The identification of HLA class II-restricted T cell epitopes to vaccinia virus membrane proteins

Virology

Volumn 408, Issue 2, 2010, Pages 232-240

  Kennedy, Richard B ^a   Poland, Gregory A ^a  

^a MAYO CLINIC   (United States)

Author keywords

CD4+ T cells; Cellular immunity; Smallpox vaccine; T cell epitopes; Vaccinia virus

Indexed keywords

EPITOPE; HLA ANTIGEN CLASS 2; MEMBRANE PROTEIN; PEPTIDE VACCINE; SUBUNIT VACCINE;

ANIMAL CELL; ANTIGEN DETECTION; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNE RESPONSE; NONHUMAN; POXVIRUS; PRIORITY JOURNAL; PROTEIN TARGETING; T LYMPHOCYTE; VACCINE PRODUCTION; VACCINIA VIRUS; VERO CELL;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CROSS REACTIONS; EPITOPES, T-LYMPHOCYTE; HELA CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; INTERFERON-GAMMA; MOLECULAR SEQUENCE DATA; SMALLPOX VACCINE; SPECIES SPECIFICITY; T-LYMPHOCYTES, HELPER-INDUCER; VACCINES, SUBUNIT; VACCINIA VIRUS; VARIOLA VIRUS; VIRAL ENVELOPE PROTEINS;

POXVIRIDAE; VACCINIA VIRUS; VARIOLA VIRUS;

EID: 78149414739     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.09.013     Document Type: Article

References (100)

1. Adamopoulou E., Diekmann J., Tolosa E., Kuntz G., Einsele H., Rammensee H.G., Topp M.S. Human CD4+ T cells displaying viral epitopes elicit a functional virus-specific memory CD8+ T cell response. J. Immunol. 2007, 178(9):5465-5472.
2. Artenstein A.W. New generation smallpox vaccines: a review of preclinical and clinical data. Rev. Med. Virol. 2008, 18(4):217-231.
3. Bell E., Shamim M., Whitbeck J.C., Sfyroera G., Lambris J.D., Isaacs S.N. Antibodies against the extracellular enveloped virus B5R protein are mainly responsible for the EEV neutralizing capacity of vaccinia immune globulin. Virology 2004, 325(2):425-431.
4. Bernard A., Coitot S., Bremont A., Bernard G. T and B cell cooperation: a dance of life and death. Transplantation 2005, 79(3 Suppl):S8-S11.
5. Bishop G.A., Hostager B.S. B lymphocyte activation by contact-mediated interactions with T lymphocytes. Curr. Opin. Immunol. 2001, 13(3):278-285.
6. Calvo-Calle J.M., Strug I., Nastke M.D., Baker S.P., Stern L.J. Human CD4+ T cell epitopes from vaccinia virus induced by vaccination or infection. PLoS Pathog. 2007, 3(10):1511-1529.
7. Chen H.D., Fraire A.E., Joris I., Brehm M.A., Welsh R.M., Selin L.K. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat. Immunol. 2001, 2(11):1067-1076.
8. Chung C.S., Hsiao J.C., Chang Y.S., Chang W. A27L protein mediates vaccinia virus interaction with cell surface heparan sulfate. J. Virol. 1998, 72(2):1577-1585.
9. Clute S.C., Watkin L.B., Cornberg M., Naumov Y.N., Sullivan J.L., Luzuriaga K., Welsh R.M., Selin L.K. Cross-reactive influenza virus-specific CD8+ T cells contribute to lymphoproliferation in Epstein-Barr virus-associated infectious mononucleosis. J. Clin. Invest. 2005, 115(12):3602-3612.
10. Combadiere B., Boissonnas A., Carcelain G., Lefranc E., Samri A., Bricaire F., Debre P., Autran B. Distinct time effects of vaccination on long-term proliferative and IFN-gamma-producing T cell memory to smallpox in humans. J. Exp. Med. 2004, 199(11):1585-1593.
11. Cornberg M., Sheridan B.S., Saccoccio F.M., Brehm M.A., Selin L.K. Protection against vaccinia virus challenge by CD8 memory T cells resolved by molecular mimicry. J. Virol. 2007, 81(2):934-944.
12. Cornberg M., Clute S.C., Watkin L.B., Saccoccio F.M., Kim S.K., Naumov Y.N., Brehm M.A., Aslan N., Welsh R.M., Selin L.K. CD8 T cell cross-reactivity networks mediate heterologous immunity in human EBV and murine vaccinia virus infections. J. Immunol. 2010, 184(6):2825-2838.
13. Crotty S., Felgner P., Davies H., Glidewell J., Villarreal L., Ahmed R. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 2003, 171(10):4969-4973.
14. Davies D.H., Molina D.M., Wrammert J., Miller J., Hirst S., Mu Y., Pablo J., Unal B., Nakajima-Sasaki R., Liang X., Crotty S., Karem K.L., Damon I.K., Ahmed R., Villarreal L., Felgner P.L. Proteome-wide analysis of the serological response to vaccinia and smallpox. Proteomics 2007, 7(10):1678-1686.
15. Davies D.H., Wyatt L.S., Newman F.K., Earl P.L., Chun S., Hernandez J.E., Molina D.M., Hirst S., Moss B., Frey S.E., Felgner P.L. Antibody profiling by proteome microarray reveals the immunogenicity of the attenuated smallpox vaccine modified vaccinia virus ankara is comparable to that of Dryvax. J. Virol. 2008, 82(2):652-663.
16. Drexler I., Staib C., Kastenmuller W., Stevanovic S., Schmidt B., Lemonnier F.A., Rammensee H.G., Busch D.H., Bernhard H., Erfle V., Sutter G. Identification of vaccinia virus epitope-specific HLA-A*0201-restricted T cells and comparative analysis of smallpox vaccines. Proc. Natl. Acad. Sci. USA 2003, 100(1):217-222.
17. Duke-Cohan J.S., Wollenick K., Witten E.A., Seaman M.S., Baden L.R., Dolin R., Reinherz E.L. The heterogeneity of human antibody responses to vaccinia virus revealed through use of focused protein arrays. Vaccine 2009, 27(8):1154-1165.
18. el-Ad B., Roth Y., Winder A., Tochner Z., Lublin-Tennenbaum T., Katz E., Schwartz T. The persistence of neutralizing antibodies after revaccination against smallpox. J. Infect. Dis. 1990, 161(3):446-448.
19. Ennis F.A., Cruz J., Demkowicz W.E., Rothman A.L., McClain D.J. Primary induction of human CD8+ cytotoxic T lymphocytes and interferon-gamma-producing T cells after smallpox vaccination. J. Infect. Dis. 2002, 185(11):1657-1659.
20. Fenner F. A successful eradication campaign. Global eradication of smallpox. Rev. Infect. Dis. 1982, 4(5):916-930.
21. Fenner F., Henderson D.A., Arita I., Jezek Z., Ladnyi I.D. Smallpox and Its Eradication. History of International Public Health 1988, 6. W.H.O., Geneva.
22. Ferrier-Rembert A., Drillien R., Tournier J.N., Garin D., Crance J.M. Short- and long-term immunogenicity and protection induced by non-replicating smallpox vaccine candidates in mice and comparison with the traditional 1st generation vaccine. Vaccine 2008, 26(14):1794-1804.
23. Fogg C., Lustig S., Whitbeck J.C., Eisenberg R.J., Cohen G.H., Moss B. Protective immunity to vaccinia virus induced by vaccination with multiple recombinant outer membrane proteins of intracellular and extracellular virions. J. Virol. 2004, 78(19):10230-10237.
24. Frey S.E., Newman F.K., Yan L., Lottenbach K.R., Belshe R.B. Response to smallpox vaccine in persons immunized in the distant past. JAMA 2003, 289(24):3295-3299.
25. Fulginiti V.A. Risks of smallpox vaccination. JAMA 2003, 290(11):1452. (author reply 1452).
26. Fulginiti V.A., Papier A., Lane J.M., Neff J.M., Henderson D.A. Smallpox vaccination: a review, part II. Adverse events. Clin. Infect. Dis. 2003, 37(2):251-271.
27. Galmiche M.C., Goenaga J., Wittek R., Rindisbacher L. Neutralizing and protective antibodies directed against vaccinia virus envelope antigens. Virology 1999, 254(1):71-80.
28. Golden J.W., Josleyn M.D., Hooper J.W. Targeting the vaccinia virus L1 protein to the cell surface enhances production of neutralizing antibodies. Vaccine 2008, 26(27-28):3507-3515.
29. Goldstein J.A., Neff J.M., Lane J.M., Koplan J.P. Smallpox vaccination reactions, prophylaxis, and therapy of complications. Pediatrics 1975, 55(3):342-347.
30. Golovkin M., Spitsin S., Andrianov V., Smirnov Y., Xiao Y., Pogrebnyak N., Markley K., Brodzik R., Gleba Y., Isaacs S.N., Koprowski H. Smallpox subunit vaccine produced in planta confers protection in mice. Proc. Natl. Acad. Sci. USA 2007, 104(16):6864-6869.
31. Hammarlund E., Lewis M.W., Hansen S.G., Strelow L.I., Nelson J.A., Sexton G.J., Hanifin J.M., Slifka M.K. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 2003, 9(9):1131-1137.
32. Hammer J., Bono E., Gallazzi F., Belunis C., Nagy Z., Sinigaglia F. Precise prediction of major histocompatibility complex class II-peptide interaction based on peptide side chain scanning. J. Exp. Med. 1994, 180(6):2353-2358.
33. Henderson D.A. The looming threat of bioterrorism. Science 1999, 283(5406):1279-1282.
34. Henderson D.A., Inglesby T.V., Bartlett J.G., Ascher M.S., Eitzen E., Jahrling P.B., Hauer J., Layton M., McDade J., Osterholm M.T., O'Toole T., Parker G., Perl T., Russell P.K., Tonat K. Smallpox as a biological weapon: medical and public health management. Working Group on Civilian Biodefense. JAMA 1999, 281(22):2127-2137.
35. Heraud J.M., Edghill-Smith Y., Ayala V., Kalisz I., Parrino J., Kalyanaraman V.S., Manischewitz J., King L.R., Hryniewicz A., Trindade C.J., Hassett M., Tsai W.P., Venzon D., Nalca A., Vaccari M., Silvera P., Bray M., Graham B.S., Golding H., Hooper J.W., Franchini G. Subunit recombinant vaccine protects against monkeypox. J. Immunol. 2006, 177(4):2552-2564.
36. Hooper J.W., Custer D.M., Schmaljohn C.S., Schmaljohn A.L. DNA vaccination with vaccinia virus L1R and A33R genes protects mice against a lethal poxvirus challenge. Virology 2000, 266(2):329-339.
37. Hooper J.W., Custer D.M., Thompson E. Four-gene-combination DNA vaccine protects mice against a lethal vaccinia virus challenge and elicits appropriate antibody responses in nonhuman primates. Virology 2003, 306(1):181-195.
38. Huang J.F., Yang Y., Sepulveda H., Shi W., Hwang I., Peterson P.A., Jackson M.R., Sprent J., Cai Z. TCR-mediated internalization of peptide-MHC complexes acquired by T cells. Science 1999, 286(5441):952-954.
39. Isaacs S.N., Wolffe E.J., Payne L.G., Moss B. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J. Virol. 1992, 66(12):7217-7224.
40. Jahrling P.B., Fritz E.A., Hensley L.E. Countermeasures to the bioterrorist threat of smallpox. Curr. Mol. Med. 2005, 5(8):817-826.
41. Jenner E. An inquiry into the causes and effects of the variolae vaccinae, a disease discovered in some of the western counties of England, particularly Gloucestershire, and known by the name of the cow pox 1798, Law, London.
42. Jing L., Chong T.M., McClurkan C.L., Huang J., Story B.T., Koelle D.M. Diversity in the acute CD8 T cell response to vaccinia virus in humans. J. Immunol. 2005, 175(11):7550-7559.
43. Jing L., Chong T.M., Byrd B., McClurkan C.L., Huang J., Story B.T., Dunkley K.M., Aldaz-Carroll L., Eisenberg R.J., Cohen G.H., Kwok W.W., Sette A., Koelle D.M. Dominance and diversity in the primary human CD4 T cell response to replication-competent vaccinia virus. J. Immunol. 2007, 178(10):6374-6386.
44. Jing L., Davies D.H., Chong T.M., Chun S., McClurkan C.L., Huang J., Story B.T., Molina D.M., Hirst S., Felgner P.L., Koelle D.M. An extremely diverse CD4 response to vaccinia virus in humans is revealed by proteome-wide T-cell profiling. J. Virol. 2008, 82(14):7120-7134.
45. Johnson K.L., Ovsyannikova I.G., Madden B.J., Poland G.A., Muddiman D.C. Accurate mass precursor ion data and tandem mass spectrometry identify a class I human leukocyte antigen A* 0201-presented peptide originating from vaccinia virus. J. Am. Soc. Mass Spectrom. 2005, 16(11):1812-1817.
46. Kan V.L., Manischewitz J., King L.R., Golding H. Durable neutralizing antibodies after remote smallpox vaccination among adults with and without HIV infection. AIDS 2007, 21(4):521-524.
47. Kennedy R., Poland G.A. T-Cell epitope discovery for variola and vaccinia viruses. Rev. Med. Virol. 2007, 17(2):93-113.
48. Kennedy R., Undale A.H., Kieper W.C., Block M.S., Pease L.R., Celis E. Direct cross-priming by th lymphocytes generates memory cytotoxic T cell responses. J. Immunol. 2005, 174(7):3967-3977.
49. Kennedy R., Pankratz V.S., Swanson E., Watson D., Golding H., Poland G.A. Statistical approach to estimate vaccinia-specific neutralizing antibody titers using a high throughput assay. Clin. Vaccine Immunol. 2009, 16(8):1105-1112.
50. Kennedy R.B., Ovsyannikova I., Poland G.A. Smallpox vaccines for biodefense. Vaccine 2009, 27(Suppl 4):D73-D79.
51. Kennedy R.B., Ovsyannikova I.G., Jacobson R.M., Poland G.A. The immunology of smallpox vaccines. Curr. Opin. Immunol. 2009, 21(3):314-320.
52. Lane J.M., Ruben F.L., Abrutyn E., Millar J.D. Deaths attributable to smallpox vaccination, 1959 to 1966, and 1968. JAMA 1970, 212(3):441-444.
53. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature 1985, 314(6011):537-539.
54. Lanzavecchia A., Bove S. Specific B lymphocytes efficiently pick up, process and present antigen to T cells. Behring Inst. Mitt. 1985, (77):82-87.
55. Larkin M. Monkeypox spreads as US public-health system plays catch-up. Lancet Infect. Dis. 2003, 3(8):461.
56. Larsen M.V., Lundegaard C., Lamberth K., Buus S., Lund O., Nielsen M. Large-scale validation of methods for cytotoxic T-lymphocyte epitope prediction. BMC Bioinform. 2007, 8:424.
57. Lawrence S.J., Lottenbach K.R., Newman F.K., Buller R.M., Bellone C.J., Chen J.J., Cohen G.H., Eisenberg R.J., Belshe R.B., Stanley S.L., Frey S.E. Antibody responses to vaccinia membrane proteins after smallpox vaccination. J. Infect. Dis. 2007, 196(2):220-229.
58. Manischewitz J., King L.R., Bleckwenn N.A., Shiloach J., Taffs R., Merchlinsky M., Eller N., Mikolajczyk M.G., Clanton D.J., Monath T., Weltzin R.A., Scott D.E., Golding H. Development of a novel vaccinia-neutralization assay based on reporter-gene expression. J. Infect. Dis. 2003, 188(3):440-448.
59. Mathew A., Terajima M., West K., Green S., Rothman A.L., Ennis F.A., Kennedy J.S. Identification of murine poxvirus-specific CD8+ CTL epitopes with distinct functional profiles. J. Immunol. 2005, 174(4):2212-2219.
60. Mayr A. Smallpox vaccination and bioterrorism with pox viruses. Comp. Immunol. Microbiol. Infect. Dis. 2003, 26(5-6):423-430.
61. Meister G.E., Roberts C.G., Berzofsky J.A., De Groot A.S. Two novel T cell epitope prediction algorithms based on MHC-binding motifs; comparison of predicted and published epitopes from Mycobacterium tuberculosis and HIV protein sequences. Vaccine 1995, 13(6):581-591.
62. Metzger W., Mordmueller B.G. Vaccines for preventing smallpox. Cochrane Database Syst. Rev. 2007, (3). (CD004913).
63. Mitra-Kaushik S., Cruz J., Stern L.J., Ennis F.A., Terajima M. Human cytotoxic CD4+ T cells recognize HLA-DR1-restricted epitopes on vaccinia virus proteins A24R and D1R conserved among poxviruses. J. Immunol. 2007, 179(2):1303-1312.
64. Moise L., McMurry J.A., Buus S., Frey S., Martin W.D., De Groot A.S. In silico-accelerated identification of conserved and immunogenic variola/vaccinia T-cell epitopes. Vaccine 2009.
65. Morgan J., Roper M.H., Sperling L., Schieber R.A., Heffelfinger J.D., Casey C.G., Miller J.W., Santibanez S., Herwaldt B., Hightower P., Moro P.L., Hibbs B.F., Levine N.H., Chapman L.E., Iskander J., Lane J.M., Wharton M., Mootrey G.T., Swerdlow D.L. Myocarditis, pericarditis, and dilated cardiomyopathy after smallpox vaccination among civilians in the United States, January-October 2003. Clin. Infect. Dis. 2008, 46(Suppl 3):S242-S250.
66. Moutaftsi M., Peters B., Pasquetto V., Tscharke D.C., Sidney J., Bui H.H., Grey H., Sette A. A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat. Biotechnol. 2006, 24(7):817-819.
67. Moutaftsi M., Tscharke D.C., Vaughan K., Koelle D.M., Stern L., Calvo-Calle M., Ennis F., Terajima M., Sutter G., Crotty S., Drexler I., Franchini G., Yewdell J.W., Head J.W., Blum J., Peters B., Sette A. Uncovering the interplay between CD8, CD4 and antibody responses to complex pathogens. Future Microbiol 2010, 5(2):221-239.
68. Neff J.M., Lane J.M., Pert J.H., Moore R., Millar J.D., Henderson D.A. Complications of smallpox vaccination. I. National survey in the United States, 1963. N. Engl. J. Med. 1967, 276(3):125-132.
69. Noelle R.J., Snow E.C. T helper cell-dependent B cell activation. FASEB J. 1991, 5(13):2770-2776.
70. Oseroff C., Kos F., Bui H.H., Peters B., Pasquetto V., Glenn J., Palmore T., Sidney J., Tscharke D.C., Bennink J.R., Southwood S., Grey H.M., Yewdell J.W., Sette A. 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 2005, 102(39):13980-13985.
71. Otero M., Calarota S.A., Dai A., De Groot A.S., Boyer J.D., Weiner D.B. Efficacy of novel plasmid DNA encoding vaccinia antigens in improving current smallpox vaccination strategy. Vaccine 2006, 24(21):4461-4470.
72. Pasquetto V., Bui H.H., Giannino R., Banh C., Mirza F., Sidney J., Oseroff C., Tscharke D.C., Irvine K., Bennink J.R., Peters B., Southwood S., Cerundolo V., Grey H., Yewdell J.W., Sette A. HLA-A*0201, HLA-A*1101, and HLA-B*ral gene products. J. Immunol. 2005, 175(8):5504-5515.
73. Pasquetto V., Bui H.H., Giannino R., Mirza F., Sidney J., Oseroff C., Tscharke D.C., Irvine K., Bennink J.R., Peters B., Southwood S., Cerundolo V., Grey H., Yewdell J.W., Sette A. 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. 2005, 175(8):5504-5515.
74. Poland G.A. Smallpox vaccines: from first to second to third generation. Lancet 2005, 365(9457):362-363.
75. Rammensee H.G., Friede T., Stevanoviic S. MHC ligands and peptide motifs: first listing. Immunogenetics 1995, 41(4):178-228.
76. Rammensee H., Bachmann J., Emmerich N.P., Bachor O.A., Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999, 50(3-4):213-219.
77. Roederer M., Koup R.A. Optimized determination of T cell epitope responses. J. Immunol. Methods 2003, 274(1-2):221-228.
78. Roomp K., Antes I., Lengauer T. Predicting MHC class I epitopes in large datasets. BMC Bioinformatics 2010, 11:90.
79. Roper R.L., Wolffe E.J., Weisberg A., Moss B. The envelope protein encoded by the A33R gene is required for formation of actin-containing microvilli and efficient cell-to-cell spread of vaccinia virus. J. Virol. 1998, 72(5):4192-4204.
80. Ryan J.E., Ovsyannikova I.G., Dhiman N., Pinsky N.A., Vierkant R.A., Jacobson R.M., Poland G.A. Inter-operator variation in ELISPOT analysis of measles virus-specific IFN-gamma-secreting T cells. Scand. J. Clin. Lab. Invest. 2005, 65(8):681-689.
81. Ryan J.E., Ovsyannikova I.G., Poland G.A. Detection of measles virus-specific interferon-gamma-secreting T-cells by ELISPOT. Methods Mol. Biol. 2005, 302:207-218.
82. Sakhatskyy P., Wang S., Zhang C., Chou T.H., Kishko M., Lu S. Immunogenicity and protection efficacy of subunit-based smallpox vaccines using variola major antigens. Virology 2008, 371(1):98-107.
83. Selin L.K., Varga S.M., Wong I.C., Welsh R.M. Protective heterologous antiviral immunity and enhanced immunopathogenesis mediated by memory T cell populations. J. Exp. Med. 1998, 188(9):1705-1715.
84. Sette A., Moutaftsi M., Moyron-Quiroz J., McCausland M.M., Davies D.H., Johnston R.J., Peters B., Rafii-El-Idrissi Benhnia M., Hoffmann J., Su H.P., Singh K., Garboczi D.N., Head S., Grey H., Felgner P.L., Crotty S. Selective CD4+ T cell help for antibody responses to a large viral pathogen: deterministic linkage of specificities. Immunity 2008, 28(6):847-858.
85. Sette A., Grey H., Oseroff C., Peters B., Moutaftsi M., Crotty S., Assarsson E., Greenbaum J., Kim Y., Kolla R., Tscharke D., Koelle D., Johnson R.P., Blum J., Head S., Sidney J. Definition of epitopes and antigens recognized by vaccinia specific immune responses: their conservation in variola virus sequences, and use as a model system to study complex pathogens. Vaccine 2009, 27(Suppl 6):G21-G26.
86. Sidney J., Assarsson E., Moore C., Ngo S., Pinilla C., Sette A., Peters B. Quantitative peptide binding motifs for 19 human and mouse MHC class I molecules derived using positional scanning combinatorial peptide libraries. Immunome Res. 2008, 4:2.
87. Sirven P., Castelli F.A., Probst A., Szely N., Maillere B. In vitro human CD4+ T cell response to the vaccinia protective antigens B5R and A33R. Mol. Immunol. 2009, 46(7):1481-1487.
88. Snyder J.T., Belyakov I.M., Dzutsev A., Lemonnier F., Berzofsky J.A. Protection against lethal vaccinia virus challenge in HLA-A2 transgenic mice by immunization with a single CD8+ T-cell peptide epitope of vaccinia and variola viruses. J. Virol. 2004, 78(13):7052-7060.
89. Strug I., Calvo-Calle J.M., Green K.M., Cruz J., Ennis F.A., Evans J.E., Stern L.J. Vaccinia peptides eluted from HLA-DR1 isolated from virus-infected cells are recognized by CD4+ T cells from a vaccinated donor. J. Proteome Res. 2008, 7(7):2703-2711.
90. Tang J., Murtadha M., Schnell M., Eisenlohr L.C., Hooper J., Flomenberg P. Human T-cell responses to vaccinia virus envelope proteins. J. Virol. 2006, 80(20):10010-10020.
91. Terajima M., Cruz J., Raines G., Kilpatrick E.D., Kennedy J.S., Rothman A.L., Ennis F.A. Quantitation of CD8+ T cell responses to newly identified HLA-A *0201-restricted T cell epitopes conserved among vaccinia and variola (smallpox) viruses. J. Exp. Med. 2003, 197(7):927-932.
92. Terajima M., Orphin L., Leporati A.M., Pazoles P., Cruz J., Rothman A.L., Ennis F.A. Vaccinia virus-specific CD8(+) T-cell responses target a group of epitopes without a strong immunodominance hierarchy in humans. Hum. Immunol. 2008, 69(12):815-825.
93. Tong J.C., Tan T.W., Ranganathan S. Methods and protocols for prediction of immunogenic epitopes. Brief. Bioinform. 2007, 8(2):96-108.
94. Tscharke D.C., Karupiah G., Zhou J., Palmore T., Irvine K.R., Haeryfar S.M., Williams S., Sidney J., Sette A., Bennink J.R., Yewdell J.W. Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 2005, 201(1):95-104.
95. Tscharke D.C., Woo W.P., Sakala I.G., Sidney J., Sette A., Moss D.J., Bennink J.R., Karupiah G., Yewdell J.W. Poxvirus CD8+ T-cell determinants and cross-reactivity in BALB/c mice. J. Virol. 2006, 80(13):6318-6323.
96. Umeshappa C.S., Huang H., Xie Y., Wei Y., Mulligan S.J., Deng Y., Xiang J. CD4+ Th-APC with acquired peptide/MHC class I and II complexes stimulate type 1 helper CD4+ and central memory CD8+ T cell responses. J. Immunol. 2009, 182(1):193-206.
97. Urbani S., Amadei B., Fisicaro P., Pilli M., Missale G., Bertoletti A., Ferrari C. Heterologous T cell immunity in severe hepatitis C virus infection. J. Exp. Med. 2005, 201(5):675-680.
98. Walsh S.R., Gillis J., Peters B., Mothe B.R., Sidney J., Sette A., Johnson R.P. Diverse recognition of conserved orthopoxvirus CD8+ T cell epitopes in vaccinated rhesus macaques. Vaccine 2009, 27(36):4990-5000.
99. Wang M., Tang S.T., Lund O., Dziegiel M.H., Buus S., Claesson M.H. High-affinity human leucocyte antigen class I binding variola-derived peptides induce CD4+ T cell responses more than 30years post-vaccinia virus vaccination. Clin. Exp. Immunol. 2009, 155(3):441-446.
100. Wolffe E.J., Vijaya S., Moss B. A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies. Virology 1995, 211(1):53-63.