CD8 T cell response and evolutionary pressure to HIV-1 cryptic epitopes derived from antisense transcription

Journal of Experimental Medicine

Volumn 207, Issue 1, 2010, Pages 51-59

  Bansal, Anju ^a   Carlson, Jonathan ^d   Yan, Jiyu ^a   Akinsiku, Olusimidele T ^b   Schaefer, Malinda ^e,f   Sabbaj, Steffanie ^a   Bet, Anne ^b   Levy, David N ^g   Heath, Sonya ^a   Tang, Jianming ^a,b   Kaslow, Richard A ^c   Walker, Bruce D ^h,i   Ndung'u, Thumbi ^h,i   Goulder, Philip J ^h,i,j   Heckerman, David ^d   Hunter, Eric ^e,f   Goepfert, Paul A ^a,b  

^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 MICROSOFT RESEARCH   (United States)

^e EMORY UNIVERSITY   (United States)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

^h MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

ⁱ UNIVERSITY OF KWAZULU NATAL   (South Africa)

^j UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAG PROTEIN; HLA ANTIGEN CLASS 1; NEF PROTEIN; POL PROTEIN;

ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COHORT ANALYSIS; CONTROLLED STUDY; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOGENICITY; MAJOR CLINICAL STUDY; NUCLEIC ACID PROBE; OPEN READING FRAME; PREDICTION; PRIORITY JOURNAL; SOUTH AFRICA; VIRUS GENOME; VIRUS IMMUNITY;

CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CHRONIC DISEASE; COHORT STUDIES; EPITOPES, T-LYMPHOCYTE; EVOLUTION, MOLECULAR; FEMALE; GENE PRODUCTS, GAG; GENES, MHC CLASS I; HIV INFECTIONS; HIV-1; HUMANS; MALE; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; POL GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; POLYMORPHISM, GENETIC; RNA, ANTISENSE; RNA, VIRAL; SOUTH AFRICA; TRANSCRIPTION, GENETIC;

EID: 76149107149     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20092060     Document Type: Article

References (40)

1. Altfeld, M., E.S. Rosenberg, R. Shankarappa, J.S. Mukherjee, F.M. Hecht, R.L. Eldridge, M.M. Addo, S.H. Poon, M.N. Phillips, G.K. Robbins, et al. 2001. Cellular immune responses and viral diversity in individuals treated during acute and early HIV-1 infection. J. Exp. Med. 193:169-180. doi:10.1084/jem.193.2.169
2. Bansal, A., L. Yue, J. Conway, K. Yusim, J. Tang, J. Kappes, R.A. Kaslow, C.M. Wilson, and P.A. Goepfert. 2007. Immunological control of chronic HIV-1 infection: HLA-mediated immune function and viral evolution in adolescents. AIDS. 21:2387-2397. doi:10.1097/QAD .0b013e3282f13823
3. Bansal, A., B. Jackson, K. West, S. Wang, S. Lu, J.S. Kennedy, and P.A. Goepfert. 2008. Multifunctional T-cell characteristics induced by a polyvalent DNA prime/protein boost human immunodeficiency virus type 1 vaccine regimen given to healthy adults are dependent on the route and dose of administration. J. Virol. 82:6458-6469. doi:10.1128/ JVI.00068-08
4. Betts, M.R., D.R. Ambrozak, D.C. Douek, S. Bonhoeffer, J.M. Brenchley, J.P. Casazza, R.A. Koup, and L.J. Picker. 2001. Analysis of total human immunodeficiency virus (HIV)-specific CD4(+) and CD8(+) T-cell responses: relationship to viral load in untreated HIV infection. J. Virol. 75:11983-11991. doi:10.1128/JVI.75.24.11983-11991.2001
5. Bruce, A.G., J.F. Atkins, and R.F. Gesteland. 1986. tRNA anticodon replacement experiments show that ribosomal frameshifting can be caused by doublet decoding. Proc. Natl. Acad. Sci. USA. 83:5062-5066. doi:10.1073/ pnas.83.14.5062
6. Brumme, Z.L., C.J. Brumme, J. Carlson, H. Streeck, M. John, Q. Eichbaum, B.L. Block, B. Baker, C. Kadie, M. Markowitz, et al. 2008. Marked epitopeand allele-specific differences in rates of mutation in human immuno-deficiency type 1 (HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/early HIV-1 infection. J. Virol. 82:9216-9227. doi:10 .1128/JVI.01041-08
7. Buchbinder, S.P., D.V. Mehrotra, A. Duerr, D.W. Fitzgerald, R. Mogg, D. Li, P.B. Gilbert, J.R. Lama, M. Marmor, C. Del Rio, et al; Step Study Protocol Team. 2008. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet. 372:1881-1893. doi:10.1016/ S0140-6736(08)61591-3
8. Bullock, T.N., A.E. Patterson, L.L. Franlin, E. Notidis, and L.C. Eisenlohr. 1997. Initiation codon scanthrough versus termination codon readthrough demonstrates strong potential for major histocompatibility complex class I-restricted cryptic epitope expression. J. Exp. Med. 186:1051-1058. doi:10.1084/jem.186.7.1051
9. Cardinaud, S., A. Moris, M. Février, P.S. Rohrlich, L. Weiss, P. Langlade-Demoyen, F.A. Lemonnier, O. Schwartz, and A. Habel. 2004. Identification of cryptic MHC I-restricted epitopes encoded by HIV-1 alternative reading frames. J. Exp. Med. 199:1053-1063. doi:10.1084/jem.20031869
10. Carlson, J.M., Z.L. Brumme, C.M. Rousseau, C.J. Brumme, P. Matthews, C. Kadie, J.I. Mullins, B.D. Walker, P.R. Harrigan, P.J. Goulder, and D. Heckerman. 2008. Phylogenetic dependency networks: inferring patterns of CTL escape and codon covariation in HIV-1 Gag. PLOS Comput. Biol. 4:e1000225. doi:10.1371/journal.pcbi.1000225
11. Flynn, N.M., D.N. Forthal, C.D. Harro, F.N. Judson, K.H. Mayer, and M.F. Para; rgp120 HIV Vaccine Study Group. 2005. Placebo-controlled phase 3 trial of a recombinant glycoprotein 120 vaccine to prevent HIV-1 infection. J. Infect. Dis. 191:654-665. doi:10.1086/428404
12. Garrison, K.E., S. Champiat, V.A. York, A.T. Agrawal, E.G. Kallas, J.N. Martin, F.M. Hecht, S.G. Deeks, and D.F. Nixon. 2009. Transcriptional errors in human immunodeficiency virus type 1 generate targets for T-cell responses. Clin. Vaccine Immunol. 16:1369-1371. doi:10.1128/CVI.00410-08
13. Gaudin, C., M.H. Mazauric, M. Traïkia, 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. doi:10.1016/ j.jmb.2005.04.045
14. Goepfert, P.A., W. Lumm, P. Farmer, P. Matthews, A. Prendergast, J.M. Carlson, C.A. Derdeyn, J. Tang, R.A. Kaslow, A. Bansal, et al. 2008. Transmission of HIV-1 Gag immune escape mutations is associated with reduced viral load in linked recipients. J. Exp. Med. 205:1009-1017. doi:10.1084/jem.20072457
15. Goonetilleke, N., M.K. Liu, J.F. Salazar-Gonzalez, G. Ferrari, E. Giorgi, V.V. Ganusov, B.F. Keele, G.H. Learn, E.L. Turnbull, M.G. Salazar, et al; CHAVI Clinical Core B. 2009. The first T cell response to transmitted/ founder virus contributes to the control of acute viremia in HIV-1 infection. J. Exp. Med. 206:1253-1272. doi:10.1084/jem.20090365
16. He, Y., B. Vogelstein, V.E. Velculescu, N. Papadopoulos, and K.W. Kinzler. 2008. The antisense transcriptomes of human cells. Science. 322:1855-1857. doi:10.1126/science.1163853
17. Heckerman, D., C. Kadie, and J. Listgarten. 2007. Leveraging information across HLA alleles/supertypes improves epitope prediction. J. Comput. Biol. 14:736-746. doi:10.1089/cmb.2007.R013
18. Kawashima, Y., K. Pfafferott, J. Frater, P. Matthews, R. Payne, M. Addo, H. Gatanaga, M. Fujiwara, A. Hachiya, H. Koizumi, et al. 2009. Adaptation of HIV-1 to human leukocyte antigen class I. Nature. 458:641-645. doi:10.1038/nature07746
19. 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. doi:10.1038/nm1520
20. Landry, S., M. Halin, S. Lefort, B. Audet, C. Vaquero, J.M. Mesnard, and B. Barbeau. 2007. Detection, characterization and regulation of antisense transcripts in HIV-1. Retrovirology. 4:71. doi:10.1186/1742-4690-4-71
21. Li, B., A.D. Gladden, M. Altfeld, J.M. Kaldor, D.A. Cooper, A.D. Kelleher, and T.M. Allen. 2007. Rapid reversion of sequence polymorphisms dominates early human immunodeficiency virus type 1 evolution. J. Virol. 81:193-201. doi:10.1128/JVI.01231-06
22. Liu, J., K.L. O'Brien, D.M. Lynch, N.L. Simmons, A. La Porte, A.M. Riggs, P. Abbink, R.T. Coffey, L.E. Grandpre, M.S. Seaman, et al. 2009. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature. 457:87-91.
23. Ludwig, L.B., J.L. Ambrus Jr., K.A. Krawczyk, S. Sharma, S. Brooks, C.B. Hsiao, and S.A. Schwartz. 2006. Human immunodeficiency virus-type 1 LTR DNA contains an intrinsic gene producing antisense RNA and protein products. Retrovirology. 3:80. doi:10.1186/1742-4690-3-80
24. Malarkannan, S., T. Horng, P.P. Shih, S. Schwab, and N. Shastri. 1999. Presentation of out-of-frame peptide/MHC class I complexes by a novel translation initiation mechanism. Immunity. 10:681-690. doi:10.1016/S1074-7613(00)80067-9
25. + T lymphocytes against an immunodominant cryptic epitope select for viral escape. J. Exp. Med. 204:2505-2512. doi:10.1084/jem.20071261
26. Maness, N.J., N.A. Wilson, J.S. Reed, S.M. Piaskowski, J.B. Sacha, A.D. Walsh, E. Thoryk, G.J. Heidecker, M.P. Citron, X. Liang, et al. 2010. Robust, vaccine-induced CD8+ T lymphocyte response against an out-of-frame epitope. J. Immunol. 184:67-72.
27. Masemola, A., T. Mashishi, G. Khoury, P. Mohube, P. Mokgotho, E. Vardas, M. Colvin, L. Zijenah, D. Katzenstein, R. Musonda, et al; HIVNET 028 Study Team. 2004. Hierarchical targeting of subtype C human immuno-deficiency virus type 1 proteins by CD8+ T cells: correlation with viral load. J. Virol. 78:3233-3243. doi:10.1128/JVI.78.7.3233-3243.2004
28. Matthews, P.C., A. Prendergast, A. Leslie, H. Crawford, R. Payne, C. Rousseau, M. Rolland, I. Honeyborne, J. Carlson, C. Kadie, et al. 2008. Central role of reverting mutations in HLA associations with human immunodeficiency virus set point. J. Virol. 82:8548-8559. doi:10.1128/JVI.00580-08
29. McBratney, S., C.Y. Chen, and P. Sarnow. 1993. Internal initiation of translation. Curr. Opin. Cell Biol. 5:961-965. doi:10.1016/0955-0674(93) 90077-4
30. McElrath, M.J., S.C. De Rosa, Z. Moodie, S. Dubey, L. Kierstead, H. Janes, O.D. Defawe, D.K. Carter, J. Hural, R. Akondy, et al; Step Study Protocol Team. 2008. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet. 372:1894-1905. doi:10.1016/S0140-6736(08) 61592-5
31. Michael, N.L., M.T. Vahey, L. d'Arcy, P.K. Ehrenberg, J.D. Mosca, J. Rappaport, and R.R. Redfield. 1994. Negative-strand RNA transcripts are produced in human immunodeficiency virus type 1-infected cells and patients by a novel promoter downregulated by Tat. J. Virol. 68:979-987.
32. 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. doi:10.1038/ni845
33. Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, et al; MOPHTAVEG Investigators. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361:2209-2220. doi:10.1056/NEJMoa0908492
34. Sabbaj, S., A. Bansal, G.D. Ritter, C. Perkins, B.H. Edwards, E. Gough, J. Tang, J.J. Szinger, B. Korber, C.M. Wilson, et al. 2003. Cross-reactive CD8+ T cell epitopes identified in US adolescent minorities. J. Acquir. Immune Defic. Syndr. 33:426-438.
35. Schwab, S.R., K.C. Li, C. Kang, and N. Shastri. 2003. Constitutive display of cryptic translation products by MHC class I molecules. Science. 301:1367-1371. doi:10.1126/science.1085650
36. Seila, A.C., J.M. Calabrese, S.S. Levine, G.W. Yeo, P.B. Rahl, R.A. Flynn, R.A. Young, and P.A. Sharp. 2008. Divergent transcription from active promoters. Science. 322:1849-1851. doi:10.1126/science.1162253
37. Storey, J.D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA. 100:9440-9445. doi:10.1073/pnas.1530509100
38. Tsomides, T.J., A. Aldovini, R.P. Johnson, B.D. Walker, R.A. Young, and H.N. Eisen. 1994. Naturally processed viral peptides recognized by cytotoxic T lymphocytes on cells chronically infected by human immuno-deficiency virus type 1. J. Exp. Med. 180:1283-1293. doi:10.1084/ jem.180.4.1283
39. Weiss, R.B., D.M. Dunn, J.F. Atkins, and R.F. Gesteland. 1987. Slippery runs, shifty stops, backward steps, and forward hops: -2, -1, +1, +2, +5, and +6 ribosomal frameshifting. Cold Spring Harb. Symp. Quant. Biol. 52:687-693.
40. Wilson, N.A., B.F. Keele, J.S. Reed, S.M. Piaskowski, C.E. MacNair, A.J. Bett, X. Liang, F. Wang, E. Thoryk, G.J. Heidecker, et al. 2009. Vaccineinduced cellular responses control simian immunodeficiency virus replication after heterologous challenge. J. Virol. 83:6508-6521. doi:10.1128/ JVI.00272-09