Selection of escape mutant by HLA-C-restricted HIV-1 Pol-specific cytotoxic T lymphocytes carrying strong ability to suppress HIV-1 replication

European Journal of Immunology

Volumn 41, Issue 1, 2011, Pages 97-106

  Honda, Kazutaka ^a   Zheng, Nan ^a   Murakoshi, Hayato ^a   Hashimoto, Masao ^a   Sakai, Keiko ^a   Borghan, Mohamed Ali ^a,b   Chikata, Takayuki ^a   Koyanagi, Madoka ^a   Tamura, Yoshiko ^a   Gatanaga, Hiroyuki ^a,c   Oka, Shinichi ^a,c   Takiguchi, Masafumi ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF NIZWA   (Oman)

^c NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

Author keywords

CTL; Escape mutation; Fitness; HIV infection; HLA C

Indexed keywords

HLA A ANTIGEN; HLA C ANTIGEN; POL PROTEIN;

ALLELE; ARTICLE; CD8+ T LYMPHOCYTE; CELL CLONING; CELL SPECIFICITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SUBSTITUTION REACTION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; EPITOPES, T-LYMPHOCYTE; HIV INFECTIONS; HIV-1; HLA-C ANTIGENS; HUMANS; IMMUNE EVASION; MOLECULAR SEQUENCE DATA; MUTATION; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; SELECTION, GENETIC; T-LYMPHOCYTES, CYTOTOXIC; VIRUS REPLICATION;

EID: 78650391873     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201040841     Document Type: Article

References (43)

1. Ogg, G. S., Jin, X., Bonhoeffer, S., Dunbar, P. R., Nowak, M. A., Monard, S., Segal, J. P. et al., Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 1998. 279: 2103-2106.
2. Goulder, P. J. and Watkins, D. I., Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat. Rev. Immunol. 2008. 8: 619-630.
3. *5101. J. Virol. 2010. 84: 7151-7160.
4. Borrow, P., Lewicki, H., Wei, X., Horwitz, M. S., Peffer, N., Meyers, H., Nelson, J. A. 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.
5. Koup, R. A., Safrit, J. T., Cao, Y., Andrews, C. A., McLeod, G., Borkowsky, W., Farthing, C. 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.
6. Harrer, E., Harrer, T., Buchbinder, S., Mann, D. L., Feinberg, M., Yilma, T., Johnson, R. P. et al., HIV-1-specific cytotoxic T lymphocyte response in healthy, long-term nonprogressing seropositive persons. AIDS Res. Hum. Retroviruses 1994. 10: S77-S78.
7. Rinaldo, C., Huang, X. L., Fan, Z. F., Ding, M., Beltz, L., Logar, A., Panicali, D. et al., High levels of anti-human 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.
8. Gandhi, R. T. and Walker, B. D., Immunologic control of HIV-1. Annu. Rev. Med. 2002. 53: 149-172.
9. Goulder, P. J., Phillips, R. E., Colbert, R. A., McAdam, S., Ogg, G., Nowak, M. A., Giangrande, P. et al., Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 1997. 3: 212-217.
10. Price, D. A., Goulder, P. J., Klenerman, P., Sewell, A. K., Easterbrook, P. J., Troop, M., Bangham, C. R. et al., Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 1997. 94: 1890-1895.
11. Kelleher, A. D., Long, C., Holmes, E. C., Allen, R. L., Wilson, J., Conlon, C., Workman, C. et al., Clustered mutations in HIV-1 gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J. Exp. Med. 2001. 193: 375-386.
12. Fujiwara, M., Tanuma, J., Koizumi, H., Kawashima, Y., Honda, K., Mastuoka-Aizawa, S., Dohki, S. et al., Different abilities of escape mutant-specific cytotoxic T cells to suppress replication of escape mutant and wild-type human immunodeficiency virus type 1 in new hosts. J. Virol. 2008. 82: 138-147.
13. Cohen, G. B., Gandhi, R. T., Davis, D. M., Mandelboim, O., Chen, B. K., Strominger, J. L. and Baltimore, D., The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 1999. 10: 661-671.
14. Williams, M., Roeth, J. F., Kasper, M. R., Fleis, R. I., Przybycin, C. G. and Collins, K. L., Direct binding of human immunodeficiency virus type 1 Nef to the major histocompatibility complex class I (MHC-I) cytoplasmic tail disrupts MHC-I trafficking. J. Virol. 2002. 76: 12173-12184.
15. Arien, K. K. and Verhasselt, B., HIV Nef: role in pathogenesis and viral fitness. Curr. HIV Res. 2008. 6: 200-208.
16. Lama, J., The physiological relevance of CD4 receptor down-modulation during HIV infection. Curr. HIV Res. 2003. 1: 167-184.
17. Chowers, M. Y., Spina, C. A., Kwoh, T. J., Fitch, N. J., Richman, D. D. and Guatelli, J. C., Optimal infectivity in vitro of human immunodeficiency virus type 1 requires an intact nef gene. J. Virol. 1994. 68: 2906-2914.
18. Couillin, I., Connan, F., Culmann-Penciolelli, B., Gomard, E., Guillet, J. G. and Choppin, J., HLA-dependent variations in human immunodeficiency virus Nef protein alter peptide/HLA binding. Eur. J. Immunol. 1995. 25: 728-732.
19. *5401-positive individuals. Hum. Immunol. 2010. 71: 123-127.
20. Allen, T. M., O'Connor, D. H., Jing, P., Dzuris, J. L., Mothe, B. R., Vogel, T. U., Dunphy, E. et al., Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 2000. 407: 386-390.
21. Evans, D. T., O'Connor, D. H., Jing, P., Dzuris, J. L., Sidney, J., da Silva, J., Allen, T. M. et al., Virus-specific cytotoxic T-lymphocyte responses select for amino-acid variation in simian immunodeficiency virus Env and Nef. Nat. Med. 1999. 5: 1270-1276.
22. McMichael, A. J. and Rowland-Jones, S. L., Cellular immune responses to HIV. Nature 2001. 410: 980-987.
23. Barouch, D. H., Kunstman, J., Kuroda, M. J., Schmitz, J. E., Santra, S., Peyerl, F. W., Krivulka, G. R. et al., Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 2002. 415: 335-339.
24. Feeney, M. E., Tang, Y., Roosevelt, K. A., Leslie, A. J., McIntosh, K., Karthas, N., Walker, B. D. et al., Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-term-nonprogressing child. J. Virol. 2004. 78: 8927-8930.
25. Kawashima, Y., Pfafferott, K., Frater, J., Matthews, P., Payne, R., Addo, M., Gatanaga, H. et al., Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009. 458: 641-645.
26. Neisig, A., Melief, C. J. and Neefjes, J., Reduced cell surface expression of HLA-C molecules correlates with restricted peptide binding and stable TAP interaction. J. Immunol. 1998. 160: 171-179.
27. McCutcheon, J. A., Gumperz, J., Smith, K. D., Lutz, C. T. and Parham, P., Low HLA-C expression at cell surfaces correlates with increased turnover of heavy chain mRNA. J. Exp. Med. 1995. 181: 2085-2095.
28. Adnan, S., Balamurugan, A., Trocha, A., Bennett, M. S., Ng, H. L., Ali, A., Brander, C. et al., Nef interference with HIV-1-specific CTL antiviral activity is epitope specific. Blood 2006. 108: 3414-3419.
29. Fellay, J., Shianna, K. V., Ge, D., Colombo, S., Ledergerber, B., Weale, M., Zhang, K. et al., A whole-genome association study of major determinants for host control of HIV-1. Science 2007. 317: 944-947.
30. van Manen, D., Kootstra, N. A., Boeser-Nunnink, B., Handulle, M. A., van't Wout, A. B. and Schuitemaker, H., Association of HLA-C and HCP5 gene regions with the clinical course of HIV-1 infection. AIDS 2009. 23: 19-28.
31. Makadzange, A. T., Gillespie, G., Dong, T., Kiama, P., Bwayo, J., Kimani, J., Plummer, F. et al., Characterization of an HLA-C restricted CTL response in chronic HIV infection. Eur. J. Immunol. 2010. 40:1036-1041.
32. Rousseau, C. M., Daniels, M. G., Carlson, J. M., Kadie, C., Crawford, H., Prendergast, A., Matthews, P. et al., HLA class I-driven evolution of human immunodeficiency virus type 1 subtype c proteome: immune escape and viral load. J. Virol. 2008. 82: 6434-6446.
33. Matthews, P. C., Prendergast, A., Leslie, A., Crawford, H., Payne, R., Rousseau, C., Rolland, M. et al., Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J. Virol. 2008. 82: 8548-8559.
34. De Groot, A. S., Jesdale, B., Martin, W., Saint Aubin, C., Sbai, H., Bosma, A., Lieberman, J. et al., Mapping cross-clade HIV-1 vaccine epitopes using a bioinformatics approach. Vaccine 2003. 21: 4486-4504.
35. Tomiyama, H., Fujiwara, M., Oka, S. and Takiguchi, M., Cutting edge: epitope-dependent effect of Nef-mediated HLA class I down-regulation on ability of HIV-1-specific CTLs to suppress HIV-1 replication. J. Immunol. 2005. 174: 36-40.
36. Tomiyama, H., Akari, H., Adachi, A. and Takiguchi, M., Different effects of Nef-mediated HLA class I down-regulation on human immunodeficiency virus type 1-specific CD8(+) T-cell cytolytic activity and cytokine production. J. Virol. 2002. 76: 7535-7543.
37. Koizumi, H., Hashimoto, M., Fujiwara, M., Murakoshi, H., Chikata, T., Borghan, M. A., Hachiya, A. et al., Different in vivo effects of HIV-1 immunodominant epitope-specific cytotoxic T lymphocytes on selection of escape mutant viruses. J. Virol. 2010. 84: 5508-5519.
38. Kiepiela, P., Leslie, A. J., Honeyborne, I., Ramduth, D., Thobakgale, C., Chetty, S., Rathnavalu, P. et al., Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 2004. 432: 769-775.
39. Akari, H., Arold, S., Fukumori, T., Okazaki, T., Strebel, K. and Adachi, A., Nef-induced major histocompatibility complex class I down-regulation is functionally dissociated from its virion incorporation, enhancement of viral infectivity, and CD4 down-regulation. J. Virol. 2000. 74: 2907-2912.
40. Thomas, R., Apps, R., Qi, Y., Gao, X., Male, V., O'HUigin, C., O'Connor, G. et al., HLA-C cell surface expression and control of HIV/AIDS correlate with a variant upstream of HLA-C. Nat. Genet. 2009. 41: 1290-1294.
41. *5401-restricted HIV-1-Nef and Pol-specific CTL epitopes. Microbes Infect. 2008. 10: 764-772.
42. Zheng, N., Fujiwara, M., Ueno, T., Oka, S. and Takiguchi, M., Strong ability of Nef-specific CD4+cytotoxic T cells to suppress human immunodeficiency virus type 1 (HIV-1) replication in HIV-1-infected CD4+T cells and macrophages. J. Virol. 2009. 83: 7668-7677.
43. Gatanaga, H., Hachiya, A., Kimura, S. and Oka, S., Mutations other than 103N in human immunodeficiency virus type 1 reverse transcriptase (RT) emerge from K103R polymorphism under non-nucleoside RT inhibitor pressure. Virology 2006. 344: 354-362.