Asymptomatic HLA-A*02:01-restricted epitopes from herpes simplex virus glycoprotein B preferentially recall polyfunctional CD8 + T cells from seropositive asymptomatic individuals and protect HLA transgenic mice against ocular herpes

Journal of Immunology

Volumn 191, Issue 10, 2013, Pages 5124-5138

  Dervillez, Xavier ^a   Qureshi, Huma ^a   Chentoufi, Aziz A ^a,e   Khan, Arif A ^a   Kritzer, Elizabeth ^a   Yu, David C ^a   Diaz, Oscar R ^a   Gottimukkala, Chetan ^a   Kalantari, Mina ^a   Villacres, Maria C ^b   Scarfone, Vanessa M ^a   McKinney, Denise M ^c   Sidney, John ^c   Sette, Alessandro ^c   Nesburn, Anthony B ^a   Wechsler, Steven L ^a,d   Ben Mohamed, Lbachir ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e KING FAHAD MEDICAL CITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; EPITOPE; GAMMA INTERFERON; GLYCOPROTEIN B; HLA A ANTIGEN; INTERLEUKIN 2; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; TUMOR NECROSIS FACTOR ALPHA; GLYCOPROTEIN B, SIMPLEXVIRUS; HLA A2 ANTIGEN; HLA-A*02:01 ANTIGEN; VIRUS ENVELOPE PROTEIN;

ADULT; AGED; ANTIGEN BINDING; ARTICLE; ASYMPTOMATIC INFECTION; BINDING AFFINITY; C57BL 6 MOUSE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DEGRANULATION; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HERPES SIMPLEX VIRUS 1; HERPES ZOSTER OPHTHALMICUS; HUMAN; HUMAN CELL; IMMUNIZATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RECURRENT INFECTION; SUSCEPTIBLE POPULATION; TRANSGENIC MOUSE; ADOLESCENT; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; KERATITIS, HERPETIC; METABOLISM; MIDDLE AGED; MOUSE; SIMPLEXVIRUS; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANIMALS; ASYMPTOMATIC INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; EPITOPES, T-LYMPHOCYTE; FEMALE; HLA-A2 ANTIGEN; HUMANS; IMMUNIZATION; KERATITIS, HERPETIC; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; SIMPLEXVIRUS; VIRAL ENVELOPE PROTEINS; YOUNG ADULT;

EID: 84887451938     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301415     Document Type: Article

References (65)

1. Zhang, X., X. Dervillez, A. A. Chentoufi, T. Badakhshan, I. Bettahi, and L. Ben Mohamed. 2012. Targeting the genital tract mucosa with a lipopeptide/recombinant adenovirus prime/boost vaccine induces potent and long-lasting CD8+ T cell immunity against herpes: importance of MyD88. J. Immunol. 189:4496-4509.
2. + T cell epitope-based vaccines against ocular herpes. J. Immunol. 184:2561-2571.
3. + cytotoxic T lymphocyte epitopes identified from herpes simplex virus glycoprotein D. J. Immunol. 180:426-437.
4. Chentoufi, A. A., L. Ben Mohamed, P. Van De Perre, and A. A. Ashkar. 2012. Immunity to ocular and genital herpes simplex viruses infections. Clin. Dev. Immunol. 2012:732546.
5. Chentoufi, A. A., and L. Ben Mohamed. 2012. Mucosal herpes immunity and immunopathology to ocular and genital herpes simplex virus infections. Clin. Dev. Immunol. 2012:149135.
6. Corey, L., A. G. Langenberg, R. Ashley, R. E. Sekulovich, A. E. Izu, J. M. Douglas, Jr., H. H. Handsfield, T. Warren, L. Marr, S. Tyring, et al; Chiron HSV Vaccine Study Group. 1999. Recombinant glycoprotein vaccine for the prevention of genital HSV-2 infection: two randomized controlled trials. JAMA 282:331-340.
7. Langenberg, A. G., L. Corey, R. L. Ashley, W. P. Leong, and S. E. Straus; Chiron HSV Vaccine Study Group. 1999. A prospective study of new infections with herpes simplex virus type 1 and type 2. N. Engl. J. Med. 341:1432-1438.
8. +-T cell-epitopes-based immunotherapeutic vaccine candidates? Vaccine 29:5824-5836.
9. + cytotoxic T-cell epitopes identified from herpes simplex virus glycoprotein B. J. Virol. 82:11792-11802.
10. + Th1-type T-cell peptide epitopes from herpes simplex virus glycoprotein D that confer protective immunity. J. Virol. 77:9463-9473.
11. + Tc1 responses and protect against ocular infection. J. Virol. 79:15289-15301.
12. Nesburn, A. B., I. Bettahi, X. Zhang, X. Zhu, W. Chamberlain, R. E. Afifi, S. L. Wechsler, and L. Ben Mohamed. 2006. Topical/mucosal delivery of sub-unit vaccines that stimulate the ocular mucosal immune system. Ocul. Surf. 4:178-187.
13. Chentoufi, A. A., E. Kritzer, D. M. Yu, A. B. Nesburn, and L. Ben Mohamed. 2012. Towards a rational design of an asymptomatic clinical herpes vaccine: the old, the new, and the unknown. Clin. Dev. Immunol. 2012:187585.
14. Dasgupta, G., A. B. Nesburn, S. L. Wechsler, and L. Ben Mohamed. 2010. Developing an asymptomatic mucosal herpes vaccine: the present and the future. Future Microbiol. 5:1-4.
15. Chentoufi, A. A., and L. Ben Mohamed. 2010. Future viral vectors for the delivery of asymptomatic herpes epitope-based immunotherapeutic vaccines. Future Virol 5:525-528.
16. Dervillez, X., C. Gottimukkala, K. W. Kabbara, C. Nguyen, T. Badakhshan, S. M. Kim, A. B. Nesburn, S. L. Wechsler, and L. Ben Mohamed. 2012. Future of an "asymptomatic" T-cell epitope-based therapeutic herpes simplex vaccine. Future Virol. 7:371-378.
17. Dasgupta, G., A. A. Chentoufi, M. Kalantari, P. Falatoonzadeh, S. Chun, C. H. Lim, P. L. Felgner, D. H. Davies, and L. Ben Mohamed. 2012. Immunodominant "asymptomatic" herpes simplex virus 1 and 2 protein antigens identified by probing whole-ORFome microarrays with serum antibodies from seropositive asymptomatic versus symptomatic individuals. J. Virol. 86:4358-4369.
18. Moraru, M., E. Cisneros, N. Gómez-Lozano, R. De Pablo, F. Portero, M. Cañizares, M. Vaquero, G. Roustán, I. Millán, M. López-Botet, and C. Vilches. 2012. Host genetic factors in susceptibility to herpes simplex type 1 virus infection: contribution of polymorphic genes at the interface of innate and adaptive immunity. J. Immunol. 188:4412-4420.
19. Lekstrom-Himes, J. A., P. Hohman, T. Warren, A. Wald, J. M. Nam, T. Simonis, L. Corey, and S. E. Straus. 1999. Association of major histocompatibility complex determinants with the development of symptomatic and asymptomatic genital herpes simplex virus type 2 infections. J. Infect. Dis. 179:1077-1085.
20. Böhringer, D., R. Sundmacher, and T. Reinhard. 2007. [HLA B27 seems to promote graft failure following penetrating keratoplasties for herpetic corneal scars]. Ophthalmologe 104:705-708.
21. Chentoufi, A. A., X. Dervillez, G. Dasgupta, C. Nguyen, K. W. Kabbara, X. Jiang, A. B. Nesburn, S. L. Wechsler, and L. Ben Mohamed. 2012. The herpes simplex virus type 1 latency-associated transcript inhibits phenotypic and functional maturation of dendritic cells. Viral Immunol. 25:204-215.
22. Jiang, X., A. A. Chentoufi, C. Hsiang, D. Carpenter, N. Osorio, L. Ben Mohamed, N. W. Fraser, C. Jones, and S. L. Wechsler. 2011. The herpes simplex virus type 1 latency-associated transcript can protect neuron-derived C1300 and Neuro2A cells from granzyme B-induced apoptosis and CD8 T-cell killing. J. Virol. 85:2325-2332.
23. + T cells in latently infected trigeminal ganglia: a novel immune evasion mechanism. J. Virol. 85:9127-9138.
24. + T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J. Exp. Med. 204:595-603.
25. + skinresident T cells in human herpes virus infection. Nature 497:494-497.
26. Blaney, J. E., Jr., E. Nobusawa, M. A. Brehm, R. H. Bonneau, L. M. Mylin, T. M. Fu, Y. Kawaoka, and S. S. Tevethia. 1998. Immunization with a single major histocompatibility complex class I-restricted cytotoxic T-lymphocyte recognition epitope of herpes simplex virus type 2 confers protective immunity. J. Virol. 72:9567-9574.
27. St Leger, A. J., B. Peters, J. Sidney, A. Sette, and R. L. Hendricks. 2011. Defining the herpes simplex virus-specific CD8+ T cell repertoire in C57BL/6 mice. J. Immunol. 186:3927-3933.
28. Sidney, J., S. Southwood, C. Moore, C. Oseroff, C. Pinilla, H. M. Grey, and A. Sette. 2013. Measurement of MHC/peptide interactions by gel filtration or monoclonal antibody capture. Curr. Protoc. Immunol. 18:18.3.
29. Bunce, M. 2003. PCR-sequence-specific primer typing of HLA class I and class II alleles. Methods Mol. Biol. 210:143-171.
30. Ben Mohamed, L., S. L. Wechsler, and A. B. Nesburn. 2002. Lipopeptide vaccines: yesterday, today, and tomorrow. Lancet Infect. Dis. 2:425-431.
31. + T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281:65-78.
32. *0201 allele. J. Immunol. 173:2126-2133.
33. Gilchuk, P., C. T. Spencer, S. B. Conant, T. Hill, J. J. Gray, X. Niu, M. Zheng, J. J. Erickson, K. L. Boyd, K. J. McAfee, et al. 2013. Discovering naturally processed antigenic determinants that confer protective T cell immunity. J. Clin. Invest. 123:1976-1987.
34. + T-cell epitopes in the murine intranasal challenge model. Eur. J. Immunol. 39:717-722.
35. + T cells and protects against herpes simplex virus type 2 challenge. Mucosal Immunol. 2:129-143.
36. McKinney, D. M., R. Skvoretz, B. D. Livingston, C. C. Wilson, M. Anders, R. W. Chesnut, A. Sette, M. Essex, V. Novitsky, and M. J. Newman. 2004. Recognition of variant HIV-1 epitopes from diverse viral subtypes by vaccineinduced CTL. J. Immunol. 173:1941-1950.
37. *0201. J. Immunol. 172:6783-6789.
38. Hertz, T., and C. Yanover. 2007. Identifying HLA supertypes by learning distance functions. Bioinformatics 23:e148-e155.
39. Botten, J., J. Alexander, V. Pasquetto, J. Sidney, P. Barrowman, J. Ting, B. Peters, S. Southwood, B. Stewart, M. P. Rodriguez-Carreno, et al. 2006. Identification of protective Lassa virus epitopes that are restricted by HLA-A2. J. Virol. 80:8351-8361.
40. Harndahl, M., M. Rasmussen, G. Roder, I. Dalgaard Pedersen, M. Sørensen, M. Nielsen, and S. Buus. 2012. Peptide-MHC class I stability is a better predictor than peptide affinity of CTL immunogenicity. Eur. J. Immunol. 42:1405-1416.
41. Remakus, S., D. Rubio, X. Ma, A. Sette, and L. J. Sigal. 2012. Memory CD8+ T cells specific for a single immunodominant or subdominant determinant induced by peptide-dendritic cell immunization protect from an acute lethal viral disease. J. Virol. 86:9748-9759.
42. Pulendran, B., and R. Ahmed. 2011. Immunological mechanisms of vaccination. Nat. Immunol. 12:509-517.
43. Bevan, M. J. 2011. Understand memory, design better vaccines. Nat. Immunol. 12:463-465.
44. Koelle, D. M., H. B. Chen, C. M. McClurkan, and E. W. Petersdorf. 2002. Herpes simplex virus type 2-specific CD8 cytotoxic T lymphocyte crossreactivity against prevalent HLA class I alleles. Blood 99:3844-3847.
45. + T cell function and epitope breadth among persons with genital herpes. J. Clin. Immunol. 30:703-722.
46. Jing, L., J. Haas, T. M. Chong, J. J. Bruckner, G. C. Dann, L. Dong, J. O. Marshak, C. L. McClurkan, T. N. Yamamoto, S. M. Bailer, et al. 2012. Cross-presentation and genome-wide screening reveal candidate T cells antigens for a herpes simplex virus type 1 vaccine. J. Clin. Invest. 122:654-673.
47. + T-cell epitope of herpes simplex virus on virus replication and pathogenicity. Invest. Ophthalmol. Vis. Sci. 50:2903-2912.
48. + T cells suppress viral replication in the cornea but contribute to VEGF-C-induced lymphatic vessel genesis. J. Immunol. 189:425-432.
49. Stanberry, L. R., S. L. Spruance, A. L. Cunningham, D. I. Bernstein, A. Mindel, S. Sacks, S. Tyring, F. Y. Aoki, M. Slaoui, M. Denis, et al; GlaxoSmithKline Herpes Vaccine Efficacy Study Group. 2002. Glycoprotein-D- adjuvant vaccine to prevent genital herpes. N. Engl. J. Med. 347:1652-1661.
50. ε- palmitoyl-lysine moiety increase uptake and maturation of dendritic cells through a Toll-like receptor-2 pathway and trigger a Th1-dependent protective immunity. Eur. J. Immunol. 34:3102-3114.
51. Zarling, J. M., P. A. Moran, L. Brewer, R. Ashley, and L. Corey. 1988. Herpes simplex virus (HSV)-specific proliferative and cytotoxic T-cell responses in humans immunized with an HSV type 2 glycoprotein subunit vaccine. J. Virol. 62:4481-4485.
52. Bettahi, I., A. B. Nesburn, S. Yoon, X. Zhang, A. Mohebbi, V. Sue, A. Vanderberg, S. L. Wechsler, and L. Ben Mohamed. 2007. Protective immunity against ocular herpes infection and disease induced by highly immunogenic self-adjuvanting glycoprotein D lipopeptide vaccines. Invest. Ophthalmol. Vis. Sci. 48:4643-4653.
53. Cornberg, M., S. C. Clute, L. B. Watkin, F. M. Saccoccio, S. K. Kim, Y. N. Naumov, M. A. Brehm, N. Aslan, R. M. Welsh, and L. K. Selin. 2010. CD8 T cell cross-reactivity networks mediate heterologous immunity in human EBV and murine vaccinia virus infections. J. Immunol. 184:2825-2838.
54. + T-cell cross-reactivity and heterologous immunity. Immunol. Rev. 211:164-181.
55. Selin, L. K., M. Cornberg, M. A. Brehm, S. K. Kim, C. Calcagno, D. Ghersi, R. Puzone, F. Celada, and R. M. Welsh. 2004. CD8 memory T cells: crossreactivity and heterologous immunity. Semin. Immunol. 16:335-347.
56. Eberle, R., and D. Black. 1993. Sequence analysis of herpes simplex virus gB gene homologs of two platyrrhine monkey alpha-herpesviruses. Arch. Virol. 129:167-182.
57. Hannah, B. P., E. E. Heldwein, F. C. Bender, G. H. Cohen, and R. J. Eisenberg. 2007. Mutational evidence of internal fusion loops in herpes simplex virus glycoprotein B. J. Virol. 81:4858-4865.
58. Heldwein, E. E., H. Lou, F. C. Bender, G. H. Cohen, R. J. Eisenberg, and S. C. Harrison. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
59. El-Awar, N., J. H. Lee, C. Tarsitani, and P. I. Terasaki. 2007. HLA class I epitopes: recognition of binding sites by mAbs or eluted alloantibody confirmed with single recombinant antigens. Hum. Immunol. 68:170-180.
60. Pekiner, F. N., E. Aytugar, G. Y. Demirel, and M. O. Borahan. 2013. HLA-A, B (class I) and HLA-DR, DQ (class II) antigens in Turkish patients with recurrent aphthous ulceration and Behçet's disease. Med. Princ. Pract. 22:464-468. PubMed
61. Castelli, E. C., D. S. Gil, L. C. Veiga, and J. L. De Camargo. 2005. Typing class I HLA-A gene using a nested PCR-RFLP procedure. Braz. J. Med. Biol. Res. 38:837-842.
62. *0201 with high affinity crossreact with other A2-supertype molecules. Hum. Immunol. 62:1200-1216.
63. Cohen, J. 2010. Immunology. Painful failure of promising genital herpes vaccine. Science 330:304.
64. Wald, A., J. Zeh, S. Selke, T. Warren, A. J. Ryncarz, R. Ashley, J. N. Krieger, and L. Corey. 2000. Reactivation of genital herpes simplex virus type 2 infection in asymptomatic seropositive persons. N. Engl. J. Med. 342:844-850.
65. Tronstein, E., C. Johnston, M. L. Huang, S. Selke, A. Magaret, T. Warren, L. Corey, and A. Wald. 2011. Genital shedding of herpes simplex virus among symptomatic and asymptomatic persons with HSV-2 infection. JAMA 305:1441-1449.