Increased valency of conserved-mosaic vaccines enhances the breadth and depth of Epitope recognition

Molecular Therapy

Volumn 24, Issue 2, 2016, Pages 375-384

  Abdul Jawad, Sultan ^a   Ondondo, Beatrice ^a   Van Hateren, Andy ^b   Gardner, Andrew ^a   Elliott, Tim ^b   Korber, Bette ^c,d   Hanke, Tomáš ^a,e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d NEW MEXICO CONSORTIUM   (United States)

^e KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; HLA A2 ANTIGEN; HLA-A*02:01 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONSENSUS SEQUENCE; CONTROLLED STUDY; CROSS REACTION; DRUG DESIGN; EMBRYO; FEMALE; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; T LYMPHOCYTE; ANIMAL; GENETICS; HIV INFECTIONS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; METABOLISM; TRANSGENIC MOUSE;

AIDS VACCINES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; EPITOPES, T-LYMPHOCYTE; HIV INFECTIONS; HIV-1; HLA-A2 ANTIGEN; HUMANS; MICE; MICE, TRANSGENIC;

EID: 84959497460     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2015.210     Document Type: Article

References (54)

1. 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.
2. 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.
3. 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.
4. Borrow, P, Lewicki, H, Hahn, BH, Shaw, GM and 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.
5. 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.
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. Goulder, PJ, Brander, C, Tang, Y, Tremblay, C, Colbert, RA, Addo, MM, et al. (2001). Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412: 334-338.
8. Koup, RA, Safrit, JT, Cao, Y, Andrews, CA, McLeod, G, Borkowsky, W, et al. (1994). Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68: 4650-4655.
9. Ogg, GS, Jin, X, Bonhoeffer, S, Dunbar, PR, Nowak, MA, Monard, S, et al. (1998). Quantitation of HIV-1-specific cytotoxic T lymphocytes and plasma load of viral RNA. Science 279: 2103-2106.
10. Walker, B and McMichael, A (2012). The T-cell response to HIV. Cold Spring Harb Perspect Med 2:.
11. Hanke, T (2014). Conserved immunogens in prime-boost strategies for the nextgeneration HIV-1 vaccines. Expert Opin Biol Ther 14: 601-616.
12. Margolis, DM and Hazuda, DJ (2013). Combined approaches for HIV cure. Curr Opin HIV AIDS 8: 230-235.
13. 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.
14. Leslie, AJ, Pfafferott, KJ, Chetty, P, Draenert, R, Addo, MM, Feeney, M, et al. (2004). HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 10: 282-289.
15. 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.
16. 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.
17. 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.
18. Hayton, EJ, Rose, A, Ibrahimsa, U, Del Sorbo, M, Capone, S, Crook, A, et al. (2014). Safety and tolerability of conserved region vaccines vectored by plasmid DNA, simian adenovirus and modified vaccinia virus ankara administered to human immunodeficiency virus type 1-uninfected adults in a randomized, single-blind phase I trial. PLoS One 9: e101591.
19. 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.
20. 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.
21. Li, F, Malhotra, U, Gilbert, PB, Hawkins, NR, Duerr, AC, McElrath, JM, et al. (2006). Peptide selection for human immunodeficiency virus type 1 CTL-based vaccine evaluation. Vaccine 24: 6893-6904.
22. 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.
23. Hulot, SL, Korber, B, Giorgi, EE, Vandergrift, N, Saunders, KO, Balachandran, H, et al. (2015). Comparison of Immunogenicity in Rhesus Macaques of Transmitted-Founder, HIV-1 Group M Consensus and Trivalent Mosaic Envelope Vaccines Formulated as a DNA Prime, NYVAC and Envelope Protein Boost. J Virol 89: 6462-6480.
24. 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.
25. Barouch, DH, Stephenson, KE, Borducchi, EN, Smith, K, Stanley, K, McNally, AG, et al. (2013). Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell 155: 531-539.
26. Pascolo, S, Bervas, N, Ure, JM, Smith, AG, Lemonnier, FA and Pérarnau, B (1997). HLA-A2.1-restricted education and cytolytic activity of CD8(+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J Exp Med 185: 2043-2051.
27. Ahmed, T, et al. Control of HIV-1 replication in vitro by vaccine-induced human CD8+T cells through conserved subdominant Pol epitopes. Vaccine (in press
28. 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.
29. Klenerman, P, Rowland-Jones, S, McAdam, S, Edwards, J, Daenke, S, Lalloo, D, et al. (1994). Cytotoxic T-cell activity antagonized by naturally occurring HIV-1 Gag variants. Nature 369: 403-407.
30. 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.
31. Lee, JK, Stewart-Jones, G, Dong, T, Harlos, K, Di Gleria, K, Dorrell, L, et al. (2004). T cell cross-reactivity and conformational changes during TCR engagement. J Exp Med 200: 1455-1466.
32. Korber, B, Gaschen, B, Yusim, K, Thakallapally, R, Kesmir, C and Detours, V (2001). Evolutionary and immunological implications of contemporary HIV-1 variation. Br Med Bull 58: 19-42.
33. Rolland, M, Nickle, DC and Mullins, JI (2007). HIV-1 group M conserved elements vaccine. PLoS Pathog 3: e157.
34. 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.
35. Fenimore, PW, Muhammad, MA, Fischer, WM, Foley, BT, Bakken, RR, Thurmond, JR, et al. (2012). Designing and testing broadly-protective filoviral vaccines optimized for cytotoxic T-lymphocyte epitope coverage. PLoS One 7: e44769.
36. Kong, WP, Wu, L, Wallstrom, TC, Fischer, W, Yang, ZY, Ko, SY, et al. (2009). Expanded breadth of the T-cell response to mosaic human immunodeficiency virus type 1 envelope DNA vaccination. J Virol 83: 2201-2215.
37. Yusim, K, Dilan, R, Borducchi, E, Stanley, K, Giorgi, E, Fischer, W, et al. (2013). Hepatitis C genotype 1 mosaic vaccines are immunogenic in mice and induce stronger T-cell responses than natural strains. Clin Vaccine Immunol 20: 302-305.
38. Santra, S, Muldoon, M, Watson, S, Buzby, A, Balachandran, H, Carlson, KR, et al. (2012). Breadth of cellular and humoral immune responses elicited in rhesus monkeys by multi-valent mosaic and consensus immunogens. Virology 428: 121-127.
39. Larke, N, Im, EJ, Wagner, R, Williamson, C, Williamson, AL, McMichael, AJ, et al. (2007). Combined single-clade candidate HIV-1 vaccines induce T cell responses limited by multiple forms of in vivo immune interference. Eur J Immunol 37: 566-577.
40. Liu, J, Ewald, BA, Lynch, DM, Nanda, A, Sumida, SM and Barouch, DH (2006). Modulation of DNA vaccine-Elicited CD8+ T-lymphocyte epitope immunodominance hierarchies. J Virol 80: 11991-11997.
41. Rodriguez, F, Harkins, S, Slifka, MK and Whitton, JL (2002). Immunodominance in virus-induced CD8(+) T-cell responses is dramatically modified by DNA immunization and is regulated by gamma interferon. J Virol 76: 4251-4259.
42. Rosario, M, Bridgeman, A, Quakkelaar, ED, Quigley, MF, Hill, BJ, Knudsen, ML, et al. (2010). Long peptides induce polyfunctional T cells against conserved regions of HIV-1 with superior breadth to single-gene vaccines in macaques. Eur J Immunol 40: 1973-1984.
43. Williamson, C, Morris, L, Maughan, MF, Ping, LH, Dryga, SA, Thomas, R, et al. (2003). Characterization and selection of HIV-1 subtype C isolates for use in vaccine development. AIDS Res Hum Retroviruses 19: 133-144.
44. Korber, BT, Letvin, NL and Haynes, BF (2009). T-cell vaccine strategies for human immunodeficiency virus, the virus with a thousand faces. J Virol 83: 8300-8314.
45. Im, EJ, Hong, JP, Roshorm, Y, Bridgeman, A, Létourneau, S, Liljeström, P, et al. (2011). Protective efficacy of serially up-ranked subdominant CD8+ T cell epitopes against virus challenges. PLoS Pathog 7: e1002041.
46. Kamlangdee, A, Kingstad-Bakke, B, Anderson, TK, Goldberg, TL and Osorio, JE (2014). Broad protection against avian influenza virus by using a modified vaccinia Ankara virus expressing a mosaic hemagglutinin gene. J Virol 88: 13300-13309.
47. Yusim, K, Kesmir, C, Gaschen, B, Addo, MM, Altfeld, M, Brunak, S, et al. (2002). Clustering patterns of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1 (HIV-1) proteins reveal imprints of immune evasion on HIV-1 global variation. J Virol 76: 8757-8768.
48. Yusim, K, Fischer, W, Yoon, H, Thurmond, J, Fenimore, PW, Lauer, G, et al. (2010). Genotype 1 and global hepatitis C T-cell vaccines designed to optimize coverage of genetic diversity. J Gen Virol 91(Pt 5): 1194-1206.
49. Warming, S, Costantino, N, Court, DL, Jenkins, NA and Copeland, NG (2005). Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33: e36.
50. Wang, Z, Martinez, J, Zhou, W, La Rosa, C, Srivastava, T, Dasgupta, A, et al. (2010). Modified H5 promoter improves stability of insert genes while maintaining immunogenicity during extended passage of genetically engineered MVA vaccines. Vaccine 28: 1547-1557.
51. Hopkins, R, Bridgeman, A, Bourne, C, Mbewe-Mvula, A, Sadoff, JC, Both, GW, et al. (2011). Optimizing HIV-1-specific CD8+ T-cell induction by recombinant BCG in prime-boost regimens with heterologous viral vectors. Eur J Immunol 41: 3542-3552.
52. 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.
53. van Hateren, A, Bailey, A, Werner, JM and Elliott, T (2015). Plasticity of empty major histocompatibility complex class I molecules determines peptide-selector function. Mol Immunol 68(2 Pt A): 98-101.
54. Hermann, C, van Hateren, A, Trautwein, N, Neerincx, A, Duriez, PJ, Stevanović, S, et al. (2015). TAPBPR alters MHC class I peptide presentation by functioning as a peptide exchange catalyst. Elife 4. doi: 10.7554/eLife.09617.