Long-term immunity against actual poxviral HLA ligands as identified by differential stable isotope labeling

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 6371-6383

  Meyer, Verena S ^a   Kastenmuller, Wolfgang ^b   Gasteiger, Georg ^b,c   Franz Wachtel, Mirita ^a   Lamkemeyer, Tobias ^a   Rammensee, Hans Georg ^a   Stevanovic, Stefan ^a   Sigurdardottir, Dagmar ^a   Drexler, Ingo ^b,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; HLA B ANTIGEN; SMALLPOX VACCINE; VIRUS PROTEIN; HLA A*0201 ANTIGEN; HLA ANTIGEN; HLA ANTIGEN CLASS 1; HLA B*0702; HLA-A*0201 ANTIGEN; HLA-B*0702; LIGAND; ONCOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DONOR; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HLA SYSTEM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNE RESPONSE; IMMUNITY; IMMUNOGENICITY; ISOTOPE LABELING; LETHALITY; LIFE CYCLE; MASS SPECTROMETRY; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RELIABILITY; ANTIGEN PRESENTATION; CELL LINE; CELL STRAIN K 562; COMPARATIVE STUDY; CYTOTOXIC T LYMPHOCYTE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; METHODOLOGY; PHYSIOLOGY; VACCINIA; VACCINIA VIRUS; VIROLOGY; VIRUS LATENCY;

ANTIGEN PRESENTATION; CELL LINE, TRANSFORMED; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HLA-A ANTIGENS; HLA-B ANTIGENS; HUMANS; IMMUNOLOGIC MEMORY; ISOTOPE LABELING; K562 CELLS; LIGANDS; ONCOGENE PROTEINS, VIRAL; T-LYMPHOCYTES, CYTOTOXIC; VACCINIA; VACCINIA VIRUS; VIRAL PROTEINS; VIRUS LATENCY;

EID: 58749110153     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.6371     Document Type: Article

References (64)

1. 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.
2. Fulginiti, V. A., A. Papier, J. M. Lane, J. M. Neff, and D. A. Henderson. 2003. Smallpox vaccination: a review. II. Adverse events. Clin. Infect. Dis. 37: 251-271. (Pubitemid 36930357)
3. Redfield, R. R., D. C. Wright, W. D. James, T. S. Jones, C. Brown, and D. S. Burke. 1987. Disseminated vaccinia in a military recruit with human immunodeficiency virus (HIV) disease. N. Engl. J. Med. 316: 673-676.
4. Fenner, F. 1989. Risks and benefits of vaccinia vaccine use in the worldwide smallpox eradication campaign. Res. Virol. 140: 465-466, 487-491.
5. Mayr, A. 2003. Smallpox vaccination and bioterrorism with pox viruses. Comp. Immunol. Microbiol. Infect. Dis. 26: 423-430. (Pubitemid 37168477)
6. Rimoin, A. W., N. Kisalu, B. Kebela-Ilunga, T. Mukaba, L. L. Wright, P. Formenty, N. D. Wolfe, R. L. Shongo, F. Tshioko, E. Okitolonda, et al. 2007. Endemic human monkeypox, Democratic Republic of Congo, 2001-2004. Emerg. Infect. Dis. 13: 934-937. (Pubitemid 46890148)
7. Vollmar, J., N. Arndtz, K. M. Eckl, T. Thomsen, B. Petzold, L. Mateo, B. Schlereth, A. Handley, L. King, V. Hulsemann, et al. 2006. Safety and immunogenicity of IMVAMUNE, a promising candidate as a third generation smallpox vaccine. Vaccine 24: 2065-2070. (Pubitemid 43255148)
8. + T cell responses. J. Exp. Med. 204: 1405-1416.
9. Davies, D. H., L. S. Wyatt, F. K. Newman, P. L. Earl, S. Chun, J. E. Hernandez, D. M. Molina, S. Hirst, B. Moss, S. E. Frey, and P. L. Felgner. 2008. 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. 82: 652-663.
10. Kennedy, R., and G. A. Poland. 2007. T-cell epitope discovery for variola and vaccinia viruses. Rev. Med. Virol. 17: 93-113. (Pubitemid 46480594)
11. Naz, R. K., and P. Dabir. 2007. Peptide vaccines against cancer, infectious diseases, and conception. Front. Biosci. 12: 1833-1844.
12. Drexler, I., C. Staib, and G. Sutter. 2004. Modified vaccinia virus Ankara as antigen delivery system: how can we best use its potential? Curr. Opin. Biotechnol. 15: 506-512. (Pubitemid 39551002)
13. 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. (Pubitemid 36078055)
14. + 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.
15. + T-cell peptide epitope of vaccinia and variola viruses. J. Virol. 78: 7052-7060.
16. 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, HLAA* 1101, and HLA-B*0702 transgenic mice recognize numerous poxvirus determinants from a wide variety of viral gene products. J. Immunol. 175: 5504-5515. (Pubitemid 41456438)
17. 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. (Pubitemid 41377689)
18. 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.
19. 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. (Pubitemid 41713454)
20. + cytotoxic T lymphocyte responses to a novel epitope in vaccinia virus that is conserved among orthopox viruses. J. Infect. Dis. 194: 168-175.
21. + 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.
22. Meyer, R. G., C. Graf, C. M. Britten, C. Huber, and T. Wolfel. 2007. Rapid identification of an HLA-B*1501-restricted vaccinia peptide antigen. Vaccine 25: 4715-4722.
23. + CTL epitopes with distinct functional profiles. J. Immunol. 174: 2212-2219.
24. + T cell determinants to enable rational design and characterization of smallpox vaccines. J. Exp. Med. 201: 95-104.
25. +)-cell responses to vaccinia virus. Nat. Biotechnol. 24: 817-819.
26. + T-cell determinants and cross-reactivity in BALB/c mice. J. Virol. 80: 6318-6323.
27. Oseroff, C., B. Peters, V. Pasquetto, M. Moutaftsi, J. Sidney, V. Panchanathan, D. C. Tscharke, B. Maillere, H. Grey, and A. Sette. 2008. Dissociation between epitope hierarchy and immunoprevalence in CD8 responses to vaccinia virus Western reserve. J. Immunol. 180: 7193-7202.
28. Gasteiger, G., W. Kastenmuller, R. Ljapoci, G. Sutter, and I. Drexler. 2007. Crosspriming of cytotoxic T-cells dictates antigen requisites for MVA vector vaccines. J. Virol. 81: 11925-11936.
29. + T cells shapes the immunodominance hierarchy during boost vaccination. J. Exp. Med. 204: 2187-2198.
30. Yewdell, J. W. 2005. The seven dirty little secrets of major histocompatibility complex class I antigen processing. Immunol. Rev. 207: 8-18.
31. Johnson, K. L., I. G. Ovsyannikova, B. J. Madden, G. A. Poland, and D. C. Muddiman. 2005. 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. 16: 1812-1817.
32. Planz, O., T. Dumrese, S. Hulpusch, M. Schirle, S. Stevanovic, and L. Stitz. 2001. A naturally processed rat major histocompatibility complex class I-associated viral peptide as target structure of borna disease virus-specific CD8+ T cells. J. Biol. Chem. 276: 13689-13694. (Pubitemid 37391741)
33. Van Els, C. A., C. A. Herberts, E. van der Heeft, M. C. Poelen, J. A. van Gaans-van den Brink, A. van der Kooi, P. Hoogerhout, G. Jan ten Hove, H. D. Meiring, and A. P. de Jong. 2000. A single naturally processed measles virus peptide fully dominates the HLA-A*0201-associated peptide display and is mutated at its anchor position in persistent viral strains. Eur. J. Immunol. 30: 1172-1181.
34. + T lymphocytes. J. Immunol. 174: 5636-5643.
35. Meiring, H. D., E. C. Soethout, M. C. Poelen, D. Mooibroek, R. Hoogerbrugge, H. Timmermans, C. J. Boog, A. J. Heck, A. P. de Jong, and C. A. van Els. 2006. Stable isotope tagging of epitopes: a highly selective strategy for the identification of major histocompatibility complex class I-associated peptides induced upon viral infection. Mol. Cell. Proteomics 5: 902-913.
36. Lemmel, C., S. Weik, U. Eberle, J. Dengjel, T. Kratt, H. D. Becker, H. G. Rammensee, and S. Stevanovic. 2004. Differential quantitative analysis of MHC ligands by mass spectrometry using stable isotope labeling. Nat. Biotechnol. 22: 450-454. (Pubitemid 38451377)
37. Weinzierl, A. O., C. Lemmel, O. Schoor, M. Muller, T. Kruger, D. Wernet, J. Hennenlotter, A. Stenzl, K. Klingel, H. G. Rammensee, and S. Stevanovic. 2007. Distorted relation between mRNA copy number and corresponding major histocompatibility complex ligand density on the cell surface. Mol. Cell. Proteomics 6: 102-113.
38. Flad, T., L. Mueller, H. Dihazi, V. Grigorova, R. Bogumil, A. Beck, C. Thedieck, G. A. Mueller, H. Kalbacher, and C. A. Mueller. 2006. T cell epitope definition by differential mass spectrometry: identification of a novel, immunogenic HLA-B8 ligand directly from renal cancer tissue. Proteomics 6: 364-374. (Pubitemid 43142959)
39. Lozzio, C. B., and B. B. Lozzio. 1975. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45: 321-334.
40. + T lymphocytes in IFN-γ ELISPOT assays. J. Immunol. Methods 259: 95-110.
41. Rebai, N., and B. Malissen. 1983. Structural and genetic analyses of HLA class I molecules using monoclonal xenoantibodies. Tissue Antigens 22: 107-117.
42. Barnstable, C. J., W. F. Bodmer, G. Brown, G. Galfre, C. Milstein, A. F. Williams, and A. Ziegler. 1978. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens: new tools for genetic analysis. Cell 14: 9-20.
43. Kastenmuller, W., I. Drexler, H. Ludwig, V. Erfle, C. Peschel, H. Bernhard, and G. Sutter. 2006. Infection of human dendritic cells with recombinant vaccinia virus MVA reveals general persistence of viral early transcription but distinct maturation-dependent cytopathogenicity. Virology 350: 276-288. (Pubitemid 43928113)
44. Schirle, M., W. Keilholz, B. Weber, C. Gouttefangeas, T. Dumrese, H. D. Becker, S. Stevanovic, and H. G. Rammensee. 2000. Identification of tumor-associated MHC class I ligands by a novel T cell-independent approach. Eur. J. Immunol. 30: 2216-2225. (Pubitemid 30655761)
45. Perkins, D. N., D. J. Pappin, D. M. Creasy, and J. S. Cottrell. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
46. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
47. Resch, A., S. Leicht, M. Saric, L. Pasztor, A. Jakob, F. Gotz, and A. Nordheim. 2006. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling. Proteomics 6: 1867-1877.
48. Blum, H., H. Beier, and H. J. Gross. 1987. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8: 93-99.
49. Falk, K., O. Rotzschke, K. Deres, J. Metzger, G. Jung, and H. G. Rammensee. 1991. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J. Exp. Med. 174: 425-434.
50. Engelhard, V. H. 2007. The contributions of mass spectrometry to understanding of immune recognition by T lymphocytes. Int. J. Mass Spectrom. 259: 32-39.
51. Assarsson, E., J. A. Greenbaum, M. Sundstrom, L. Schaffer, J. A. Hammond, V. Pasquetto, C. Oseroff, R. C. Hendrickson, E. J. Lefkowitz, D. C. Tscharke, et al. 2008. Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc. Natl. Acad. Sci. USA 105: 2140-2145.
52. + T-lymphocyte immune responses to human cytomegalovirus pp65 in persons sharing HLA-A*02 and HLA-B*07 alleles. Hum. Immunol. 64: 440-452.
53. + T-cell responses against Epstein-Barr virus. Scand. J. Immunol. 55: 189-195.
54. Boon, A. C., G. de Mutsert, Y. M. Graus, R. A. Fouchier, K. Sintnicolaas, A. D. Osterhaus, and G. F. Rimmelzwaan. 2002. The magnitude and specificity of influenza A virus-specific cytotoxic T-lymphocyte responses in humans is related to HLA-A and -B phenotype. J. Virol. 76: 582-590.
55. Learned, L. A., M. G. Reynolds, D. W. Wassa, Y. Li, V. A. Olson, K. Karem, L. L. Stempora, Z. H. Braden, R. Kline, A. Likos, et al. 2005. Extended inter-human transmission of monkeypox in a hospital community in the Republic of the Congo, 2003. Am. J. Trop. Med. Hyg. 73: 428-434.
56. Alcami, A., and G. L. Smith. 1992. A soluble receptor for interleukin-1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 71: 153-167.
57. Zhang, W. H., D. Wilcock, and G. L. Smith. 2000. Vaccinia virus F12L protein is required for actin tail formation, normal plaque size, and virulence. J. Virol. 74: 11654-11662.
58. Alcami, A., J. A. Symons, and G. L. Smith. 2000. The vaccinia virus soluble α/β interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J. Virol. 74: 11230-11239. (Pubitemid 32223991)
59. Murcia-Nicolas, A., G. Bolbach, J. C. Blais, and G. Beaud. 1999. Identification by mass spectroscopy of three major early proteins associated with virosomes in vaccinia virus-infected cells. Virus Res. 59: 1-12. (Pubitemid 29069049)
60. Amegadzie, B. Y., B. Y. Ahn, and B. Moss. 1992. Characterization of a 7-kilodalton subunit of vaccinia virus DNA-dependent RNA polymerase with structural similarities to the smallest subunit of eukaryotic RNA polymerase II. J. Virol. 66: 3003-3010.
61. Condit, R. C. 2007. Vaccinia, Inc.: probing the functional substructure of poxviral replication factories. Cell Host Microbe 2: 205-207.
62. Katsafanas, G. C., and B. Moss. 2007. Colocalization of transcription and translation within cytoplasmic poxvirus factories coordinates viral expression and subjugates host functions. Cell Host Microbe 2: 221-228.
63. Chahroudi, A., D. A. Garber, P. Reeves, L. Liu, D. Kalman, and M. B. Feinberg. 2006. Differences and similarities in viral life cycle progression and host cell physiology after infection of human dendritic cells with modified vaccinia virus Ankara and vaccinia virus. J. Virol. 80: 8469-8481. (Pubitemid 44384859)
64. Kratzer, R., C. Eckerskorn, M. Karas, and F. Lottspeich. 1998. Suppression effects in enzymatic peptide ladder sequencing using ultraviolet-matrix assisted laser desorption/ionization-mass spectrometry. Electrophoresis 19: 1910-1919. (Pubitemid 28392236)