Novel conserved-region T-cell mosaic vaccine with high global HIV-1 coverage is recognized by protective responses in untreated infection

Molecular Therapy

Volumn 24, Issue 4, 2016, Pages 832-842

  Ondondo, Beatrice ^a   Murakoshi, Hayato ^b   Clutton, Genevieve ^a,c   Abdul Jawad, Sultan ^a   Wee, Edmund G T ^a   Gatanaga, Hiroyuki ^b,d   Oka, Shinichi ^b,d   McMichael, Andrew J ^a   Takiguchi, Masafumi ^b   Korber, Bette ^e,f   Hanke, Tom ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KUMAMOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

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

^e LOS ALAMOS NATIONAL LABORATORY   (United States)

^f NEW MEXICO CONSORTIUM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; PLASMID DNA; T CELL MOSAIC VACCINE; UNCLASSIFIED DRUG; VACCINE;

ADENOVIRIDAE; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; DNA VECTOR; DRUG DESIGN; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; MAJOR CLINICAL STUDY; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; POXVIRIDAE; SIMIAN VIRUS; VACCINIA VIRUS; VIRUS LOAD; ANIMAL; HELA CELL LINE; HIV INFECTIONS; IMMUNOLOGY; PHYSIOLOGY;

ADENOVIRUSES, SIMIAN; AIDS VACCINES; ANIMALS; CD4 LYMPHOCYTE COUNT; CD8-POSITIVE T-LYMPHOCYTES; HELA CELLS; HIV INFECTIONS; HIV-1; HUMANS; MICE; VACCINIA VIRUS; VIRAL LOAD;

EID: 84957823994     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2016.3     Document Type: Article

References (47)

1. Hanke, T. (2014). Conserved immunogens in prime-boost strategies for the nextgeneration HIV-1 vaccines. Expert Opin Biol Ther 14: 601-616
2. McMichael, AJ, and Haynes, BF. (2012). Lessons learned from HIV-1 vaccine trials: new priorities, and directions. Nat Immunol 13: 423-427
3. Gaschen, B, Taylor, J, Yusim, K, Foley, B, Gao, F, Lang, D, et al. (2002). Diversity considerations in HIV-1 vaccine selection. Science 296: 2354-2360
4. Kuebler, PJ, Mehrotra, ML, McConnell, JJ, Holditch, SJ, Shaw, BI, Tarosso, LF, et al. (2015). Cellular immune correlates analysis of an HIV-1 preexposure prophylaxis trial. Proc Natl Acad Sci USA 112: 8379-8384
5. Freel, SA, Picking, RA, Ferrari, G, Ding, H, Ochsenbauer, C, Kappes, JC, et al. (2012). Initial HIV-1 antigen-specific CD8+ T cells in acute HIV-1 infection inhibit transmitted/founder virus replication. J Virol 86: 6835-6846
6. Goonetilleke, N, Liu, MK, Salazar-Gonzalez, JF, Ferrari, G, Giorgi, E, Ganusov, VV, 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
7. Fellay, J, Shianna, KV, Ge, D, Colombo, S, Ledergerber, B, Weale, M, et al. (2007). A whole-genome association study of major determinants for host control of HIV-1. Science 317: 944-947
8. Roederer, M, Keele, BF, Schmidt, SD, Mason, RD, Welles, HC, Fischer, W, et al. (2014). Immunological, and virological mechanisms of vaccine-mediated protection against SIV, and HIV. Nature 505: 502-508
9. Hansen, SG, Ford, JC, Lewis, MS, Ventura, AB, Hughes, CM, Coyne-Johnson, L, et al. (2011). Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473: 523-527
10. Hansen, SG, Piatak, M Jr, Ventura, AB, Hughes, CM, Gilbride, RM, Ford, JC, et al. (2013). Immune clearance of highly pathogenic SIV infection. Nature 502: 100-104
11. Fischer, W, Perkins, S, Theiler, J, Bhattacharya, T, Yusim, K, Funkhouser, R, et al. (2007). Polyvalent vaccines for optimal coverage of potential T-cell epitopes in global HIV-1 variants. Nat Med 13: 100-106
12. Abdul-Jawad, S, Ondondo, B, van Hateren, A, Gardner, A, Elliott, T, Korber, B, et al. (2015). Increased valency of conserved-mosaic vaccines enhances the breadth, and depth of epitope recognition. Mol Ther (epub ahead of print
13. Barouch, DH, O?Brien, KL, Simmons, NL, King, SL, Abbink, P, Maxfield, LF, et al. (2010). Mosaic HIV-1 vaccines expand the breadth, and depth of cellular immune responses in rhesus monkeys. Nat Med 16: 319-323
14. Santra, S, Liao, HX, Zhang, R, Muldoon, M, Watson, S, Fischer, W, 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
15. Létourneau, S, Im, EJ, Mashishi, T, Brereton, C, Bridgeman, A, Yang, H, et al. (2007). Design, and pre-clinical evaluation of a universal HIV-1 vaccine. PLoS One 2: e984
16. Rolland, M, Nickle, DC, and Mullins, JI. (2007). HIV-1 group M conserved elements vaccine. PLoS Pathog 3: e157
17. Yang, OO, Ali, A, Kasahara, N, Faure-Kumar, E, Bae, JY, Picker, LJ, et al. (2015). Short conserved sequences of HIV-1 are highly immunogenic, and shift immunodominance. J Virol 89: 1195-1204
18. Carlson, JM, Schaefer, M, Monaco, DC, Batorsky, R, Claiborne, DT, Prince, J, et al. (2014). HIV transmission. Selection bias at the heterosexual HIV-1 transmission bottleneck. Science 345: 1254031
19. Claiborne, DT, Prince, JL, Scully, E, Macharia, G, Micci, L, Lawson, B, et al. (2015). Replicative fitness of transmitted HIV-1 drives acute immune activation, proviral load in memory CD4+ T cells, and disease progression. Proc Natl Acad Sci USA 112: E1480-E1489
20. Deng, K, Pertea, M, Rongvaux, A, Wang, L, Durand, CM, Ghiaur, G, et al. (2015). Broad CTL response is required to clear latent HIV-1 due to dominance of escape mutations. Nature 517: 381-385
21. Ferguson, AL, Mann, JK, Omarjee, S, Ndung?u, T, Walker, BD, and Chakraborty, AK. (2013). Translating HIV sequences into quantitative fitness landscapes predicts viral vulnerabilities for rational immunogen design. Immunity 38: 606-617
22. Ahmed, T, et al. (2016).Control of HIV-1 replication by vaccine-induced CD8+ T cells in humans through conserved subdominant non-Gag epitopes. Vaccine (epub ahead of print
23. Borthwick, N, Ahmed, T, Ondondo, B, Hayes, P, Rose, A, Ebrahimsa, U, et al. (2014). Vaccine-elicited human T cells recognizing conserved protein regions inhibit HIV-1. Mol Ther 22: 464-475
24. Mothe, B, Llano, A, Ibarrondo, J, Daniels, M, Miranda, C, Zamarreño, J, et al. (2011). Definition of the viral targets of protective HIV-1-specific T cell responses. J Transl Med 9: 208
25. Mothe, B, Hu, X, Llano, A, Rosati, M, Olvera, A, Kulkarni, V, et al. (2015). A human immune data-informed vaccine concept elicits strong, and broad T-cell specificities associated with HIV-1 control in mice, and macaques. J Transl Med 13: 60
26. Dicks, MD, Spencer, AJ, Edwards, NJ, Wadell, G, Bojang, K, Gilbert, SC, et al. (2012). A novel chimpanzee adenovirus vector with low human seroprevalence: improved systems for vector derivation, and comparative immunogenicity. PLoS One 7: e40385
27. Kiepiela, P, Ngumbela, K, Thobakgale, C, Ramduth, D, Honeyborne, I, Moodley, E, et al. (2007). CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13: 46-53
28. Masemola, A, Mashishi, T, Khoury, G, Mohube, P, Mokgotho, P, Vardas, E, et al.; HIVNET 028 Study Team. (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
29. Rolland, M, Heckerman, D, Deng, W, Rousseau, CM, Coovadia, H, Bishop, K, et al. (2008). Broad, and Gag-biased HIV-1 epitope repertoires are associated with lower viral loads. PLoS One 3: e1424
30. Zuñiga, R, Lucchetti, A, Galvan, P, Sanchez, S, Sanchez, C, Hernandez, A, et al. (2006). Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J Virol 80: 3122-3125
31. Korber, BT, Farber, RM, Wolpert, DH, and Lapedes, AS. (1993). Covariation of mutations in the V3 loop of human immunodeficiency virus type 1 envelope protein: an information theoretic analysis. Proc Natl Acad Sci USA 90: 7176-7180
32. Takahashi, H, Germain, RN, Moss, B, and Berzofsky, JA. (1990). An immunodominant class I-restricted cytotoxic T lymphocyte determinant of human immunodeficiency virus type 1 induces CD4 class II-restricted help for itself. J Exp Med 171: 571-576
33. Ondondo, B, Abdul-Jawad, S, Bridgeman, A, and Hanke, T. (2014). Characterization of T-cell responses to conserved regions of the HIV-1 proteome in BALB/c mice. Clin Vaccine Immunol 21: 1565-1572
34. Naruto, T, Gatanaga, H, Nelson, G, Sakai, K, Carrington, M, Oka, S, et al. (2012). HLA class I-mediated control of HIV-1 in the Japanese population, in which the protective HLA-B.57, and HLA-B 27 alleles are absent. J Virol 86: 10870-10872
35. Ternette, N, Block, PD, Sánchez-Bernabéu, Á, Borthwick, N, Pappalardo, E, Abdul-Jawad, S, et al. (2015). Early kinetics of the HLA class I-Associated peptidome of MVA. HIVconsv-infected cells. J Virol 89: 5760-5771
36. Murakoshi, H, Akahoshi, T, Koyanagi, M, Chikata, T, Naruto, T, Maruyama, R, et al. (2015). Clinical control of HIV-1 by cytotoxic T cells specific for multiple conserved epitopes. J Virol 89: 5330-5339
37. Hancock, G, Yang, H, Yorke, E, Wainwright, E, Bourne, V, Frisbee, A, et al. (2015). Identification of effective subdominant anti-HIV-1 CD8+ T cells within entire postinfection, and post-vaccination immune responses. PLoS Pathog 11: e1004658
38. Li, F, Finnefrock, AC, Dubey, SA, Korber, BT, Szinger, J, Cole, S, 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
39. Buchbinder, SP, Mehrotra, DV, Duerr, A, Fitzgerald, DW, Mogg, R, Li, D, 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-ofconcept trial. Lancet 372: 1881-1893
40. Hammer, SM, Sobieszczyk, ME, Janes, H, Karuna, ST, Mulligan, MJ, Grove, D, et al. (2013) Efficacy trial of a DNA/rAd5 HIV-1 preventive vaccine. N Engl J Med 369: 2083-2092
41. Liu, MK, Hawkins, N, Ritchie, AJ, Ganusov, VV, Whale, V, Brackenridge, S, et al.; CHAVI Core B. (2013). Vertical T cell immunodominance, and epitope entropy determine HIV-1 escape. J Clin Invest 123: 380-393
42. Manocheewa, S, Lanxon-Cookson, EC, Liu, Y, Swain, JV, McClure, J, Rao, U, et al. (2015) Pairwise growth competition assay for determining the replication fitness of human immunodeficiency viruses. J Vis Exp 4: e52610
43. Manocheewa, S, Mittler, JE, Samudrala, R, and Mullins, JI. (2015). Composite sequence-structure stability models as screening tools for identifying vulnerable targets for HIV drug, and vaccine development. Viruses 7: 5718-5735
44. Rolland, M, Manocheewa, S, Swain, JV, Lanxon-Cookson, EC, Kim, M, Westfall, DH, et al. (2013). HIV-1 conserved-element vaccines: relationship between sequence conservation, and replicative capacity. J Virol 87: 5461-5467
45. Ewer, KJ, O?Hara, GA, Duncan, CJ, Collins, KA, Sheehy, SH, Reyes-Sandoval, A, et al. (2013). Protective CD8+ T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat Commun 4: 2836
46. Sheehy, SH, Duncan, CJ, Elias, SC, Collins, KA, Ewer, KJ, Spencer, AJ, et al. (2011). Phase Ia clinical evaluation of the Plasmodium falciparum blood-stage antigen MSP1 in ChAd63, and MVA vaccine vectors. Mol Ther 19: 2269-2276
47. Margolis, DM, and Hazuda, DJ. (2013). Combined approaches for HIV cure. Curr Opin HIV AIDS 8: 230-235