Functional consequences of human immunodeficiency virus escape from an HLA-B*13-restricted CD8+ T-cell epitope in p1 gag protein

Journal of Virology

Volumn 83, Issue 2, 2009, Pages 1018-1025

  Prado, Julia G ^a   Honeyborne, Isobella ^a   Brierley, Ian ^b   Puertas, Maria Carmen ^c   Martinez Picado, Javier ^c,d   Goulder, Philip J R ^a,e,f  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^e UNIVERSITY OF KWAZULU NATAL   (South Africa)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAG PROTEIN; HLA B ANTIGEN;

AMINO ACID SUBSTITUTION; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR RECOGNITION; MUTATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOMAL FRAMESHIFTING;

AMINO ACID SUBSTITUTION; CELL LINE; EPITOPES, T-LYMPHOCYTE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HLA-B ANTIGENS; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 58149517692     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01882-08     Document Type: Article

References (51)

1. Baril, M., D. Dulude, K. Gendron, G. Lemay, and L. Brakier-Gingras. 2003. Efficiency of a programmed 1 ribosomal frameshift in the different subtypes of the human immunodeficiency virus type 1 group M. RNA 9:1246-1253.
2. Bidou, L., G. Stahl, B. Grima, H. Liu, M. Cassan, and J. P. Rousset. 1997. In vivo HIV-1 frameshifting efficiency is directly related to the stability of the stem-loop stimulatory signal. RNA 3:1153-1158.
3. Brander, C., N. Frahm, and B. D. Walker. 2006. The challenges of host and viral diversity in HIV vaccine design. Curr. Opin. Immunol. 18:430-437.
4. Brockman, M. A., A. Schneidewind, M. Lahaie, A. Schmidt, T. Miura, I. Desouza, F. Ryvkin, C. A. Derdeyn, S. Allen, E. Hunter, J. Mulenga, P. A. Goepfert, B. D. Walker, and T. M. Allen. 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.
5. Brumme, Z. L., I. Tao, S. Szeto, C. J. Brumme, J. M. Carlson, D. Chan, C. Kadie, N. Frahm, C. Brander, B. Walker, D. Heckerman, and P. R. Harrigan. 2008. Human leukocyte antigen-specific polymorphisms in HIV-1 Gag and their association with viral load in chronic untreated infection. AIDS 22:1277-1286.
6. Butz, E. A., and M. J. Bevan. 1998. Massive expansion of antigen-specific CD8 T cells during an acute virus infection. Immunity 8:167-175.
7. Gag late domain associated with drug resistance. J. Virol. 82:495-502.
8. Chopera, D. R., Z. Woodman, K. Mlisana, M. Mlotshwa, D. P. Martin, C. Seoighe, F. Treurnicht, D. A. de Rosa, W. Hide, S. A. Karim, C. M. Gray, and C. Williamson. 2008. Transmission of HIV-1 CTL escape variants provides HLA-mismatched recipients with a survival advantage. PLoS Pathog 4:e1000033.
9. Crawford, H., J. G. Prado, A. Leslie, S. Hue, I. Honeyborne, S. Reddy, M. van der Stok, Z. Mncube, C. Brander, C. Rousseau, J. I. Mullins, R. Kaslow, P. Goepfert, S. Allen, E. Hunter, J. Mulenga, P. Kiepiela, B. D. Walker, and P. J. Goulder. 2007. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLAB*5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 81:8346-8351.
10. da Silva, J. 2003. The evolutionary adaptation of HIV-1 to specific immunity. Curr. HIV Res. 1:363-371.
11. Dulude, D., Y. A. Berchiche, K. Gendron, L. Brakier-Gingras, and N. Heveker. 2006. Decreasing the frameshift efficiency translates into an equivalent reduction of the replication of the human immunodeficiency virus type 1. Virology 345:127-136.
12. + 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.
13. Feeney, M. E., Y. Tang, K. A. Roosevelt, A. J. Leslie, K. McIntosh, N. Karthas, B. D. Walker, and P. J. Goulder. 2004. 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. 78:8927-8930.
14. Gaudin, C., M. H. Mazauric, M. Traikia, E. Guittet, S. Yoshizawa, and D. Fourmy. 2005. Structure of the RNA signal essential for translational frameshifting in HIV-1. J. Mol. Biol. 349:1024-1035.
15. Girnary, R., L. King, L. Robinson, R. Elston, and I. Brierley. 2007. Structure-function analysis of the ribosomal frameshifting signal of two human immunodeficiency virus type 1 isolates with increased resistance to viral protease inhibitors. J. Gen. Virol. 88:226-235.
16. Goepfert, P. A., W. Lumm, P. Farmer, P. Matthews, A. Prendergast, J. M. Carlson, C. A. Derdeyn, J. Tang, R. A. Kaslow, A. Bansal, K. Yusim, D. Heckerman, J. Mulenga, S. Allen, P. J. Goulder, and E. Hunter. 2008. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J. Exp. Med. 205:1009-1017.
17. Goulder, P. J., M. M. Addo, M. A. Altfeld, E. S. Rosenberg, Y. Tang, U. Govender, N. Mngqundaniso, K. Annamalai, T. U. Vogel, M. Hammond, M. Bunce, H. M. Coovadia, and B. D. Walker. 2001. Rapid definition of five novel HLA-A*3002-restricted human immunodeficiency virus-specific cytotoxic T-lymphocyte epitopes by Elispot and intracellular cytokine staining assays. J. Virol. 75:1339-1347.
18. Goulder, P. J., R. E. Phillips, R. A. Colbert, S. McAdam, G. Ogg, M. A. Nowak, P. Giangrande, G. Luzzi, B. Morgan, A. Edwards, A. J. McMichael, and S. Rowland-Jones. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
19. Goulder, P. J., and D. I. Watkins. 2004. HIV and SIV CTL escape: implications for vaccine design. Nat. Rev. Immunol. 4:630-640.
20. Harrer, E. G., S. Bergmann, K. Eismann, M. Rittmaier, A. Goldwich, S. M. Muller, B. M. Spriewald, and T. Harrer. 2005. A conserved HLA B13-restricted cytotoxic T lymphocyte epitope in Nef is a dominant epitope in HLA B13-positive HIV-1-infected patients. AIDS 19:734-735.
21. Hill, M. K., M. Shehu-Xhilaga, S. M. Crowe, and J. Mak. 2002. Proline residues within spacer peptide p1 are important for human immunodeficiency virus type 1 infectivity, protein processing, and genomic RNA dimer stability. J. Virol. 76:11245-11253.
22. + T-cell epitopes. J. Virol. 81:3667-3672.
23. Hung, M., P. Patel, S. Davis, and S. R. Green. 1998. Importance of ribosomal frameshifting for human immunodeficiency virus type 1 particle assembly and replication. J. Virol. 72:4819-4824.
24. Karacostas, V., E. J. Wolffe, K. Nagashima, M. A. Gonda, and B. Moss. 1993. Overexpression of the HIV-1 gag-pol polyprotein results in intracellular activation of HIV-1 protease and inhibition of assembly and budding of virus-like particles. Virology 193:661-671.
25. Kiepiela, P., A. J. Leslie, I. Honeyborne, D. Ramduth, C. Thobakgale, S. Chetty, P. Rathnavalu, C. Moore, K. J. Pfafferott, L. Hilton, P. Zimbwa, S. Moore, T. Allen, C. Brander, M. M. Addo, M. Altfeld, I. James, S. Mallal, M. Bunce, L. D. Barber, J. Szinger, C. Day, P. Klenerman, J. Mullins, B. Korber, H. M. Coovadia, B. D. Walker, and P. J. Goulder. 2004. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432:769-775.
26. + T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
27. Laalami, S., G. Grentzmann, L. Bremaud, and Y. Cenatiempo. 1996. Messenger RNA translation in prokaryotes: GTPase centers associated with translational factors. Biochimie 78:577-589.
28. 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, M. Altfeld, C. Brander, C. Dixon, D. Ramduth, P. Jeena, S. A. Thomas, A. St John, T. A. Roach, B. Kupfer, G. Luzzi, A. Edwards, G. Taylor, H. Lyall, G. Tudor-Williams, V. Novelli, J. Martinez-Picado, P. Kiepiela, B. D. Walker, and P. J. Goulder. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10:282-289.
29. Loffredo, J. T., J. Maxwell, Y. Qi, C. E. Glidden, G. J. Borchardt, T. Soma, A. T. Bean, D. R. Beal, N. A. Wilson, W. M. Rehrauer, J. D. Lifson, M. Carrington, and D. I. Watkins. 2007. Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J. Virol. 81:8827-8832.
30. Martinez-Picado, J., J. G. Prado, E. E. Fry, K. Pfafferott, A. Leslie, S. Chetty, C. Thobakgale, I. Honeyborne, H. Crawford, P. Matthews, T. Pillay, C. Rousseau, J. I. Mullins, C. Brander, B. D. Walker, D. I. Stuart, P. Kiepiela, and P. Goulder. 2006. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80:3617-3623.
31. Martinez-Picado, J., L. Sutton, M. P. De Pasquale, A. V. Savara, and R. T. D'Aquila. 1999. Human immunodeficiency virus type 1 cloning vectors for antiretroviral resistance testing. J. Clin. Microbiol. 37:2943-2951.
32. Matthews, P. C., A. Prendergast, A. Leslie, H. Crawford, R. Payne, C. Rousseau, M. Rolland, I. Honeyborne, J. Carlson, C. Kadie, C. Brander, K. Bishop, N. Mlotshwa, J. I. Mullins, H. Coovadia, T. Ndung'u, B. D. Walker, D. Heckerman, and P. J. Goulder. 2008. Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J. Virol. 82:8548-8559.
33. Migueles, S. A., M. S. Sabbaghian, W. L. Shupert, M. P. Bettinotti, F. M. Marincola, L. Martino, C. W. Hallahan, S. M. Selig, D. Schwartz, J. Sullivan, and M. Connors. 2000. HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc. Natl. Acad. Sci. USA 97:2709-2714.
34. Moriyama, E. N., Y. Ina, K. Ikeo, N. Shimizu, and T. Gojobori. 1991. Mutation pattern of human immunodeficiency virus gene. J. Mol. Evol. 32:360-363.
35. Muench, L. J., and H. Reed. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
36. O'Brien, S. J., X. Gao, and M. Carrington. 2001. HLA and AIDS: a cautionary tale. Trends Mol. Med. 7:379-381.
37. O'Connor, D. H., B. R. Mothe, J. T. Weinfurter, S. Fuenger, W. M. Rehrauer, P. Jing, R. R. Rudersdorf, M. E. Liebl, K. Krebs, J. Vasquez, E. Dodds, J. Loffredo, S. Martin, A. B. McDermott, T. M. Allen, C. Wang, G. G. Doxiadis, D. C. Montefiori, A. Hughes, D. R. Burton, D. B. Allison, S. M. Wolinsky, R. Bontrop, L. J. Picker, and D. I. Watkins. 2003. Major histocompatibility complex class I alleles associated with slow simian immunodeficiency virus disease progression bind epitopes recognized by dominant acute-phase cytotoxic-T-lymphocyte responses. J. Virol. 77:9029-9040.
38. Park, J., and C. D. Morrow. 1991. Overexpression of the gag-pol precursor from human immunodeficiency virus type 1 proviral genomes results in efficient proteolytic processing in the absence of virion production. J. Virol. 65:5111-5117.
39. Parkin, N. T., M. Chamorro, and H. E. Varmus. 1992. Human immunodeficiency virus type 1 gag-pol frameshifting is dependent on downstream mRNA secondary structure: demonstration by expression in vivo. J. Virol. 66:5147-5151.
40. Pettit, S. C., J. N. Lindquist, A. H. Kaplan, and R. Swanstrom. 2005. Processing sites in the human immunodeficiency virus type 1 (HIV-1) Gag-Pro-Pol precursor are cleaved by the viral protease at different rates. Retrovirology 2:66.
41. Peyerl, F. W., D. H. Barouch, and N. L. Letvin. 2004. Structural constraints on viral escape from HIV- and SIV-specific cytotoxic T-lymphocytes. Viral Immunol. 17:144-151.
42. Plikat, U., K. Nieselt-Struwe, and A. Meyerhans. 1997. Genetic drift can dominate short-term human immunodeficiency virus type 1 nef quasispecies evolution in vivo. J. Virol. 71:4233-4240.
43. Prado, J. G., S. Franco, T. Matamoros, L. Ruiz, B. Clotet, L. Menendez-Arias, M. A. Martinez, and J. Martinez-Picado. 2004. Relative replication fitness of multi-nucleoside analogue-resistant HIV-1 strains bearing a dipeptide insertion in the fingers subdomain of the reverse transcriptase and mutations at codons 67 and 215. Virology 326:103-112.
44. Schneidewind, A., M. A. Brockman, J. Sidney, Y. E. Wang, H. Chen, T. J. Suscovich, B. Li, R. I. Adam, R. L. Allgaier, B. R. Mothe, T. Kuntzen, C. Oniangue-Ndza, A. Trocha, X. G. Yu, C. Brander, A. Sette, B. D. Walker, and T. M. Allen. 2008. Structural and functional constraints limit options for cytotoxic T-lymphocyte escape in the immunodominant HLA-B27-restricted epitope in human immunodeficiency virus type 1 capsid. J. Virol. 82:5594-5605.
45. 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, T. Kuntzen, C. S. Tung, M. X. LaBute, S. M. Mueller, T. Harrer, A. J. McMichael, P. J. Goulder, C. Aiken, C. Brander, A. D. Kelleher, and T. M. Allen. 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.
46. Shehu-Xhilaga, M., S. M. Crowe, and J. Mak. 2001. Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity. J. Virol. 75:1834-1841.
47. Telenti, A., R. Martinez, M. Munoz, G. Bleiber, G. Greub, D. Sanglard, and S. Peters. 2002. Analysis of natural variants of the human immunodeficiency virus type 1 gag-pol frameshift stem-loop structure. J. Virol. 76:7868-7873.
48. Weber, J., J. Weberova, M. Carobene, M. Mirza, J. Martinez-Picado, P. Kazanjian, and M. E. Quinones-Mateu. 2006. Use of a novel assay based on intact recombinant viruses expressing green (eGFP) or red (DsRed2) fluorescent proteins to examine the contribution of pol and env genes to overall HIV-1 replicative fitness. J. Virol. Methods 136:102-117.
49. Yant, L. J., T. C. Friedrich, R. C. Johnson, G. E. May, N. J. Maness, A. M. Enz, J. D. Lifson, D. H. O'Connor, M. Carrington, and D. I. Watkins. 2006. The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J. Virol. 80:5074-5077.
50. Zar, J. H. 1984. Biostatistical analysis, 2nd ed., p. 396-439. Prentice-Hall, Inc., Englewood Cliffs, NJ.
51. Zuñiga, R., A. Lucchetti, P. Galvan, S. Sanchez, C. Sanchez, A. Hernandez, H. Sanchez, N. Frahm, C. H. Linde, H. S. Hewitt, W. Hildebrand, M. Altfeld, T. M. Allen, B. D. Walker, B. T. Korber, T. Leitner, J. Sanchez, and C. Brander. 2006. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J. Virol. 80:3122-3125.