Characterization of T-Cell responses to cryptic epitopes in recipients of a noncodon-optimized HIV-1 Vaccine

Journal of Acquired Immune Deficiency Syndromes

Volumn 65, Issue 2, 2014, Pages 142-150

  Bet, Anne ^a   Sterrett, Sarah ^a   Sato, Alicia ^b   Bansal, Anju ^a   Goepfert, Paul A ^a  

^a University of Alabama at Birmingham   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Alternative reading frames; CD8+ T cells; Codon optimized; Cryptic epitopes; HIV 1; HVTN 205 vaccine trial

Indexed keywords

ARF PROTEIN; CRYPTIC EPITOPE; EPITOPE; GAG PROTEIN; GAMMA INTERFERON; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; PLACEBO; POL PROTEIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS ENVELOPE PROTEIN;

ANTIGEN SPECIFICITY; ARTICLE; BIOINFORMATICS; CELLULAR IMMUNITY; CODON; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RESPONSE; ENZYME LINKED IMMUNOSPOT ASSAY; EX VIVO STUDY; GENE INSERTION; GENE VECTOR; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOGENICITY; LIMIT OF DETECTION; MAJOR CLINICAL STUDY; NUCLEOTIDE SEQUENCE; PHASE 2 CLINICAL TRIAL; PRIORITY JOURNAL; T LYMPHOCYTE;

AIDS VACCINES; COHORT STUDIES; EPITOPES, T-LYMPHOCYTE; HUMANS; T-LYMPHOCYTES;

EID: 84893718910     PISSN: 15254135     EISSN: 10779450     Source Type: Journal    
DOI: 10.1097/QAI.0b013e3182a9917e     Document Type: Article

References (59)

1. Taylor BS, Hammer SM. The challenge of HIV-1 subtype diversity. N Engl J Med. 2008;359:1965-1966.
2. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med. 2009;361:2209-2220.
3. Picker LJ, Hansen SG, Lifson JD. New paradigms for HIV/AIDS vaccine development. Annu Rev Med. 2012;63:95-111.
4. Haynes BF, Gilbert PB, McElrath MJ, et al. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med. 2012;366:1275-1286.
5. McElrath MJ, De Rosa SC, Moodie Z, et al. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet. 2008;372:1894-1905.
6. Buchbinder SP, Mehrotra DV, Duerr A, et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a doubleblind, randomised, placebo-controlled, test-of-concept trial. Lancet. 2008;372:1881-1893.
7. Letvin NL, Mascola JR, Sun Y, et al. Preserved CD4+ central memory T cells and survival in vaccinated SIV-challenged monkeys. Science. 2006; 312:1530-1533.
8. Barouch DH, Liu J, Li H, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature. 2012; 482:89-93.
9. Hansen SG, Ford JC, Lewis MS, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature. 2011;473: 523-527.
10. Fukazawa Y, Park H, Cameron MJ, et al. Lymph node T cell responses predict the efficacy of live attenuated SIV vaccines. Nat Med. 2012;18: 1673-1681.
11. Liu J, O'Brien KL, Lynch DM, et al. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature. 2009;457: 87-91.
12. Wilson NA, Keele BF, Reed JS, et al. Vaccine-induced cellular responses control simian immunodeficiency virus replication after heterologous challenge. J Virol. 2009;83:6508-6521.
13. Mudd PA, Martins MA, Ericsen AJ, et al. Vaccine-induced CD8+ T cells control AIDS virus replication. Nature. 2012;491:129-133.
14. Edwards BH, Bansal A, Sabbaj S, et al. 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. 2002;76: 2298-2305.
15. Goulder PJ, Watkins DI. Impact of MHC class I diversity on immune control of immunodeficiency virus replication. Nat Rev Immunol. 2008;8: 619-630.
16. Brumme ZL, Brumme CJ, Carlson J, et al. Marked epitope- and allelespecific differences in rates of mutation in human immunodeficiency type 1 (HIV-1) Gag, Pol, and Nef cytotoxic T-lymphocyte epitopes in acute/ early HIV-1 infection. J Virol. 2008;82:9216-9227.
17. Chevalier MF, Julg B, Pyo A, et al. HIV-1-specific interleukin-21+ CD4 + T cell responses contribute to durable viral control through the modulation of HIV-specific CD8+ T cell function. J Virol. 2011;85:733-741.
18. Bansal A, Carlson J, Yan J, et al. CD8 T cell response and evolutionary pressure to HIV-1 cryptic epitopes derived from antisense transcription. J Exp Med. 2010;207:51-59.
19. Berger CT, Carlson JM, Brumme CJ, et al. Viral adaptation to immune selection pressure by HLA class I-restricted CTL responses targeting epitopes in HIV frameshift sequences. J Exp Med. 2010;207:61-75.
20. Champiat S, Raposo RA, Maness NJ, et al. Influence of HAART on alternative reading frame immune responses over the course of HIV-1 infection. PLoS One. 2012;7:e39311.
21. Gaur A, Green WR. Role of a cytotoxic-T-lymphocyte epitope-defined, alternative gag open reading frame in the pathogenesis of a murine retrovirus-induced immunodeficiency syndrome. J Virol. 2005;79: 4308-4315.
22. Dolan BP, Li L, Takeda K, et al. Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase. J Immunol. 2010;184:1419-1424.
23. Michael NL, Vahey MT, d'Arcy L, et al. 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. 1994;68:979-987.
24. Yewdell JW, Anton LC, Bennink JR. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules. J Immunol. 1996;157:1823-1826.
25. Cardinaud S, Moris A, Fevrier M, et al. Identification of cryptic MHC I-restricted epitopes encoded by HIV-1 alternative reading frames. J Exp Med. 2004;199:1053-1063.
26. Maness NJ, Valentine LE, May GE, et al. AIDS virus-specific CD8(+) T lymphocytes against an immunodominant cryptic epitope select for viral escape. J Exp Med. 2007;204:2505-2512.
27. Ochsenbauer C, Edmonds TG, Ding H, et al. Generation of transmitted/ founder HIV-1 infectious molecular clones and characterization of their replication capacity in CD4 T lymphocytes and monocyte-derived macrophages. J Virol. 2012;86:2715-2728.
28. Drummond AJ, Ashton B, Buxton S, Cheung M, et al. Geneious. 5.6 ed. 2012.
29. Goepfert PA, Elizaga ML, Sato A, et al. Phase 1 safety and immunogenicity testing of DNA and recombinant modified vaccinia Ankara vaccines expressing HIV-1 virus-like particles. J Infect Dis. 2011;203:610-619.
30. Draenert R, Brander C, Yu XG, et al. Impact of intrapeptide epitope location on CD8 T cell recognition: implications for design of overlapping peptide panels. AIDS. 2004;18:871-876.
31. Yewdell JW, Hickman HD. New lane in the information highway: alternative reading frame peptides elicit T cells with potent antiretrovirus activity. J Exp Med. 2007;204:2501-2504.
32. Bullock TN, Patterson AE, Franlin LL, et al. Initiation codon scanthrough versus termination codon readthrough demonstrates strong potential for major histocompatibility complex class I-restricted cryptic epitope expression. J Exp Med. 1997;186:1051-1058.
33. Bansal A, Yue L, Conway J, et al. Immunological control of chronic HIV-1 infection: HLA-mediated immune function and viral evolution in adolescents. AIDS. 2007;21:2387-2397.
34. Muturi M, Gichuki C, Mutua G, et al. Cultured enzyme-linked immunospot assay (ELISPOT) enhances detection of low HIV-specific immune responses in exposed seronegative individuals in Kenya. Retrovirology. 2006:3(suppl 1):44.
35. Goonetilleke N, Moore S, Dally L, et al. Induction of multifunctional human immunodeficiency virus type 1 (HIV-1)-specific T cells capable of proliferation in healthy subjects by using a prime-boost regimen of DNA- and modified vaccinia virus Ankara-vectored vaccines expressing HIV-1 Gag coupled to CD8+ T-cell epitopes. J Virol. 2006;80: 4717-4728.
36. Winstone N, Guimaraes-Walker A, Roberts J, et al. Increased detection of proliferating, polyfunctional, HIV-1-specific T cells in DNA-modified vaccinia virus Ankara-vaccinated human volunteers by cultured IFNgamma ELISPOT assay. Eur J Immunol. 2009;39:975-985.
37. Campion S, Cohen MS, McMichael AJ, et al. Improved detection of latent Mycobacterium tuberculosis infection in HIV-1 seropositive individuals using cultured cellular assays. Eur J Immunol. 2011;41:255-257.
38. Ritchie AJ, Campion SL, Kopycinski J, et al. Differences in HIV-specific T cell responses between HIV-exposed and -unexposed HIV-seronegative individuals. J Virol. 2011;85:3507-3516.
39. Nagata T, Uchijima M, Yoshida A, et al. Codon optimization effect on translational efficiency of DNA vaccine in mammalian cells: analysis of plasmid DNA encoding a CTL epitope derived from microorganisms. Biochem Biophys Res Commun. 1999;261:445-451.
40. Abdulhaqq SA, Weiner DB. DNA vaccines: developing new strategies to enhance immune responses. Immunol Res. 2008;42:219-232.
41. Keele BF, Giorgi EE, Salazar-Gonzalez JF, et al. Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A. 2008;105:7552-7557.
42. Priddy FH, Brown D, Kublin J, et al. Safety and immunogenicity of a replication-incompetent adenovirus type 5 HIV-1 clade B gag/pol/nef vaccine in healthy adults. Clin Infect Dis. 2008;46:1769-1781.
43. Graham BS, Enama ME, Nason MC, et al. DNA vaccine delivered by a needle-free injection device improves potency of priming for antibody and CD8+ T-cell responses after rAd5 boost in a randomized clinical trial. PLoS One. 2013;8:e59340.
44. Cannarozzi G, Schraudolph NN, Faty M, et al. A role for codon order in translation dynamics. Cell. 2010;141:355-367.
45. Smith JM, Amara RR, Campbell D, et al. DNA/MVA vaccine for HIV type 1: effects of codon-optimization and the expression of aggregates or virus-like particles on the immunogenicity of the DNA prime. AIDS Res Hum Retroviruses. 2004;20:1335-1347.
46. Malhotra I, Wamachi AN, Mungai PL, et al. Fine specificity of neonatal lymphocytes to an abundant malaria blood-stage antigen: epitope mapping of Plasmodium falciparum MSP1(33). J Immunol. 2008;180: 3383-3390.
47. Kotlar D, Lavner Y. The action of selection on codon bias in the human genome is related to frequency, complexity, and chronology of amino acids. BMC Genomics. 2006;7:67.
48. Watts JM, Dang KK, Gorelick RJ, et al. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature. 2009;460:711-716.
49. Stephenson KE, SanMiguel A, Simmons NL, et al. Full-length HIV-1 immunogens induce greater magnitude and comparable breadth of T lymphocyte responses to conserved HIV-1 regions compared with conserved- region-only HIV-1 immunogens in rhesus monkeys. J Virol. 2012;86:11434-11440.
50. Bull M, Lee D, Stucky J, et al. Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. J Immunol Methods. 2007;322:57-69.
51. Filbert H, Attig S, Bidmon N, et al. Serum-free freezing media support high cell quality and excellent ELISPOT assay performance across a wide variety of different assay protocols. Cancer Immunol Immunother. 2013; 62:615-627.
52. Janetzki S, Price L, Britten CM, et al. Performance of serum-supplemented and serum-free media in IFNgamma Elispot assays for human T cells. Cancer Immunol Immunother. 2010;59:609-618.
53. Bruce AG, Atkins JF, Gesteland RF. tRNA anticodon replacement experiments show that ribosomal frameshifting can be caused by doublet decoding. Proc Natl Acad Sci U S A. 1986;83:5062-5066.
54. Bansal A, Gough E, Sabbaj S, et al. CD8 T-cell responses in early HIV-1 infection are skewed towards high entropy peptides. AIDS. 2005;19: 241-250.
55. Harari A, Bart PA, Stohr W, et al. An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T cell responses. J Exp Med. 2008;205:63-77.
56. Maness NJ, Wilson NA, Reed JS, et al. Robust, vaccine-induced CD8(+) T lymphocyte response against an out-of-frame epitope. J Immunol. 2010;184:67-72.
57. Maness NJ, Walsh AD, Piaskowski SM, et al. CD8+ T cell recognition of cryptic epitopes is a ubiquitous feature of AIDS virus infection. J Virol. 2010;84:11569-11574.
58. Otting N, Heijmans CM, Noort RC, et al. Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci U S A. 2005; 102:1626-1631.
59. Schirmbeck R, Riedl P, Fissolo N, et al. Translation from cryptic reading frames of DNA vaccines generates an extended repertoire of immunogenic, MHC class I-restricted epitopes. J Immunol. 2005;174:4647-4656.