Conservation of HIV-1 T cell epitopes across time and clades: Validation of immunogenic HLA-A2 epitopes selected for the GAIA HIV vaccine

Vaccine

Volumn 30, Issue 52, 2012, Pages 7547-7560

  Levitz, Lauren ^a   Koita, Ousmane A ^d   Sangare, Kotou ^d   Ardito, Matthew T ^a   Boyle, Christine M ^a   Rozehnal, John ^b   Tounkara, Karamoko ^c   Dao, Sounkalo M ^e   Koné, Youssouf ^c   Koty, Zoumana ^c   Buus, Soren ^f   Moise, Leonard ^a,b   Martin, William D ^a   De Groot, Anne S ^a,b,c  

^a EpiVax Inc   (United States)

^b UNIVERSITY OF RHODE ISLAND   (United States)

^c GAIA Vaccine Foundation   (Mali)

^d UNIVERSITY OF BAMAKO   (Mali)

^e Infectious Disease and Tropical Medicine Unit   (Mali)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

GAIA vaccine; HIV 1 vaccine; HLA A2 epitope; Immunoinformatics; T cell epitopes

Indexed keywords

AMINO ACID; GAMMA INTERFERON; HLA A2 ANTIGEN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE;

AMINO ACID SEQUENCE; ANTIGEN BINDING; ARTICLE; CLADISTICS; EPITOPE MAPPING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOGENICITY; MALI; PRIORITY JOURNAL; SPECIES DIVERSITY; T LYMPHOCYTE; UNITED STATES;

AIDS VACCINES; ANTIGENS, VIRAL; CONSERVED SEQUENCE; EPITOPES, T-LYMPHOCYTE; GEOGRAPHY; HIV-1; HLA-A2 ANTIGEN; HUMANS; LEUKOCYTES, MONONUCLEAR; MALI; RHODE ISLAND; TIME FACTORS;

EID: 84870524263     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.10.042     Document Type: Article

References (88)

1. Graham B.S. Clinical trials of HIV vaccines. Annu Rev Med 2002, 53:207-221.
2. Ho D.D., Huang Y. The HIV-1 vaccine race. Cell 2002, 110(2):135-138.
3. Korber B.T., Letvin N.L., Haynes B.F. T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J Virol 2009, 83(17):8300-8314.
4. Kawashima Y., Pfafferott K., Frater J., Matthews P., Payne R., Addo M., et al. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009, 458(7238):641-645.
5. Rousseau C.M., Daniels M.G., Carlson J.M., Kadie C., Crawford H., Prendergast A., 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(13):6434-6446.
6. McCarthy M. HIV vaccine fails in phase 3 trial. Lancet 2003, 361(9359):755-756.
7. Cohen J. Public health. AIDS vaccine trial produces disappointment and confusion. Science 2003, 299(5611):1290-1291.
8. Hoag H. Mixed results win HIV vaccine a guarded response. Nature 2003, 421:877.
9. Vaccination and Enrollment Are Discontinued in Phase II Trials of Merck's Investigational HIV Vaccine Candidate. Merck & Co. 2007 September 21. http://www.merck.com/newsroom/press_releases/.
10. Kresge KJ. What Next? As data analysis for the STEP trial gets underway, some other trials are placed in a temporary holding pattern. IAVI Report. 2007;11(5). http://www.iavireport.org/.
11. Catanzaro A.T., Koup R.A., Roederer M., Bailer R.T., Enama M.E., Moodie Z., et al. Vaccine Research Center 006 Study Team. Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 candidate vaccine delivered by a replication-defective recombinant adenovirus vector. J Infect Dis 2006, 194(12):1638-1649.
12. Dubey S., Clair J., Fu T.M., Guan L., Long R., Mogg R., et al. Detection of HIV vaccine-induced cell-mediated immunity in HIV-seronegative clinical trial participants using an optimized and validated enzyme-linked immunospot assay. J Acquir Immune Defic Syndr 2007, 45(1):20-27.
13. Rolland M., Tovanabutra S., deCamp A.C., Frahm N., Gilbert P.B., Sanders-Buell E., et al. Genetic impact of vaccination on breakthrough HIV-1 sequences from the STEP trial. Nat Med 2011, 17(March (3)):366-371.
14. Rerks-Ngarm S., Pitisuttihum P., Nitayaphan S., et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009, 361(23):2209-2220.
15. Letvin N.L. Strategies for an HIV vaccine. J Clin Invest 2002, 110(1):15-20.
16. Borrow P., Lewicki H., Hahn B.H., Shaw G.M., Oldstone M.B. Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 1994, 68(9):6103-6110.
17. Musey L., Hughes J., Schacker T., Shea T., Corey L., McElrath M.J. Cytotoxic-T-cell responses, viral load, and disease progression in early human immunodeficiency virus type 1 infection. N Engl J Med 1997, 337(18):1267-1274.
18. Rosenberg E.S., Billingsley J.M., Caliendo A.M., Boswell S.L., Sax P.E., Kalams S.A., et al. Vigorous HIV-1-specific CD4+ T-cell responses associated with control of viremia. Science 1997, 278:1447-1450.
19. Schmitz J.E., Kuroda M.J., Santra S., Sasseville V.G., Simon M.A., Lifton M.A., et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999, 283(5403):857-860.
20. Goulder P.J., Brander C., Tang Y., Tremblay C., Colbert R.A., Addo M.M., et al. Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 2001, 412(6844):334-338.
21. Ferre A.L., Hunt P.W., McConnell D.H., Morris M.M., Garcia J.C., Pollard R.B., et al. HIV controllers with HLA-DRB1*13 and HLA-DQB1*06 alleles have strong, polyfunctional mucosal CD4+ T-cell responses. J Virol 2010, 84(November (21)):11020-11029.
22. Shedlock D.J., Shen H. Requirement for CD4 T-cell help in generating functional CD8 T-cell memory. Science 2003, 300:337-339.
23. Rosa D.S., Ribeiro S.P., Almeida R.R., Mairena E.C., Postól E., Kalil J., Cunha-Neto E. A DNA vaccine encoding multiple HIV CD4 epitopes elicits vigorous polyfunctional, long-lived CD4+ and CD8+ T cell responses. PLoS One 2011, 6(February (2)):e16921.
24. Koup R.A., Safrit J.T., Cao Y., Andrews C.A., McLeod G., Borkowsky W., 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(7):4650-4655.
25. Ferrari G., Korber B., Goonetilleke N., Liu M.K.P., Turnbull E.L., et al. Relationship between functional profile of HIV-1 specific CD8T Cells and epitope variability with the selection of escape mutants in acute HIV-1 infection. PLoS Pathog 2011, 7(2):e1001273.
26. Troyer R.M., McNevin J., Liu Y., Zhang S.C., Krizan R.W., Abraha A., et al. Variable fitness impact of HIV-1 escape mutations to cytotoxic T lymphocyte (CTL) response. PLoS Pathog 2009, 5(April (4)):e1000365.
27. Streeck H., Jolin J.S., Qi Y., Yassine-Diab B., Johnson R.C., Kwon D.S., et al. 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 2009, 83(August (15)):7641-7648.
28. Brumme Z.L., John M., Carlson J.M., Brumme C.J., Chan D., Brockman M.A., et al. HLA-associated immune escape pathways in HIV-1 subtype B Gag, Pol and Nef proteins. PLoS One 2009, 4(August (8)):e6687.
29. Dembek C.J., Kutscher S., Heltai S., Allgayer S., Biswas P., Ghezzi S., et al. Nef-specific CD45RA+ CD8+ T cells secreting MIP-1beta but not IFN-gamma are associated with nonprogressive HIV-1 infection. AIDS Res Ther 2010, 7(July):20.
30. Wong J.K., Strain M.C., Porrata R., Reay E., Sankaran-Walters S., et al. In Vivo CD8+ T-Cell suppression of SIV viremia is not mediated by CTL clearance of productively infected cells. PLoS Pathog 2010, 6(1):e1000748.
31. Allen T.M., Altfeld M., Geer S.C., Kalife E.T., Moore C., O'Sullivan K.M., et al. Selective escape from CD8+ T-cell responses represents a major driving force of human immunodeficiency virus type 1 (HIV-1) sequence diversity and reveals constraints on HIV-1 evolution. J Virol 2005, 79(21):13239-13249.
32. De Groot A.S., Rivera D.S., McMurry J.A., Buus S., Martin W. Identification of immunogenic HLA-B7 Achilles' Heel epitopes within highly conserved regions of HIV. Vaccine 2008, 26:305-307.
33. Matthews P.C., Leslie A.J., Katzourakis A., Crawford H., Payne R., Prendergast A., et al. HLA footprints on human immunodeficiency virus type 1 are associated with interclade polymorphisms and intraclade phylogenetic clustering. J Virol 2009, 83(May (9)):4605-4615.
34. Peyerl F.W., Bazick H.S., Newberg M.H., Barouch D.H., Sodroski J., Letvin N.L. Fitness costs limit viral escape from cytotoxic T lymphocytes at a structurally constrained epitope. J Virol 2004, 78(24):13901-13910.
35. Frahm N., Korber B.T., Adams C.M., Szinger J.J., Draenert R., Addo M.M., et al. Brander C Consistent cytotoxic-T-lymphocyte targeting of immunodominant regions in human immunodeficiency virus across multiple ethnicities. J Virol 2004, 78(5):2187-2200.
36. Korber B.T., Letvin N.L., Haynes B.F. T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J Virol 2009 Sep, 83(17):8300-8314.
37. Rolland M., Nickle D.C., Mullins J.I. HIV-1 group M conserved elements vaccine. PLoS Pathog 2007, 3(11):e157. 10.1371/journal.ppat.0030157.
38. Fischer W., Liao H.X., Haynes B.F., Letvin N.L., Korber B. Coping with viral diversity in HIV vaccine design: a response to Nickle et al. PLoS Comput Biol 2008, 4(1):e15. 10.1371/journal.pcbi.0040015.
39. Nickle D.C., Jojic N., Heckerman D., Jojic V., Kirovski D., et al. Comparison of immunogen designs that optimize peptide coverage: reply to Fischer et al. PLoS Comput Biol 2008, 4(1):e25. 10.1371/journal.pcbi.0040025.
40. Wang Y.E., Li B., Carlson J.M., Streeck H., Gladden A.D., Goodman R., et al. Protective HLA class I alleles that restrict acute-phase CD8+ T-cell responses are associated with viral escape mutations located in highly conserved regions of human immunodeficiency virus type 1. J Virol 2009, 83(4):1845-1855.
41. Yang O.O., Daar E.S., Ng H.L., Shih R., Jamieson B.D. Increasing CTL targeting of conserved sequences during early HIV-1 infection is correlated to decreasing viremia. AIDS Res Hum Retroviruses 2011, 27(April (4)):391-398.
42. Rousseau C., Daniels Mg 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(13):6434-6446.
43. Julg B., Williams K.L., Reddy S., Bishop K., Qi Y., Carrington M., et al. Enhanced anti-HIV functional activity associated with Gag-specific CD8 T-cell responses. J Virol 2010, 84(June (11)):5540-5549.
44. Duda A., Lee-Turner L., Fox J., Robinson N., Dustan S., Kaye S., et al. SPARTAC Trial Investigators. HLA-associated clinical progression correlates with epitope reversion rates in early human immunodeficiency virus infection. Virol 2009, 83(February (3)):1228-1239.
45. Ahlers J.D., Belyakov I.M. Lessons learned from natural infection: focusing on the design of protective T cell vaccines for HIV/AIDS. Trends Immunol 2010, 31(March (3)):120-130.
46. Zhang C., Cornette J.L., Berzofsky J.A., DeLisi C. The organization of human leucocyte antigen class I epitopes in HIV genome products: implications for HIV evolution and vaccine design. Vaccine 1997, 15(12-13):1291-1302.
47. Sidney J., Peters B., Frahm N., Brander C., Sette A. HLA class I supertypes: a revised and updated classification. BMC Immunol 2008, 9:1-15.
48. De Groot A.S., Levitz L., Ardito M.T., Skowron G., Mayer K.H., Buus S., Boyle C.M., Martin WD Further progress on defining highly conserved immunogenic epitopes for a global HIV vaccine: HLA-A3-restricted GAIA vaccine epitopes. Hum Vaccin Immunother 2012, 8(July (7)).
49. Koita O.A.D., Dabitao I., Mahamadou M., Tall A.S., Dao A., Tounkara H., et al. Confirmation of immunogenic consensus sequence HIV-1 T-cell epitopes in Bamako, Mali and Providence, Rhode Island. Hum Vaccines 2006, 2(3):119-128.
50. Ellis J.M., Henson V., Slack R., Ng J., Hartzman R.J., Katovich Hurley C. Frequencies of HLA-A2 alleles in five U.S. population groups. Predominance of A*02011 and identification of HLA-A*0231. Hum Immunol 2000, 61(3):334-340.
51. Gong X., Gui X., Zhang Y., Tien P. Screening for CD8 cytotoxic T lymphocytes specific for Gag of human immunodeficiency virus type1 subtype B' Henan isolate from China and identification of novel epitopes restricted by the HLA-A2 and HLA-A11 alleles. J Gen Virol 2006, 87(Pt 1):151-158.
52. Lyke K.E., Burges R.B., Cissoko Y., Sangare L., Kone A., Dao M., et al. HLA-A2 supertype-restricted cell-mediated immunity by peripheral blood mononuclear cells derived from Malian children with severe or uncomplicated Plasmodium falciparum malaria and healthy controls. Infect Immun 2005, 73(September (9)):5799-5808.
53. De Groot A.S., Bosma A., Chinai N., Frost J., Jesdale B.M., et al. From genome to vaccine: in silico predictions, ex vivo verification. Vaccine 2001, 19:4385-4395.
54. DeGroot A.S., Jesdale B., Martin W., Saint Aubin C., Sbai H., Bosma A., et al. Mapping cross-clade HIV-1 vaccine epitopes using a bioinformatics approach. Vaccine 2003, 21:4486-4504.
55. De Groot A.S., Martin W. Reducing risk, improving outcomes: bioengineering immunogenic protein therapeutics. Clin Immunol. 2009, 131:189-201. Epub 2009 March 6.
56. Sylvester-Hvid C., Kristensen N., Blicher T., Ferre H., Lauemoller S.L., Wolf X.A., et al. Establishment of a quantitative ELISA capable of determining peptide-MHC class I interaction. Tissue Antigens 2002, 59(40):251-258.
57. Schaubert K.L., Price D.A., Frahm N., Li J., Ng H.L., Joseph A., et al. Availability of a diverselt avid CD8+ T cell repertoire specific for the subdominant HLA-A2-restricted HIV-1 Gag p 2419-27 epitope. J Immunol 2007, 178(12):7756-7766.
58. Altfeld M., Addo M.M., Shankarappa R., Lee P.K., Allen T.M., Yu X.G., et al. 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 2003, 77(13):7330-7340.
59. Otto O. Candidate vaccine sequences to represent intra- and inter-clade HIV-1 variation. PLoS One 2009, 4(10):e7388.
60. Tang C., Ndassa Y., Summers N.F. Structure of the N-terminal 283-residue fragment of the immature HIV-1 Gag polyprotein. Nat Struct Biol 2002, 9(7):537-543.
61. Iversen A.K., Stewart-Jones G., Learn G.H., Christie N., Sylvester-Hviid C., Armitage A.E., et al. Conflicting selective forces affect T cell receptor contacts in an immunodominant human immunodeficiency virus epitope. Nat Immunol 2006, 7(February (2)):179-189.
62. Nguyen L., Chaowanachan T., Vanichseni S., McNicholl J.M., Mock P.A., Nelson R., et al. Frequent human leukocyte antigen class I alleles are associated with higher viral load among HIV type 1 seroconverters in Thailand. J Acquir Immune Defic Syndr 2004, 37(October (2)):1318-1323.
63. Schafer J.R.A., Jesdale B.M., George J.A., Kouttab N.M., De Groot A.S. Prediction of well-conserved HIV-1 ligands using a matrix-based algorithm, EpiMatrix. Vaccine 1998, 16(19):1880-1884.
64. DeGroot A.S., Marcon L., Bishop E.A., Kutzler M., Weiner D.B., Martin W. HIV vaccine development by computer assisted design: the GAIA vaccine. Vaccine 2005, 23:2136-2148.
65. Corbet S., Nielsen H.V., Vinner L., Lauemoller S., Therrien D., Tang S., et al. Optimization and immune recognition of multiple novel conserved HLA-A2, human immunodeficiency virus type 1-specific CTL epitopes. J Gen Virol 2003, 84:2409-2421.
66. Thakar M.R., Bhonge L.S., Lakhashe S.K., Shankarkumar U., Sane S.S., Kulkarni S.S., et al. Cytolytic T lymphocytes (CTLs) from HIV-1 subtype C-infected Indian patients recognize CTL epitopes from a conserved immunodominant region of HIV-1 Gag and Nef. J Infect Dis 2005, 192(5):749-759.
67. Bernard N.F., Pederson K., Chung F., Ouellet L., Wainberg M.A., Tsoukas C.M. HIV-specific cytotoxic T-lymphocyte activity in immunologically normal HIV-infected persons. AIDS 1998, 12(16):2125-2139.
68. Goonetilleke N., Liu M.K., Salazar-Gonzalez J.F., Ferrari G., Giorgi E., Ganusov V.V., et al. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 2009, 206(6):1253-1272.
69. Wang Z., Liu H.W., Hong K.X., Yu Z.J., Chen J.P., Ruan Y.H., et al. Complete human immunodeficiency virus-1 specific T lymphocyte response to Chinese human immunodeficiency virus-1 B/C chronic infectors. Biomed Environ Sci 2009, 22(December (6)):522-528.
70. Kiepiela P., Nqumbela K., Thobakagale C., Ramduth D., Honeyborne I., Moodley E., et al. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 2007, 13(1):46-53.
71. Boutwell C.L., Essex M. Identification of HLA class I-associated amino acid polymorphisms in the HIV-1C proteome. AIDS Res Hum Retroviruses 2007, 23(1):165-174.
72. Schmitz E., Kuroda M.J., Santra S., Sasseville V.G., Simon M.A., Lifton M.A., et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 1999, 283:857-860.
73. Ogg G.S., Jin X., Bonhoeffer S., Dunbar P.R., Novak M.A., Monard S., et al. Quantitation of HIV-1-specific cytotoxic T-lymphocytes and plasma load of viral RNA. Science 1998, 279:2130-2136.
74. Kawashima Y., Pfafferott K., Frater J., Matthews P., Payne R., Addo M., et al. Adaptation of HIV-1 to human leukocyte antigen class I. Nature 2009, 458(April (7238)):641-645.
75. Leslie A., Kavanagh D., Honeyborne I., Pfafferott K., Edwards C., Pillay T., et al. Transmission and accumulation of CTL escape variants drive negative associations between HIV polymorphisms and HLA. J Exp Med 2005, 201(March (6)):891-902.
76. Karlsson A.C., Chapman J.M., Heiken B.D., Hoh R., Kallas E.G., Martin J.N., et al. Antiretroviral drug therapy alters the profile of human immunodeficiency virus type 1-specific T-cell Responses and shifts the immunodominant cytotoxic T-lymphocyte response from Gag to Pol. J Virol 2007, 81(20):11543-11548.
77. Ogg G., Jin X., Bonhoeffer S., Moss P., Nowak M.A., Monard S., et al. Decay kinetics of HIV-specific CTL after combination antiretroviral therapy. J Virol 1999, 73:797-800.
78. Goulder P.J.R., Phillips R.E., Colbert R.A., McAdam S., Ogg G., Nowak M.A., et al. Late escape from an immunodominant-cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 1997, 3(2):212-217.
79. Im E.J., Hong J.P., Roshorm Y., Bridgeman A., Letourneau S., Lijestrom P., et al. Protective efficacy of serially up-ranked subdominant CD8+ T cell epitopes against virus challenge. PLoS Pathog 2011, 7(5):e1002041.
80. Wilson C.C., McKinney D., Anders M., MaWhinney S., Forster J., Crimi C., et al. Development of a DNA vaccine to induce cytotoxic T lymphocyte responses to multiple conserved epitopes in HIV-1. J Immunol 2003, 15:5611-5623.
81. Altfeld M., Allen T.M., Kalife E.T., Frahm N., Addo M.M., Mothe B.R., et al. The majority of currently circulating human immunodeficiency virus type 1 clade B viruses fail to prime cytotoxic T-lymphocyte responses against an otherwise immunodominant HLA-A2-restricted epitope: implications for vaccine design. J Virol 2005, 79(April (8)):5000-5005.
82. Letourneau S., Im E-J., Mashishi T., Brereton C., Bridgeman A., Yang H., et al. Design and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS One 2007, 2(10):e984.
83. Fischer W., Perkins S., Theiler T., Bhattacharya K., Yusim K., Funkhouser R., et al. Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat Med 2007, 13:100-106.
84. Santra S., Liao H-X., Zhang R., Muldoon M., Watson S., Fischer W., et al. Mosaic vaccines elicit CD8+ T lymphocyte responses in monkeys that confer enhanced immune coverage of diverse HIV strains. Nat Med 2010, 16(3):324-328.
85. Perez C.L., Larsen M.V., Gustafsson R., Norstrom M.M., Atlas A., Nixon D.F., et al. Broadly immunogenic HLA class I supertype-restricted elite CTL epitopes recognized in a diverse population infected with different HIV-1 subtypes. J Immunol 2008, 180(7):5092-5100.
86. Borrow P., Shaw G.M. Cytotoxic T-lymphocyte escape viral variants: how important are they in viral evasion of immune clearance in vivo. Immunol Rev 1998, 164:37-51.
87. Liu Y., McNevin J., Rolland M., Zhao H., Deng W., Maenza J., et al. Conserved HIV-1 epitopes continuously elicit subdominant cytotoxic T-lymphocyte responses. J Infect Dis 2009, 200(12):1825-1833.
88. Goulder P.J., Altfeld M.A., Rosenberg E.S., Nguyen T., Tang Y., Eldridge R.L., et al. Substantial differences in specificity of HIV-specific cytotoxic T cells in acute and chronic HIV infection. J Exp Med 2001, 193(2):181-194.