QUASI analysis of host immune responses to Gag polyproteins of human immunodeficiency virus type 1 by a systematic bioinformatics approach

Biochemistry and Cell Biology

Volumn 88, Issue 4, 2010, Pages 671-681

  Liang, Binhua ^a   Luo, Ma ^a,b   Ball, T Blake ^a,b   Jones, Steven J M ^a,c   Plummer, Francis A ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^c BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

Author keywords

Cytotoxic t lymphocyte response; Gag; Human immunodeficiency virus type 1; Positive selection

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANTIBODY RESPONSE; CLASS I; CTL EPITOPE; CYTOTOXIC T LYMPHOCYTES; DISEASE PROGRESSION; HOST IMMUNE RESPONSE; HUMAN IMMUNODEFICIENCY VIRUS TYPE-1; IMMUNE CONTROL; POLYPROTEINS; POSITIVE SELECTION; SEQUENCE DATABASE;

BIOINFORMATICS; IMMUNOLOGY; VIRUSES;

DISEASES;

GAG PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALLELE; ARTICLE; CLADISTICS; CYTOTOXIC T LYMPHOCYTE; GENETIC DATABASE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE;

AIDS VACCINES; AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; DATABASES, PROTEIN; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HIV INFECTIONS; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNODOMINANT EPITOPES; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, PROTEIN;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77954904807     PISSN: 08298211     EISSN: 12086002     Source Type: Journal    
DOI: 10.1139/O10-002     Document Type: Article

References (44)

1. Addo, M.M., Yu, X.G., Rathod, A., Cohen, D., Eldridge, R.L., Strick, D., et al. 2003. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to iral load. J. Virol. 77(3): 2081-2092. doi:10.1128/JVI.77.3. 2081-2092.2003. PMID:12525643.
2. Alter, G., Teigen, N., Ahern, R., Streeck, H., Meier, A., Rosenberg, E.S., and Altfeld, M. 2007. Evolution of innate and adaptive effector cell functions during acute HIV-1 infection. J. Infect. Dis. 195(10): 1452-1460. doi:10.1086/513878. PMID:17436225.
3. Altfeld, M., Kalife, E.T., Qi, Y., Streeck, H., Lichterfeld, M., Johnston, M.N., 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(10): e403. doi:10. 1371/journal.pmed.0030403. PMID:17076553.
4. Bandawe, G.P., Martin, D.P., Treurnicht, F., Mlisana, K., Karim, S.S., and Williamson, C.; CAPRISA 002 Acute Infection Study Team. 2008. Conserved positive selection signals in gp41 across multiple subtypes and difference in selection signals detectable in gp41 sequences sampled during acute and chronic HIV-1 subtype C infection. Virol. J. 5: 141. PMID:19025632.
5. Boutwell, C.L., Rowley, C.F., and Essex, M. 2009. Reduced viral replication capacity of human immunodeficiency virus type 1 subtype C caused by cytotoxic-T-lymphocyte escape mutations in HLA-B57 epitopes of capsid protein. J. Virol. 83(6): 2460-2468. doi:10.1128/JVI.01970-08. PMID:19109381
6. Choisy, M., Woelk, C.H., Guégan, J.F., and Robertson, D.L. 2004. Comparative study of adaptive molecular evolution in different human immunodeficiency virus groups and subtypes. J. Virol. 78(4): 1962-1970. doi:10.1128/JVI.78.4.1962-1970.2004. PMID:14747561.
7. Coplan, P.M., Gupta, S.B., Dubey, S.A., Pitisuttithum, P., Nikas, A., Mbewe, B., et al. 2005. Cross-reactivity of anti-HIV-1 T cell immune responses among the major HIV-1 clades in HIV- 1-positive individuals from 4 continents. J. Infect. Dis. 191(9): 1427-1434. doi:10.1086/428450. PMID:15809900.
8. Crawford, H., Prado, J.G., Leslie, A., Hué, S., Honeyborne, I., Reddy, S., 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(15): 8346-8351. doi:10.1128/JVI.00465-07. PMID:17507468.
9. Day, C.L., Kiepiela, P., Leslie, A.J., van der Stok, M., Nair, K., Ismail, N., et al. 2007. Proliferative capacity of epitope-specific CD8 T-cell responses is inversely related to viral load in chronic human immunodeficiency virus type 1 infection. J. Virol. 81(1): 434-438. doi:10.1128/JVI.01754-06. PMID:17050606.
10. De Groot, A.S., Jesdale, B., Martin, W., Saint Aubin, C., Sbai, H., Bosma, A., et al. 2003. Mapping cross-clade HIV-1 vaccine epitopes using a bioinformatics approach. Vaccine, 21(27-30): 4486-4504. doi:10.1016/S0264-410X(03)00390-6. PMID: 14505932.
11. Ferrari, G., Humphrey, W., McElrath, M.J., Excler, J.L., Duliege, A.M., Clements, M.L., et al. 1997. Clade B-based HIV-1 vaccines elicit cross-clade cytotoxic T lymphocyte reactivities in uninfected volunteers. Proc. Natl. Acad. Sci. U.S.A. 94(4): 1396-1401doi:10.1073/pnas.94.4.1396. PMID:9037064.
12. Fischer, W., Perkins, S., Theiler, J., Bhattacharya, T., Yusim, K., Funkhouser, R., et al. 2007. Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat. Med. 13(1): 100-106. doi:10.1038/nm1461. PMID: 17187074.
13. Frater, A.J., Brown, H., Oxenius, A., Gunthard, H.F., Hirschel, B., Robinson, N., et al. 2007. Effective T-cell responses select human immunodeficiency virus mutants and slow disease progression. J. Virol. 81(12): 6742-6751. doi:10.1128/JVI.00022-07. PMID:17409157.
14. Gaschen, B., Taylor, J., Yusim, K., Foley, B., Gao, F., Lang, D., et al. 2002. Diversity considerations in HIV-1 vaccine selection. Science, 296(5577): 2354-2360. doi:10.1126/science.1070441. PMID:12089434.
15. Geels, M.J., Dubey, S.A., Anderson, K., Baan, E., Bakker, M., Pollakis, G., et al. 2005. Broad cross-clade T-cell responses to gag in individuals infected with human immunodeficiency virus type 1 non-B clades (A to G): importance of HLA anchor residue conservation. J. Virol. 79(17): 11247-11258. doi:10.1128/JVI. 79.17.11247-11258.2005. PMID:16103177.
16. Geldmacher, C., Currier, J.R., Herrmann, E., Haule, A., Kuta, E., McCutchan, F., et al. 2007. CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J. Virol. 81(5): 2440-2448.doi:10.1128/JVI.01847-06. PMID:17182686.
17. Goulder, P.J., and Watkins, D.I. 2008. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 8(8): 619-630. doi:10.1038/nri2357. PMID:18617886.
18. Goulder, P.J., Phillips, R.E., Colbert, R.A., McAdam, S., Ogg, G., Nowak, M.A., et al. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3(2): 212-217. doi:10.1038/nm0297-212. PMID:9018241.
19. Groenink, M., Andeweg, A.C., Fouchier, R.A., Broersen, S., van der Jagt, R.C., Schuitemaker, H., et al. 1992. Phenotype-associated env gene variation among eight related human immunodeficiency virus type 1 clones: evidence for in vivo recombination and determinants of cytotropism outside the V3 domain. J. Virol. 66(10): 6175-6180. PMID:1527855.
20. Gudmundsdotter, L., Bernasconi, D., Hejdeman, B., Sandstrom, E., Alaeus, A., Lidman, K., et al. 2008. Cross-clade immune responses to Gag p24 in patients infected with different HIV-1 subtypes and correlation with HLA class I and II alleles. Vaccine, 26(40): 5182-5187. doi:10.1016/j.vaccine.2008.03.094. PMID:18479789.
21. Harari, A., and Pantaleo, G. 2008. HIV-1-specific immune response. Adv. Pharmacol. 56: 75-92. doi:10.1016/S1054-3589(07)56003-5. PMID:18086409.
22. Honeyborne, I., Prendergast, A., Pereyra, F., Leslie, A., Crawford, H., Payne, R., et al. 2007. Control of human immunodeficiency virus type 1 is associated with HLA-B*13 and targeting of multiple gag-specific CD8+ T-cell epitopes. J. Virol. 81(7): 3667-3672. doi:10.1128/JVI.02689-06. PMID:17251285.
23. Jones, N.A., Wei, X., Flower, D.R., Wong, M., Michor, F., Saag, M.S., et al. 2004. Determinants of human immunodeficiency virus type 1 escape from the primary CD8+ cytotoxic T lymphocyte response. J. Exp. Med. 200(10): 1243-1256. doi:10.1084/ jem.20040511. PMID:15545352.
24. Kiepiela, P., Ngumbela, K., Thobakgale, C., Ramduth, D., Honeyborne, I., Moodley, E., et al. 2007. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13(1): 46-53. doi:10.1038/nm1520. PMID: 17173051.
25. Klein, M.R., van der Burg, S.H., Hovenkamp, E., Holwerda, A.M., Drijfhout, J.W., Melief, C.J., and Miedema, F. 1998. Characterization of HLA-B57-restricted human immunodeficiency virus type 1 Gagand RT-specific cytotoxic T lymphocyte responses. J. Gen. Virol. 79(Pt 9): 2191-2201. PMID:9747728.
26. Liang, B., Luo, M., Ball, T.B., and Plummer, F.A. 2007. QUASI analysis of the HIV-1 envelope sequences in the Los Alamos National Laboratory HIV sequence database: pattern and distribution of positive selection sites and their frequencies over years. Biochem. Cell Biol. 85(2): 259-264. doi:10.1139/O06-143. PMID:17534408.
27. Liang, B., Luo, M., Ball, T.B., Yao, X., Van Domselaar, G., Cuff, W.R., et al. 2008. Systematic analysis of host immunological pressure on the envelope gene of human immunodeficiency virus type 1 by an immunobioinformatics approach. Curr. HIV Res. 6(4): 370-379. doi:10.2174/157016208785132554. PMID: 18691035.
28. Malhotra, U., Nolin, J., Mullins, J.I., and McElrath, M.J. 2007. Comprehensive epitope analysis of cross-clade Gag-specific T-cell responses in individuals with early HIV-1 infection in the US epidemic. Vaccine, 25(2): 381-390. doi:10.1016/j.vaccine. 2006.07.045. PMID:17112643.
29. Martinez-Picado, J., Prado, J.G., Fry, E.E., Pfafferott, K., Leslie, A., Chetty, S., et al. 2006. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80(7): 3617-3623. doi:10.1128/ JVI.80.7.3617-3623.2006. PMID:16537629.
30. McKinnon, L.R., Ball, T.B., Kimani, J., Wachihi, C., Matu, L., Luo, M., et al. 2005. Cross-clade CD8(+) T-cell responses with a preference for the predominant circulating clade. J. Acquir. Immune Defic. Syndr. 40(3): 245-249. doi:10.1097/01.qai. 0000184858.16447.04. PMID:16249696.
31. Migueles, S.A., and Connors, M. 2001. Frequency and function of HIV-specific CD8(+) T cells. Immunol. Lett. 79(1-2): 141-150. doi:10.1016/S0165-2478(01)00276-0. PMID:11595301.
32. Moore, C.B., John, M., James, I.R., Christiansen, F.T., Witt, C.S., and Mallal, S.A. 2002. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science, 296(5572): 1439-1443. doi:10.1126/science.1069660. PMID: 12029127.
33. Oxenius, A., Price, D.A., Trkola, A., Edwards, C., Gostick, E., Zhang, H.T., et al. 2004. Loss of viral control in early HIV-1 infection is temporally associated with sequential escape from CD8+ T cell responses and decrease in HIV-1-specific CD4+ and CD8+ T cell frequencies. J. Infect. Dis. 190(4): 713-721. doi:10.1086/422760. PMID:15272399.
34. Payne, R.P., Matthews, P.C., Prado, J.G., and Goulder, P.J. 2009. HLA-mediated control of HIV and HIV adaptation to HLA. Adv. Parasitol. 68: 1-20. doi:10.1016/S0065-308X(08)00601-5. PMID:19289188.
35. Peters, H.O., Mendoza, M.G., Capina, R.E., Luo, M., Mao, X., Gubbins, M., et al. 2008. An integrative bioinformatic approach for studying escape mutations in human immunodeficiency virus type 1 gag in the Pumwani Sex Worker Cohort. J. Virol. 82(4): 1980-1992. doi:10.1128/JVI.02742-06. PMID:18057233.
36. Preston, B.D., Poiesz, B.J., and Loeb, L.A. 1988. Fidelity of HIV-1 reverse transcriptase. Science, 242(4882): 1168-1171. doi:10. 1126/science.2460924. PMID:2460924.
37. Ross, H.A., and Rodrigo, A.G. 2002. Immune-mediated positive selection drives human immunodeficiency virus type 1 molecular variation and predicts disease duration. J. Virol. 76(22): 11715-1720. doi:10.1128/JVI.76.22.11715-11720.2002. PMID: 12388731.
38. Sacha, J.B., Chung, C., Rakasz, E.G., Spencer, S.P., Jonas, A.K., Bean, A.T., et al. 2007. Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178(5): 2746-2754. PMID: 17312117.
39. Schmitz, J.E., Johnson, R.P., McClure, H.M., Manson, K.H., Wyand, M.S., Kuroda, M.J., et al. 2005. Effect of CD8+ lymphocyte depletion on virus containment after simian immunodeficiency virus SIVmac251 challenge of live attenuated SIVmac239delta3-vaccinated rhesus macaques. J. Virol. 79(13):8131-8141. doi:10.1128/JVI.79.13.8131-8141.2005. PMID: 15956558.
40. Schneidewind, A., Brockman, M.A., Yang, R., Adam, R.I., Li, B., Le Gall, S., 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(22): 12382-12393. doi:10.1128/ JVI.01543-07. PMID:17804494.
41. Stewart, J.J., Watts, P., and Litwin, S. 2001. An algorithm for mapping positively selected members of quasispecies-type viruses. BMC Bioinformatics, 2(1): 1. doi:10.1186/1471-2105-2-1. PMID:11265061.
42. Travers, S.A., O'Connell, M.J., McCormack, G.P., and McInerney, J.O. 2005. Evidence for heterogeneous selective pressures in the evolution of the env gene in different human immunodeficiency virus type 1 subtypes. J. Virol. 79(3): 1836-1841. doi:10.1128/ JVI.79.3.1836-1841.2005. PMID:15650207.
43. Turnbull, E.L., Lopes, A.R., Jones, N.A., Cornforth, D., Newton, P., Aldam, D., et al. 2006. HIV-1 epitope-specific CD8+ T cell responses strongly associated with delayed disease progression cross-recognize epitope variants efficiently. J. Immunol. 176(10): 6130-6146. PMID:16670322.
44. Yusim, K., Kesmir, C., Gaschen, B., Addo, M.M., Altfeld, M., Brunak, S., et al. 2002. Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation. J. Virol. 76(17): 8757-8768. doi:10.1128/JVI.76.17. 8757-8768.2002. PMID:12163596.