high entropy peptides. AIDS. 19:241-250.
19. Draenert, R., S. Le Gall, K.J. Pfafferott, A.J. Leslie, P. Chetty, C. Brander, E.C. Holmes, S.C. Chang, M.E. Feeney, M.M. Addo, et al. 2004. Immune selection for altered antigen processing leads to cytotoxic T lymphocyte escape in chronic HIV-1 infection. J. Exp. Med. 199:905-915.
20. Leslie, A., D.A. Price, P. Mkhize, K. Bishop, A. Rathod, C. Day, H. Crawford, I. Honeyborne, T.E. Asher, G. Luzzi, et al. 2006. Differential selection pressure exerted on HIV by CTL targeting identical epitopes but restricted by distinct HLA alleles from the same HLA supertype. J. Immunol. 177:4699-4708.
21. Fideli, U.S., S.A. Allen, R. Musonda, S. Trask, B.H. Hahn, H. Weiss, J. Mulenga, F. Kasolo, S.H. Vermund, and G.M. Aldrovandi. 2001. Virologic and immunologic determinants of heterosexual transmission of human immunodeficiency virus type 1 in Africa. AIDS Res. Hum. Retroviruses. 17:901-910.
22. Trask, S.A., C.A. Derdeyn, U. Fideli, Y. Chen, S. Meleth, F. Kasolo, R. Musonda, E. Hunter, F. Gao, S. Allen, and B.H. Hahn. 2002. Molecular epidemiology of human immunodeficiency virus type 1 transmission in a heterosexual cohort of discordant couples in Zambia. J. Virol. 76:397-405.
23. Kiepiela, P., A.J. Leslie, I. Honeyborne, D. Ramduth, C. Thobakgale, S. Chetty, P. Rathnavalu, C. Moore, K.J. Pfafferott, L. Hilton, et al. 2004. Dominant influence of HLA-B in mediating the potential coevolution of HIV and HLA. Nature. 432:769-775.
24. Frater, A.J., H. Brown, A. Oxenius, H.F. Gunthard, B. Hirschel, N. Robinson, A.J. Leslie, R. Payne, H. Crawford, A. Prendergast, et al. 2007. Effective T-cell responses select human immunodeficiency virus mutants and slow disease progression. J. Virol. 81:6742-6751.
25. Lanman, J., T.T. Lam, M.R. Emmett, A.G. Marshall, M. Sakalian, and P.E. Prevelige Jr. 2004. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11:676-677.
26. Borghans, J.A., A. Molgaard, R.J. de Boer, and C. Kesmir. 2007. HLA alleles associated with slow progression to AIDS truly prefer to present HIV-1 p24. PLoS ONE. 2:e920.
27. Johnson, D.R. 2000. Differential expression of human major histocompatibility class I loci: HLA-A, -B, and -C. Hum. Immunol. 61:389-396.
28. Alter, G., M.P. Martin, N. Teigen, W.H. Carr, T.J. Suscovich, A. Schneidewind, H. Streeck, M. Waring, A. Meier, C. Brander, et al. 2007. Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J. Exp. Med. 204:3027-3036.
29. Lyles, R.H., A. Munoz, T.E. Yamashita, H. Bazmi, R. Detels, C.R. Rinaldo, J.B. Margolick, J.P. Phair, and J.W. Mellors. 2000. Natural history of human immunodeficiency virus type 1 viremia after seroconversion and proximal to AIDS in a large cohort of homosexual men. Multicenter AIDS Cohort Study. J. Infect. Dis. 181:872-880.
30. Kuntzen, T., J. Timm, A. Berical, L.L. Lewis-Ximenez, A. Jones, B. Nolan, J. Schulze zur Wiesch, B. Li, A. Schneidewind, A.Y. Kim, et al. 2007. Viral sequence evolution in acute HCV infection. J. Virol. 81:11658-11668.
31. + T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200:749-759.
32. Shugars, D.C., M.S. Smith, D.H. Glueck, P.V. Nantermet, F. Seillier-Moiseiwitsch, and R. Swanstrom. 1993. Analysis of human immunodeficiency virus type 1 nef gene sequences present in vivo. J. Virol. 67:4639-4650.
33. Tang, J., S. Tang, E. Lobashevsky, A.D. Myracle, U. Fideli, G. Aldrovandi, S. Allen, R. Musonda, and R.A. Kaslow. 2002. Favorable and unfavorable HLA class I alleles and haplotypes in Zambians predominantly infected with clade C human immunodeficiency virus type 1. J. Virol. 76:8276-8284.
34. Carlson, J., C. Kadie, S. Mallal, and D. Heckerman. 2007. Leveraging hierarchical population structure in discrete association studies. PLoS ONE. 2:e591.