Human cytotoxic CD4+ T cells recognize HLA-DR1-restricted epitopes on vaccinia virus proteins A24R and D1R conserved among poxviruses

Journal of Immunology

Volumn 179, Issue 2, 2007, Pages 1303-1312

  Mitra Kaushik, Shibani ^a   Cruz, John ^a   Stern, Lawrence J ^a   Ennis, Francis A ^a   Terajima, Masanori ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

A24R VIRUS VACCINIA VIRUS PROTEIN; CONCANAMYCIN A; D1R VACCINIA VIRUS PROTEIN; EPITOPE; HLA DR1 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SMALLPOX VACCINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; COWPOX; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; LYSIS; MONKEYPOX; PHOCOMELIA; POXVIRUS; PRIORITY JOURNAL; SMALLPOX VIRUS; VACCINIA VIRUS; AMINO ACID SEQUENCE; CELL LINE; EPITOPE MAPPING; GENETICS; IMMUNOLOGY; SEQUENCE HOMOLOGY; VIRUS GENE;

AMINO ACID SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; GENES, VIRAL; HLA-DR1 ANTIGEN; HUMANS; POXVIRIDAE; SEQUENCE HOMOLOGY, AMINO ACID; SMALLPOX VACCINE; T-LYMPHOCYTES, CYTOTOXIC; VACCINIA VIRUS; VIRAL PROTEINS;

EID: 34548779833     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.2.1303     Document Type: Article

References (93)

1. Fenner, F., D. A. Henderson, I. Arita, Z. Jezek, and I. D. Ladny. 1998. Smallpox and Its Eradication. World Health Organization, Geneva, Switzerland.
2. Enserink, M. 2002. Bioterrorism: in search of a kinder, gentler vaccine. Science 296: 1594.
3. Halsell, J. S., J. R. Riddle, J. E. Atwood, P. Gardner, R. Shope, G. A. Poland, G. C. Gray, S. Ostroff, R. E. Eckart, D. R. Hospenthal, et al. 2003. Myopericarditis following smallpox vaccination among vaccinia-naive US military personnel. J. Am. Med. Assoc. 289: 3283-3289.
4. U.S. Department of Defense, Office of the Assistant Secretary of Defense (Public Affairs). News Release June 22, 2006. Vaccines may have caused a soldier's death. Immediate Release No. 587- 06. www.defenselink.mil/ Releases/Release.aspx?ReleaseID=9675
5. Lane, J. M., F. L. Ruben, J. M. Neff, and J. D. Millar. 1969. Complications of smallpox vaccination, 1968. N. Engl. J. Med. 281: 1201-1208.
6. Lane, J. M., and J. D. Millar. 1971. Risks of smallpox vaccination complications in the United States. Am. J. Epidemiol. 93: 238-240.
7. Kempe, C. H., C. Bowles, G. Meiklejohn, T. O. Berge, L. St. Vincent, B. V. Babu, S. Govindarajan, N. R. Ratnakannan, A. W. Downie, and V. R. Murthy. 1961. The use of vaccinia hyperimmune γ-globulin in the prophylaxis of smallpox. Bull. W. H. O. 25: 41-48.
8. Hammarlund, E., M. W. Lewis, S. G. Hansen, L. I. Strelow, J. A. Nelson, G. J. Sexton, J. M. Hanifin, and M. K. Slifka. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9: 1131-1137.
9. Crotty, S., P. Felgner, H. Davies, J. Glidewell, L. Villarreal, and R. Ahmed. 2003. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171: 4969-4973.
10. Galmiche, M. C., J. Goenaga, R. Wittek, and L. Rindisbacher. 1999. Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 254: 71-80.
11. Edghill-Smith, Y., H. Golding, J. Manischewitz, L. R. King, D. Scott, M. Bray, A. Nalca, J. W. Hooper, C. A. Whitehouse, J. E. Schmitz, et al. 2005. Smallpox vaccine-induced antibodies are necessary and sufficient for protection against monkeypox virus. Nat. Med. 11: 740-747.
12. Stanford, M. M., and G. McFadden. 2005. The 'supervirus'? Lessons from IL-4-expressing poxviruses. Trends Immunol. 26: 339-345.
13. Sharma, D. P., A. J. Ramsay, D. J. Maguire, M. S. Rolph, and I. A. Ramshaw. 1996. Interleukin-4 mediates down-regulation of antiviral cytokine expression and cytotoxic T-lymphocyte responses and exacerbates vaccinia virus infection in vivo. J. Virol. 70: 7103-7107.
14. Hugin, A. W., C. Flexner, and B. Moss. 1993. Clearance of recombinant vaccinia virus expressing IL-2: role of local host immune responses. Cell. Immunol. 152: 499-509.
15. Flexner, C., A. Hugin, and B. Moss. 1987. Prevention of vaccinia virus infection in immunodeficient mice by vector-directed IL-2 expression. Nature 330: 259-262.
16. Perera, L. P., C. K. Goldman, and T. A. Waldmann. 2001. Comparative assessment of virulence of recombinant vaccinia viruses expressing IL-2 and IL-15 in immunodeficient mice. Proc. Natl. Acad. Sci. USA 98: 5146-5151.
17. Ramshaw, I., J. Ruby, A. Ramsay, G. Ada, and G. Karupiah. 1992. Expression of cytokines by recombinant vaccinia viruses: a model for studying cytokines in virus infections in vivo. Immunol. Rev. 127: 157-182.
18. + T cells is dependent on interferon-γ. Lymphokine Cytokine Res. 10: 353-358.
19. Muller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
20. Ramshaw, I. A., M. E. Andrew, S. M. Phillips, D. B. Boyle, and B. E. Coupar. 1987. Recovery of immunodeficient mice from a vaccinia virus/IL-2 recombinant infection. Nature 329: 545-546.
21. Selin, L. K., P. A. Santolucito, A. K. Pinto, E. Szomolanyi-Tsuda, and R. M. Welsh. 2001. Innate immunity to viruses: control of vaccinia virus infection by γδ T cells. J. Immunol. 166: 6784-6794.
22. Karupiah, G., B. E. Coupar, M. E. Andrew, D. B. Boyle, S. M. Phillips, A. Mullbacher, R. V. Blanden, and I. A. Ramshaw. 1990. Elevated natural killer cell responses in mice infected with recombinant vaccinia virus encoding murine IL-2. J. Immunol. 144: 290-298.
23. Kennedy, J. S., S. E. Frey, L. Yan, A. L. Rothman, J. Cruz, F. K. Newman, L. Orphin, R. B. Belshe, and F. A. Ennis. 2004. Induction of human T cell-mediated immune responses after primary and secondary smallpox vaccination. J. Infect. Dis. 190: 1286-1294.
24. Belyakov, I. M., P. Earl, A. Dzutsev, V. A. Kuznetsov, M. Lemon, L. S. Wyatt, J. T. Snyder, J. D. Ahlers, G. Franchini, B. Moss, and J. A. Berzofsky. 2003. Shared modes of protection against poxvirus infection by attenuated and conventional smallpox vaccine viruses. Proc. Natl. Acad. Sci. USA 100: 9458-9463.
25. Xu, R., A. J. Johnson, D. Liggitt, and M. J. Bevan. 2004. Cellular and humoral immunity against vaccinia virus infection of mice. J. Immunol. 172: 6265-6271.
26. + T-cell epitopes conserved among vaccinia and variola viruses restricted by common MHC class I molecules, HLA-A2 or HLA-B7. Hum. Immunol. 67: 512-520.
27. + T cell responses to newly identified HLA-A*0201-restricted T cell epitopes conserved among vaccinia and variola (smallpox) viruses. J. Exp. Med. 197: 927-932.
28. Pasquetto, V., H. H. Bui, R. Giannino, C. Banh, F. Mirza, J. Sidney, C. Oseroff, D. C. Tscharke, K. Irvine, J. R. Bennink, et al. 2005. HLA-A*0201, HLA-A* 1101, and HLA-B*0702 transgenic mice recognize numerous poxvirus determinants from a wide variety of viral gene products. J. Immunol. 175: 5504-5515.
29. Oseroff, C., F. Kos, H. H. Bui, B. Peters, V. Pasquetto, J. Glenn, T. Palmore, J. Sidney, D. C. Tscharke, J. R. Bennink, et al. 2005. HLA class I-restricted responses to vaccinia recognize a broad array of proteins mainly involved in virulence and viral gene regulation. Proc. Natl. Acad. Sci. USA 102: 13980-13985.
30. Drexler, I., C. Staib, W. Kastenmuller, S. Stevanovic, B. Schmidt, F. A. Lemonnier, H. G. Rammensee, D. H. Busch, H. Bernhard, V. Erfle, and G. Sutter. 2003. Identification of vaccinia virus epitope-specific HLA-A*0201- restricted T cells and comparative analysis of smallpox vaccines. Proc. Natl. Acad. Sci. USA 100: 217-222.
31. Jing, L., T. M. Chong, C. L. McClurkan, J. Huang, B. T. Story, and D. M. Koelle. 2005. Diversity in the acute CD8 T cell response to vaccinia virus in humans. J. Immunol. 175: 7550-7559.
32. Tang, J., M. Murtadha, M. Schnell, L. C. Eisenlohr, J. Hooper, and P. Flomenberg. 2006. Human T-cell responses to vaccinia virus envelope proteins. J. Virol. 80: 10010-10020.
33. + cytotoxic T lymphocyte responses to a novel epitope in vaccinia virus that is conserved among orthopox viruses. J. Infect. Dis. 194: 168-175.
34. Sahin, U., O. Tureci, C. Graf, R. G. Meyer, V. Lennerz, C. M. Britten, C. Dumrese, E. Scandella, T. Wolfel, and B. Ludewig. 2006. Rapid molecular dissection of viral and bacterial immunomes. Eur. J. Immunol. 36: 1049-1057.
35. + CTL epitopes with distinct functional profiles. J. Immunol. 174: 2212-2219.
36. + T-cell determinants and cross-reactivity in BALB/c mice. J. Virol. 80: 6318-6323.
37. +)-cell responses to vaccinia virus. Nat. Biotechnol. 24: 817-819.
38. + T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 201: 95-104.
39. Demkowicz, W. E., Jr., R. A. Littaua, J. Wang, and F. A. Ennis. 1996. Human cytotoxic T-cell memory: long-lived responses to vaccinia virus. J. Virol. 70: 2627-2631.
40. + cytotoxic T-lymphocyte clones. J. Virol. 66: 2274-2280.
41. Amara, R. R., P. Nigam, S. Sharma, J. Liu, and V. Bostik. 2004. Long-lived poxvirus immunity, robust CD4 help, and better persistence of CD4 than CD8 T cells. J. Virol. 78: 3811-3816.
42. Rock, M. T., S. M. Yoder, T. R. Talbot, K. M. Edwards, and J. E. Crowe, Jr. 2006. Cellular immune responses to diluted and undiluted aventis Pasteur smallpox vaccine. J. Infect. Dis. 194: 435-443.
43. Harrington, L. E., R. Most Rv, J. L. Whitton, and R. Ahmed. 2002. Recombinant vaccinia virus-induced T-cell immunity: quantitation of the response to the virus vector and the foreign epitope. J. Virol. 76: 3329-3337.
44. + T-cell-deficient mice survive inoculation with high doses of vaccinia virus and exhibit altered IgG responses. Proc. Natl. Acad. Sci. USA 89: 6070-6074.
45. Kagi, D., P. Seiler, J. Pavlovic, B. Ledermann, K. Burki, R. M. Zinkernagel, and H. Hengartner. 1995. The roles of perforin- and Fas-dependent cytotoxicity in protection against cytopathic and noncytopathic viruses. Eur. J. Immunol. 25: 3256-3262.
46. Centers for Disease Control and Prevention. 2001. Vaccinia (smallpox) vaccine recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep. 50: 1-25.
47. Salter, R. D., D. N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21: 235-246.
48. Terajima, M., H. L. Van Epps, D. Li, A. M. Leporati, S. E. Juhlin, J. Mustonen, A. Vaheri, and F. A. Ennis. 2002. Generation of recombinant vaccinia viruses expressing Puumala virus proteins and use in isolating cytotoxic T cells specific for Puumala virus. Virus Res. 84: 67-77.
49. + cytotoxic T-lymphocyte clone to a conserved epitope on human immunodeficiency virus type 1 p24: cytotoxic activity and secretion of interleukin-2 and interleukin-6. J. Virol. 66: 608-611.
50. Antoine, G., F. Scheiflinger, F. Dorner, and F. G. Falkner. 1998. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244: 365-396.
51. Hammer, J., E. Bono, F. Gallazzi, C. Belunis, Z. Nagy, and F. Sinigaglia. 1994. Precise prediction of major histocompatibility complex class II-peptide interaction based on peptide side chain scanning. J. Exp. Med. 180: 2353-2358.
52. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanovic. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
53. +-ATPase inhibitors on CTL-mediated cytotoxicity. Immunol. Lett. 55: 139-144.
54. Kataoka, T., N. Shinohara, H. Takayama, K. Takaku, S. Kondo, S. Yonehara, and K. Nagai. 1996. Concanamycin A, a powerful tool for characterization and estimation of contribution of perforin- and Fas-based lytic pathways in cell-mediated cytotoxicity. J. Immunol. 156: 3678-3686.
55. + cytotoxic T lymphocytes in humans. Blood 95: 2352-2355.
56. + T-cell clone directed against an acute myelogenous leukemia-associated DEK-CAN fusion peptide. Blood 93: 925-935.
57. Li, Q., A. Nakadai, K. Takeda, and T. Kawada. 2004. Dimethyl 2,2-dichlorovinyl phosphate (DDVP) markedly inhibits activities of natural killer cells, cytotoxic T lymphocytes and lymphokine-activated killer cells via the Fas-ligand/Fas pathway in perforin-knockout (PKO) mice. Toxicology 204: 41-50.
58. Van Epps, H. L., M. Terajima, J. Mustonen, T. P. Arstila, E. A. Corey, A. Vaheri, and F. A. Ennis. 2002. Long-lived memory T lymphocyte responses after hantavirus infection. J. Exp. Med. 196: 579-588.
59. Weltzin, R., J. Liu, K. V. Pugachev, G. A. Myers, B. Coughlin, P. S. Blum, R. Nichols, C. Johnson, J. Cruz, J. S. Kennedy, et al. 2003. Clonal vaccinia virus grown in cell culture as a new smallpox vaccine. Nat. Med. 9: 1125-1130.
60. + cytotoxic T lymphocytes and interferon-γ-producing T cells after smallpox vaccination. J. Infect. Dis. 185: 1657-1659.
61. Marsh, S. G. E., P. Parham, and L. D. Barber. 2000. HLA-DR. In The HLA FactsBook. Academic Press, San Diego, pp. 323-390.
62. Imanishi, T., T. Akaza, A. Kimura, K. Tokunaga, and T. Gojobori. 1997. Allele and haplotype frequencies for HLA and complement loci in various ethnic group. In Proceedings of the Twelfth International Histocompatibility Workshop and Conference, June 9-12. D. Charron, ed. Medical and Scientific Publisher, Paris, pp. 1065-1074.
63. Sinigaglia, F., M. Guttinger, J. Kilgus, D. M. Doran, H. Matile, H. Etlinger, A. Trzeciak, D. Gillessen, and J. R. Pink. 1988. A malaria T-cell epitope recognized in association with most mouse and human MHC class II molecules. Nature 336: 778-780.
64. Doolan, D. L., S. Southwood, R. Chesnut, E. Appella, E. Gomez, A. Richards, Y. I. Higashimoto, A. Maewal, J. Sidney, R. A. Gramzinski, et al. 2000. HLA-DR-promiscuous T cell epitopes from Plasmodium falciparum pre-erythrocytic-stage antigens restricted by multiple HLA class II alleles. J. Immunol. 165: 1123-1137.
65. + T cell epitope from the C1 domain of factor VIII. J. Thromb. Haemost. 3: 991-1000.
66. Southwood, S., J. Sidney, A. Kondo, M. F. del Guercio, E. Appella, S. Hoffman, R. T. Kubo, R. W. Chesnut, H. M. Grey, and A. Sette. 1998. Several common HLA-DR types share largely overlapping peptide binding repertoires. J. Immunol. 160: 3363-3373.
67. Doytchinova, I. A., and D. R. Flower. 2005. In silico identification of supertypes for class II MHCs. J. Immunol. 174: 7085-7095.
68. Roche, P. A., and P. Cresswell. 1990. High-affinity binding of an influenza hemagglutinin-derived peptide to purified HLA-DR. J. Immunol. 144: 1849-1856.
69. + CTLs ex vivo. J. Immunol. 168: 5954-5958.
70. Penna, A., P. Fowler, A. Bertoletti, S. Guilhot, B. Moss, R. F. Margolskee, A. Cavalli, A. Valli, F. Fiaccadori, F. V. Chisari, et al. 1992. Hepatitis B virus (HBV)-specific cytotoxic T-cell (CTL) response in humans: characterization of HLA class II-restricted CTLs that recognize endogenously synthesized HBV envelope antigens. J. Virol. 66: 1193-1198.
71. + cytotoxic T lymphocyte clones. Virology 234: 383-386.
72. + cytotoxic T-cell responses and long-term T-cell memory in individuals vaccinated against polio. J. Virol. 79: 5988-5995.
73. + phenotype. J. Immunol. 146: 257-264.
74. Gyulai, Z., V. Endresz, K. Burian, S. Pincus, J. Toldy, W. I. Cox, C. Meric, S. Plotkin, E. Gonczol, and K. Berencsi. 2000. Cytotoxic T lymphocyte (CTL) responses to human cytomegalovirus pp65, IE1-Exon4, gB, pp150, and pp28 in healthy individuals: reevaluation of prevalence of IE1-specific CTLs. J. Infect. Dis. 181: 1537-1546.
75. + T lymphocytes consistently respond to the latent Epstein-Barr virus nuclear antigen EBNA1. J. Exp. Med. 191: 1649-1660.
76. - T cells and is restricted to the DR region of the MHC complex. J. Immunol. 140: 3610-3616.
77. + cytotoxic T-lymphocyte clones. J. Virol. 73: 3623-3629.
78. + cell elimination regularly develops in uncloned human antiviral cell lines. J. Immunol. 142: 252-256.
79. + T cells. J. Virol. 78: 8844-8851.
80. Jellison, E. R., S. K. Kim, and R. M. Welsh. 2005. Cutting edge: MHC class II-restricted killing in vivo during viral infection. J. Immunol. 174: 614-618.
81. + T cells in protective immunity to influenza. Immunol. Rev. 211: 8-22.
82. + T lymphocytes with cellular maturation. J. Exp. Med. 203: 2865-2877.
83. Smith, C., L. F. Mirza, V. Pasquetto, D. C. Tscharke, M. J. Palmowski, P. R. Dunbar, A. Sette, A. L. Harris, and V. Cerundolo. 2005. Immunodominance of poxviral-specific CTL in a human trial of recombinant-modified vaccinia Ankara. J. Immunol. 175: 8431-8437.
84. Rudensky, A., P. Preston-Hurlburt, S. C. Hong, A. Barlow, and C. A. Janeway, Jr. 1991. Sequence analysis of peptides bound to MHC class II molecules. Nature 353: 622-627.
85. Chicz, R. M., R. G. Urban, J. C. Gorga, D. A. Vignali, W. S. Lane, and J. L. Strominger. 1993. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J. Exp. Med. 178: 27-47.
86. Jaraquemada, D., M. Marti, and E. O. Long. 1990. An endogenous processing pathway in vaccinia virus-infected cells for presentation of cytoplasmic antigens to class II-restricted T cells. J. Exp. Med. 172: 947-954.
87. Jacobson, S., R. P. Sekaly, W. J. Bellini, C. L. Johnson, H. F. McFarland, and E. O. Long. 1988. Recognition of intracellular measles virus antigens by HLA class II restricted measles virus-specific cytotoxic T lymphocytes. Ann. NY Acad. Sci. 540: 352-353.
88. Malnati, M. S., S. Ceman, M. Weston, R. DeMars, and E. O. Long. 1993. Presentation of cytosolic antigen by HLA-DR requires a function encoded in the class II region of the MHC. J. Immunol. 151: 6751-6756.
89. Morrison, L. A., A. E. Lukacher, V. L. Braciale, D. P. Fan, and T. J. Braciale. 1986. Differences in antigen presentation to MHC class I- and class II-restricted influenza virus-specific cytolytic T lymphocyte clones. J. Exp. Med. 163: 903-921.
90. Tewari, M. K., G. Sinnathamby, D. Rajagopal, and L. C. Eisenlohr. 2005. A cytosolic pathway for MHC class II-restricted antigen processing that is proteasome and TAP dependent. Nat. Immunol. 6: 287-294.
91. + T cells proliferating in response to influenza A antigen. J. Clin. Invest. 104: R63-R67.
92. + T cell responses directed against influenza viral antigens postinfluenza vaccination. J. Immunol. 171: 3163-3169.
93. + T cells with specificity for a new major histocompatibility complex class II-restricted influenza A virus matrix protein epitope in peripheral blood of influenza patients. J. Virol. 74: 8740-8743.