Superior Control of HIV-1 Replication by CD8+ T Cells Targeting Conserved Epitopes: Implications for HIV Vaccine Design

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Kunwar, Pratima ^a,d   Hawkins, Natalie ^b   Dinges, Warren L ^a,c   Liu, Yi ^d   Gabriel, Erin E ^b   Swan, David A ^b   Stevens, Claire E ^d   Maenza, Janine ^d   Collier, Ann C ^d   Mullins, James I ^d   Hertz, Tomer ^b   Yu, Xuesong ^b   Horton, Helen ^a,d  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c Infectious Diseases Research Institute   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAG PROTEIN; HLA A ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; NEF PROTEIN; POL PROTEIN;

ADAPTIVE IMMUNITY; ARTICLE; CD8+ T LYMPHOCYTE; DRUG DESIGN; DRUG RESPONSE; ENTROPY; ENZYME LINKED IMMUNOSPOT ASSAY; EPITOPE MAPPING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMORAL IMMUNITY; INFECTION CONTROL; PREVALENCE; SEQUENCE ALIGNMENT; VIREMIA; VIRUS LOAD; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANTIGENS, VIRAL; CD8-POSITIVE T-LYMPHOCYTES; CONSERVED SEQUENCE; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; GENE EXPRESSION; GENETIC HETEROGENEITY; HIV INFECTIONS; HIV-1; HOMOSEXUALITY, MALE; HUMANS; IMMUNITY, CELLULAR; MALE; MOLECULAR SEQUENCE DATA; VIRAL LOAD; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84878594580     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064405     Document Type: Article

References (77)

1. Mascola JR, Montefiori DC, (2010) The role of antibodies in HIV vaccines. Annu Rev Immunol 28: 413-444.
2. McElrath MJ, Haynes BF, (2010) Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 33: 542-554.
3. McMichael AJ, Rowland-Jones SL, (2001) Cellular immune responses to HIV. Nature 410: 980-987.
4. Girard MP, Plotkin SA, (2012) HIV vaccine development at the turn of the 21st century. Curr Opin HIV AIDS 7: 4-9.
5. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, et al. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 361: 2209-2220.
6. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, et al. (2012) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 366: 1275-1286.
7. Fukazawa Y, Park H, Cameron MJ, Lefebvre F, Lum R, et al. (2012) Lymph node T cell responses predict the efficacy of live attenuated SIV vaccines. Nat Med.
8. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, et al. (2011) Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473: 523-527.
9. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, et al. (1999) Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189: 991-998.
10. Fellay J, Ge D, Shianna KV, Colombo S, Ledergerber B, et al. (2009) Common genetic variation and the control of HIV-1 in humans. PLoS Genet 5: e1000791.
11. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, et al. (2007) A whole-genome association study of major determinants for host control of HIV-1. Science 317: 944-947.
12. Pereyra F, Jia X, McLaren PJ, Telenti A, de Bakker PI, et al. (2010) The major genetic determinants of HIV-1 control affect HLA class I peptide presentation. Science 330: 1551-1557.
13. Carrington M, Nelson GW, Martin MP, Kissner T, Vlahov D, et al. (1999) HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283: 1748-1752.
14. Carrington M, O'Brien SJ, (2003) The influence of HLA genotype on AIDS. Annu Rev Med 54: 535-551.
15. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, et al. (1997) Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med 3: 205-211.
16. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, et al. (1997) Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 3: 212-217.
17. Price DA, Goulder PJ, Klenerman P, Sewell AK, Easterbrook PJ, et al. (1997) Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc Natl Acad Sci U S A 94: 1890-1895.
18. Alimonti JB, Kimani J, Matu L, Wachihi C, Kaul R, et al. (2006) Characterization of CD8 T-cell responses in HIV-1-exposed seronegative commercial sex workers from Nairobi, Kenya. Immunol Cell Biol 84: 482-485.
19. Promadej N, Costello C, Wernett MM, Kulkarni PS, Robison VA, et al. (2003) Broad human immunodeficiency virus (HIV)-specific T cell responses to conserved HIV proteins in HIV-seronegative women highly exposed to a single HIV-infected partner. J Infect Dis 187: 1053-1063.
20. Rowland-Jones SL, Dong T, Dorrell L, Ogg G, Hansasuta P, et al. (1999) Broadly cross-reactive HIV-specific cytotoxic T-lymphocytes in highly-exposed persistently seronegative donors. Immunol Lett 66: 9-14.
21. Rowland-Jones SL, Pinheiro S, Kaul R, Hansasuta P, Gillespie G, et al. (2001) How important is the 'quality' of the cytotoxic T lymphocyte (CTL) response in protection against HIV infection? Immunol Lett 79: 15-20.
22. Reynolds MR, Weiler AM, Weisgrau KL, Piaskowski SM, Furlott JR, et al. (2008) Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J Exp Med 205: 2537-2550.
23. Wyand MS, Manson K, Montefiori DC, Lifson JD, Johnson RP, et al. (1999) Protection by live, attenuated simian immunodeficiency virus against heterologous challenge. J Virol 73: 8356-8363.
24. Barouch DH, O'Brien KL, Simmons NL, King SL, Abbink P, et al. (2010) Mosaic HIV-1 vaccines expand the breadth and depth of cellular immune responses in rhesus monkeys. Nat Med 16: 319-323.
25. Santra S, Liao HX, Zhang R, Muldoon M, Watson S, et al. (2010) Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat Med 16: 324-328.
26. Altfeld M, Allen TM, (2006) Hitting HIV where it hurts: an alternative approach to HIV vaccine design. Trends Immunol 27: 504-510.
27. Letourneau S, Im EJ, Mashishi T, Brereton C, Bridgeman A, et al. (2007) Design and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS One 2: e984.
28. Niu L, Termini JM, Kanagavelu SK, Gupta S, Rolland MM, et al. (2011) Preclinical evaluation of HIV-1 therapeutic ex vivo dendritic cell vaccines expressing consensus Gag antigens and conserved Gag epitopes. Vaccine 29: 2110-2119.
29. Rolland M, Nickle DC, Mullins JI, (2007) HIV-1 group M conserved elements vaccine. PLoS Pathog 3: e157.
30. Draenert R, Verrill CL, Tang Y, Allen TM, Wurcel AG, et al. (2004) Persistent recognition of autologous virus by high-avidity CD8 T cells in chronic, progressive human immunodeficiency virus type 1 infection. J Virol 78: 630-641.
31. Gea-Banacloche JC, Migueles SA, Martino L, Shupert WL, McNeil AC, et al. (2000) Maintenance of large numbers of virus-specific CD8+ T cells in HIV-infected progressors and long-term nonprogressors. J Immunol 165: 1082-1092.
32. Ogg GS, Jin X, Bonhoeffer S, Dunbar PR, Nowak MA, et al. (1998) Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279: 2103-2106.
33. Cao J, McNevin J, Holte S, Fink L, Corey L, et al. (2003) Comprehensive analysis of human immunodeficiency virus type 1 (HIV-1)-specific gamma interferon-secreting CD8+ T cells in primary HIV-1 infection. J Virol 77: 6867-6878.
34. Addo MM, Yu XG, Rathod A, Cohen D, Eldridge RL, 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 viral load. J Virol 77: 2081-2092.
35. Betts MR, Ambrozak DR, Douek DC, Bonhoeffer S, Brenchley JM, et al. (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.
36. Masemola A, Mashishi T, Khoury G, Mohube P, Mokgotho P, et al. (2004) Hierarchical targeting of subtype C human immunodeficiency virus type 1 proteins by CD8+ T cells: correlation with viral load. J Virol 78: 3233-3243.
37. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, et al. (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
38. Thobakgale CF, Streeck H, Mkhwanazi N, Mncube Z, Maphumulo L, et al. (2011) Short communication: CD8(+) T cell polyfunctionality profiles in progressive and nonprogressive pediatric HIV type 1 infection. AIDS Res Hum Retroviruses 27: 1005-1012.
39. Julg B, Williams KL, Reddy S, Bishop K, Qi Y, et al. (2010) Enhanced anti-HIV functional activity associated with Gag-specific CD8 T-cell responses. J Virol 84: 5540-5549.
40. Horton H, Frank I, Baydo R, Jalbert E, Penn J, et al. (2006) Preservation of T cell proliferation restricted by protective HLA alleles is critical for immune control of HIV-1 infection. J Immunol 177: 7406-7415.
41. Payne RP, Kloverpris H, Sacha JB, Brumme Z, Brumme C, et al. (2010) Efficacious early antiviral activity of HIV Gag- and Pol-specific HLA-B 2705-restricted CD8+ T cells. J Virol 84: 10543-10557.
42. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, et al. (2007) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13: 46-53.
43. Sacha JB, Chung C, Rakasz EG, Spencer SP, Jonas AK, et al. (2007) Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J Immunol 178: 2746-2754.
44. Hertz T, Nolan D, James I, John M, Gaudieri S, et al. (2011) Mapping the landscape of host-pathogen coevolution: HLA class I binding and its relationship with evolutionary conservation in human and viral proteins. J Virol 85: 1310-1321.
45. Mothe B, Llano A, Ibarrondo J, Daniels M, Miranda C, et al. (2011) Definition of the viral targets of protective HIV-1-specific T cell responses. J Transl Med 9: 208.
46. Feeney ME, Tang Y, Roosevelt KA, Leslie AJ, McIntosh K, et al. (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.
47. Brockman MA, Schneidewind A, Lahaie M, Schmidt A, Miura T, 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.
48. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, et al. (2004) HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 10: 282-289.
49. Dinges WL, Richardt J, Friedrich D, Jalbert E, Liu Y, et al. (2010) Virus-specific CD8+ T-cell responses better define HIV disease progression than HLA genotype. J Virol 84: 4461-4468.
50. Brambilla D, Leung S, Lew J, Todd J, Herman S, et al. (1998) Absolute copy number and relative change in determinations of human immunodeficiency virus type 1 RNA in plasma: effect of an external standard on kit comparisons. J Clin Microbiol 36: 311-314.
51. Kristiansen TB, Knudsen TB, Ohlendorff S, Eugen-Olsen J, (2001) A new multiplex PCR strategy for the simultaneous determination of four genetic polymorphisms affecting HIV-1 disease progression. J Immunol Methods 252: 147-151.
52. Horton H, Havenar-Daughton C, Lee D, Moore E, Cao J, et al. (2006) Induction of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses in HIV vaccine trial participants who subsequently acquire HIV-1 infection. J Virol 80: 9779-9788.
53. Kern F, Surel IP, Faulhaber N, Frommel C, Schneider-Mergener J, et al. (1999) Target structures of the CD8(+)-T-cell response to human cytomegalovirus: the 72-kilodalton major immediate-early protein revisited. J Virol 73: 8179-8184.
54. Betts MR, Casazza JP, Patterson BA, Waldrop S, Trigona W, et al. (2000) Putative immunodominant human immunodeficiency virus-specific CD8(+) T-cell responses cannot be predicted by major histocompatibility complex class I haplotype. J Virol 74: 9144-9151.
55. Liu Y, McNevin J, Rolland M, Zhao H, Deng W, et al. (2009) Conserved HIV-1 epitopes continuously elicit subdominant cytotoxic T-lymphocyte responses. J Infect Dis 200: 1825-1833.
56. Li F, Finnefrock AC, Dubey SA, Korber BT, Szinger J, et al. (2011) Mapping HIV-1 vaccine induced T-cell responses: bias towards less-conserved regions and potential impact on vaccine efficacy in the Step study. PLoS One 6: e20479.
57. Cover TM, Thomas JA (2006) Elements of Information Theory: Wiley-Interscience. 776 p.
58. Mayrose I, Graur D, Ben-Tal N, Pupko T, (2004) Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior. Molecular Biology and Evolution 21: 1781-1791.
59. Berezin C, Glaser F, Rosenberg J, Paz I, Pupko T, et al. (2004) ConSeq: the identification of functionally and structurally important residues in protein sequences. Bioinformatics (Oxford, England) 20: 1322-1324.
60. Bansal A, Gough E, Sabbaj S, Ritter D, Yusim K, et al. (2005) CD8 T-cell responses in early HIV-1 infection are skewed towards high entropy peptides. AIDS 19: 241-250.
61. Frahm N, Korber BT, Adams CM, Szinger JJ, Draenert R, et al. (2004) Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. Journal of Virology 78: 2187-2200.
62. Fontaine Costa AI, Rao X, Lechenadec E, van Baarle D, Keşmir C, (2010) HLA-B molecules target more conserved regions of the HIV-1 proteome. AIDS (London, England) 24: 211-215.
63. Penn O, Stern A, Rubinstein ND, Dutheil J, Bacharach E, et al. (2008) Evolutionary modeling of rate shifts reveals specificity determinants in HIV-1 subtypes. PLoS Computational Biology 4: e1000214.
64. Li F, Malhotra U, Gilbert PB, Hawkins NR, Duerr AC, et al. (2006) Peptide selection for human immunodeficiency virus type 1 CTL-based vaccine evaluation. Vaccine 24: 6893-6904.
65. Liu Y, McNevin J, Cao J, Zhao H, Genowati I, et al. (2006) Selection on the human immunodeficiency virus type 1 proteome following primary infection. J Virol 80: 9519-9529.
66. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB, (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68: 6103-6110.
67. Altfeld M, Rosenberg ES, Shankarappa R, Mukherjee JS, Hecht FM, 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.
68. Streeck H, Jolin JS, Qi Y, Yassine-Diab B, Johnson RC, et al. (2009) Human immunodeficiency virus type 1-specific CD8+ T-cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J Virol 83: 7641-7648.
69. Malhotra U, Li F, Nolin J, Allison M, Zhao H, et al. (2007) Enhanced detection of human immunodeficiency virus type 1 (HIV-1) Nef-specific T cells recognizing multiple variants in early HIV-1 infection. J Virol 81: 5225-5237.
70. Altfeld M, Addo MM, Shankarappa R, Lee PK, Allen TM, et al. (2003) Enhanced detection of human immunodeficiency virus type 1-specific T-cell responses to highly variable regions by using peptides based on autologous virus sequences. J Virol 77: 7330-7340.
71. Mothe B, Llano A, Ibarrondo J, Zamarreno J, Schiaulini M, et al. (2012) CTL responses of high functional avidity and broad variant cross-reactivity are associated with HIV control. PLoS One 7: e29717.
72. Kawashima Y, Pfafferott K, Frater J, Matthews P, Payne R, et al. (2009) Adaptation of HIV-1 to human leukocyte antigen class I. Nature. 458: 641-645.
73. Elahi S, Dinges WL, Lejarcegui N, Laing KJ, Collier AC, et al. (2011) Protective HIV-specific CD8+ T cells evade Treg cell suppression. Nat Med 17: 989-995.
74. Edwards BH, Bansal A, Sabbaj S, Bakari J, Mulligan MJ, et al. (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.
75. Berger CT, Frahm N, Price DA, Mothe B, Ghebremichael M, et al. (2011) High-functional-avidity cytotoxic T lymphocyte responses to HLA-B-restricted Gag-derived epitopes associated with relative HIV control. J Virol 85: 9334-9345.
76. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, et al. (2007) Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 204: 2473-2485.
77. Lichterfeld M, Yu XG, Mui SK, Williams KL, Trocha A, et al. (2007) Selective depletion of high-avidity human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T cells after early HIV-1 infection. J Virol 81: 4199-4214.