Cytotoxic CD8+ T Cells Recognize EBV Antigen but Poorly Kill Autologous EBV-Infected B Lymphoblasts: Immunodominance Is Elicited by a Peptide Epitope That Is Presented at Low Levels in Vitro

Journal of Immunology

Volumn 159, Issue 4, 1997, Pages 1844-1852

  Shi, Yan ^a,b   Smith, Kelly D ^a,b,d   Kurilla, Michael G ^c   Lutz, Charles T ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; EPSTEIN BARR VIRUS ANTIGEN;

AMINO ACID SEQUENCE; ARTICLE; B LYMPHOCYTE; CELL LINE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; EPSTEIN BARR VIRUS; IMMUNOLOGY; MOLECULAR GENETICS; VIROLOGY;

AMINO ACID SEQUENCE; B-LYMPHOCYTES; CELL LINE; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HERPESVIRUS 4, HUMAN; MOLECULAR SEQUENCE DATA; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0031571277     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Miller, G. 1990. Epstein-Barr virus: biology, pathogenesis, and medical aspects. In B. Fields and D. Knipe, eds. Virology, 2nd Ed. Raven Press Ltd., New York, pp. 1921-1958.
2. Pallesen, G., S. J. Hamilton-Dutoit, M. Rowe, and L. S. Young. 1991. Expression of Epstein-Barr virus latent gene products in tumour cells of Hodgkin's disease. Lancet 337:320.
3. Penn, I. 1990. Cancers complicating organ transplantation. N. Engl. J. Med. 323: 1767.
4. Neri, A., F. Barriga, G. Inghirami, D. M. Knowles, J. Neequaye, I. T. Magrath, and R. Dalla-Favera. 1991. Epstein-Barr virus infection precedes clonal expansion in Burkitt's and acquired immunodeficiency syndrome-associated lymphoma. Blood 77:1092.
5. Garnier, J. L., F. Berger, H. Betuel, M. Vuillaume, C. Chapuis-Cellier, N. Blanc, J. L. Faure, J. M. Dubernard, G. Lenoir, and J. L. Touraine. 1989. Epstein-Barr virus associated lymphoproliferative diseases (B cell lymphoma) after transplantation. Nephrol. Dialysis Transplant. 4:818.
6. Rickinson, A. B., S. P. Lee, and N. M. Steven. 1996. Cytotoxic T lymphocyte response to Epstein-Barr virus. Curr. Opin. Immunol. 8:492.
7. York, L. J., and L. F. Qualtiere. 1990. Cyclosporin abrogates virus-specific T-cell control of EBV-induced B-cell lymphoproliferation. Viral Immunol. 3:127.
8. Swinnen, L. J., M. R. Costanzo-Nordin, S. G. Fisher, E. J. O'Sullivan, M. R. Johnson, A. L. Heroux, G. J. Dizikes, R. Pifarre, and R. I. Fisher. 1990. Increased incidence of lymphoproliferative disorder after immunosuppression with the monoclonal antibody OKT3 in cardiac-transplant recipients. N. Engl. J. Med. 323:1723.
9. Rooney, C. M., C. A. Smith, C. Y. Ng, S. Loftin, C. Li, R. A. Krance, M. K. Brenner, and H. E. Heslop. 1995. Use of gene-modified virus-specific T lymphocytes to control Epstein-Barr-virus-related lymphoproliferation. Lancet 345:9.
10. DiMaio, J. M., P. Van Trigt, J. W. Gaynor, R. D. Davis, E. Coveney, B. M. Clary, and H. K. Lyerly. 1995. Generation of tumor-specific T lymphocytes for the treatment of posttransplant lymphoma. Circulation 92:202.
11. Hill, A. B., S. P. Lee, J. S. Haurum, N. Murray, Q. Y. Yao, M. Rowe, N. Signoret, A. B. Rickinson, and A. J. McMichael. 1995. Class I major histocompatibility complex-restricted cytotoxic T lymphocytes specific for Epstein-Barr virus (EBV)-transformed B lymphoblastoid cell lines against which they were raised. J. Exp. Med. 181:2221.
12. + memory cells. J. Immunol. 134:2287.
13. Rickinson, A. B., R. J. Murray, J. Brooks, H. Griffin, D. J. Moss, and M. G. Masucci. 1992. T cell recognition of Epstein-Barr virus associated lymphomas. Cancer Surv. 13:53.
14. Khanna, R., S. R. Burrows, M. G. Kurilla, C. A. Jacob, I. S. Misko, T. B. Sculley, E. Kieff, and D. J. Moss. 1992. Localization of Epstein-Barr virus cytotoxic T cell epitopes using recombinant vaccinia: implications for vaccine development. J. Exp. Med. 176:169.
15. Murray, R. J., M. G. Kurilla, J. M. Brooks, W. A. Thomas, M. Rowe, E. Kieff, and A. B. Rickinson. 1992. Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies. J. Exp. Med. 176:157.
16. Murray, R. J., M. G. Kurilla, H. M. Griffin, J. M. Brooks, M. Mackett, J. R. Arrand, M. Rowe, S. R. Burrows, D. J. Moss and E. Kieff, and A. B. Rickinson. 1990. Human cytotoxic T-cell responses against Epstein-Barr virus nuclear antigens demonstrated by using recombinant vaccinia viruses. Proc. Natl. Acad. Sci. USA 87:2906.
17. Murray, R. J., D. Wang, L. S. Young, F. Wang, M. Rowe, E. Kieff, and A. B. Rickinson. 1988. Epstein-Barr virus-specific cytotoxic T-cell recognition of transfectants expressing the virus-coded latent membrane protein LMP. J. Virol. 62:3747.
18. Levitskaya, J., M. Coram, V. Levitsky, S. Imreh, P. M. Steigerwald-Mullen, G. Klein, M. G. Kurilla, and M. G. Masucci. 1995. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375:685.
19. Bejarano, M. T., S. Thorsteinsdottir, J. P. Andersson, U. G. Andersson, M. G. Masucci, R. Szigeti, E. Klein, and G. Klein. 1987. Defective cell-mediated response to EBV-transformed B cells in a healthy individual with regular EBV antibody titers. Int. J. Cancer 40:149.
20. Kageyama, S., T. J. Tsomides, Y. Sykulev, and H. N. Eisen. 1995. Variations in the number of peptide-MHC class I complexes required to activate cytotoxic T cell responses. J. Immunol. 154:567.
21. Kurago, Z. B., K. D. Smith, and C. T. Lutz. 1995. NK cell recognition of MHC class I: NK cells are sensitive to peptide-binding groove and surface alpha-helical mutations that affect T cells. J. Immunol. 154:2631.
22. Khanna, R., C. A. Jacob, S. R. Burrows, M. G. Kurilla, E. Kieff, I. S. Misko, T. B. Sculley, and D. J. Moss. 1991. Expression of Epstein-Barr virus nuclear antigen in anti-IgM-stimulated B cells following recombinant vaccinia infection and their recognition by human cytotoxic T cells. Immunology 74:504.
23. Chakrabati, S., K. Brechling, and B. Moss. 1985. Vaccinia virus expression vector: coexpression of β-galactosidase provides visual screening of recombinant virus plaques. Mol. Cell. Biol. 5:3403.
24. Smith, K. D., E. Huczko, V. H. Engelhard, Y. Y. Li, and C. T. Lutz. 1997. Alloreactive cytotoxic T lymphocytes focus on specific MHC-bound peptides. Transplantation. In press.
25. Misko, I. S.; T. B. Sculley, C. Schmidt, D. J. Moss, T. Soszynski, and K. Burman. 1991. Composite response of naive T cells to stimulation with the autologous lymphoblastoid cell line is mediated by CD4 cytotoxic T cell clones and includes an Epstein-Barr virus-specific component. Cell. Immunol. 132:295.
26. Gavioli, R., M. G. Kurilla, P. O. de Campos-Lima, L. E. Wallace, R. Dolcetti, R. J. Murray, A. B. Rickinson, and M. G. Masucci. 1993. Multiple HLA A11-restricted cytotoxic T-lymphocyte epitopes of different immunogenicities in the Epstein-Barr virus-encoded nuclear antigen 4. J. Virol. 67:1572.
27. Zemmour, J., and P. Parham. 1993. HLA class I nucleotide sequences. Immunogenetics 37:239.
28. Falk, K., O. Rotzschke, B. Grahovac, D. Schendel, S. Stevanovic, G. Jung, and H. G. Rammensee. 1993. Peptide motifs of HLA-B35 and -B37 molecules [published erratum appears in Immunogenetics 1994;39(5):379]. Immunogenetics 38: 161.
29. Sample, J., L. Young, B. Martin, T. Chatman, E. Kieff, A. Rickinson, and E. Kieff. 1990. Epstein-Barr virus types 1 and 2 differ in their EBNA-3A, EBNA-3B, and EBNA-3C genes. J. Virol. 64:4084.
30. Coupar, B. E. H., M. E. Andrew., G. W. Both, and D. B. Boyle. 1986. Temporal regulation of influenza hemagglutinin expression in vaccinia virus recombinants and effects on the immune response. Eur. J. Immunol. 16:1479.
31. Townsend, A., J. Bastin, K. Gould, G. Brownlee, M. Andrew, B. Coupar, D. Boyle, S. Chan, and G. Smith. 1988. Defective presentation to class I-restricted cytotoxic T lymphocytes in vaccinia-infected cells is overcome by enhanced degradation of antigen. J. Exp. Med. 168:1211.
32. Kieff, E. 1996. Epstein-Barr virus and its replication. In B. N. Fields, D. M. Knipe, and P. M. Howley, eds. Fundamental Virology, 3rd Ed. Lippincott-Raven Press, Philadelphia, pp. 1109-1162.
33. Tomkinson, B., E. Robertson, and E. Kieff. 1993. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol. 67:2014.
34. Tierney, R. J., N. Steven, L. S. Young, and A. B. Rickinson. 1994. Epstein-Barr virus latency in blood mononuclear cells: analysis of viral gene transcription during primary infection and in the carrier state. J. Virol. 68:7374.
35. Momburg, F., J. J. Neefjes, and G. J. Hammerling. 1994. Peptide selection by MHC-encoded TAP transporters. Curr. Opin. Immunol. 6:32.
36. Momburg, F., J. Roelse, J. C. Howard, G. W. Butcher, G. J. Hammerling, and J. J. Neefjes. 1994. Selectivity of MHC-encoded peptide transporters from human, mouse and rat. Nature 367:648.
37. Del Val, M., H. J. Schlicht, T. Ruppert, M. J. Reddehase, and U. H. Koszinowski. 1991. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell 66: 1145.
38. Eisenlohr, L. C., J. W. Yewdell, and J. R. Bennink. 1992. Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes. J. Exp. Med. 175:481.
39. Niedermann, G., S. Butz, H. G. Ihlenfeldt, R. Grimm, M. Lucchiari, H. Hoschutzky, G. Jung, B. Maier, and K. Eichmann. 1995. Contribution of proteasome-mediated proteolysis to the hierarchy of epitopes presented by major histocompatibility complex class I molecules. Immunity 2:289.
40. Kerr, B. M., N. Kienzle, J. M. Burrows, S. Corss, S. L. Silins, M. Buck, E. M. Benson, B. Coupar, D. J. Moss, and T. B. Sculley. 1996. Identification of type B-specific and cross-reactive cytotoxic T-lymphocyte responses to Epstein-Barr virus. J. Virol. 70:8858.
41. Valitutti, S., S. Mueller, M. Dessing, and A. Lanzavecchia. 1996. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J. Exp. Med. 183:1917.
42. Tosato, G., and R. M. Blaese. 1985. Epstein-Barr virus infection and immunoregulation in man. Adv. Immunol. 37:99.
43. Freedman, A. S., G. Freeman, J. C. Horowitz, J. Daley, and L. M. Nadler. 1987. B7, a B-cell-restricted antigen that identifies preactivated B cells. J. Immunol. 139:3260.
44. Freeman, G. J., A. S. Freedman, J. M. Segil, G. Lee, J. F. Whitman, and L. M. Nadler. 1989. B7, a new member of the Ig superfamily with unique expression on activated and neoplastic B cells. J. Immunol. 143:2714.
45. Guerder, S., S. R. Carding, and R. A. Flavell. 1995. B7 costimulation is necessary for the activation of the lytic function in cytotoxic T lymphocyte precursors. J. Immunol. 155:5167.
46. Viola, A., and A. Lanzavecchia. 1996. T cell activation determined by T cell receptor number and tunable thresholds. Science 273:104.
47. Hedrick, J. A., D. Watry, C. Speiser, P. O'Donnell, J. D. Lambris, and C. D. Tsoukas. 1992. Interaction between Epstein-Barr virus and a T cell line (HSB-2) via a receptor phenotypically distinct from complement receptor type 2. Eur. J. Immunol. 22:1123.
48. Koizumi, S., X. K. Zhang, S. Imai, M. Sugiura, N. Usui, and T. Osato. 1992. Infection of the HTLV-I-harbouring T-lymphoblastoid line MT-2 by Epstein-Barr virus. Virology 188:859.
49. Sinha, S. K., S. C. Todd, J. A. Hedrick, C. L. Speiser, J. D. Lambris, and C. D. Tsoukas. 1993. Characterization of the EBV/C3d receptor on the human Jurkat T cell line: evidence for a novel transcript. J. Immunol. 150:5311.
50. Qu, L., and D. T. Rowe. 1992. Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes. J. Virol. 66:3715.
51. Miyashita, E. M., B. Yang, K. M. Lam, D. H. Crawford, D. A. Thorley-Lawson. 1995. A novel form of Epstein-Barr virus latency in normal B cells in vivo. Cell 80:593.
52. Guidotti, L. G., T. Ishikawa, M. V. Hobbs, B. Mutzke, R. Schreiber, and F. V. Chisari. 1996. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 4:25.
53. Ando, K., T. Moriyama, L. G. Guidotti, S. Wirth, R. D. Schreiber, H. J. Schlicht, S. N. Huang, and F. V. Chisari. 1993. Mechanisms of class I restricted immunopathology: a transgenic mouse model of fulminant hepatitis. J. Exp. Med. 18: 1541.
54. Gerth, U. C., P. A. Moss, J. I. Bell, and A. J. McMichael. 1995. T-cell receptor usage of major histocompatibility complex class I restricted peptide-specific T-lymphocytes. Ann. NY Acad. Sci. 756:12.
55. Nowak, M. A., R. M. May, R. E. Phillips, S. Rowland-Jones, D. G. Lalloo, S. McAdam, P. Klenerman, B. Koppe, K. Sigmund, C. R. Bangham, and A. J. McMichael. 1995. Antigenic oscillations and shifting immunodominance in HIV-1 infections. Nature 375:606.
56. Gavioli, R., P. O. De Campos-Lima, M. G. Kurilla, E. Kieff, G. Klein, and M. G. Masucci. 1992. Recognition of the Epstein-Barr virus-encoded nuclear antigens EBNA-4 and EBNA-6by HLA-A11-restricted cytotoxic T lymphocytes: implications for down-regulation of HLA-A11 in Burkitt lymphoma. Proc. Natl. Acad. Sci. USA 89:5862.
57. de Campos-Lima, P. O., V. Levitsky, J. Brooks, S. P. Lee, L. F. Hu, A. B. Rickinson, and M. G. Masucci. 1994. T cell responses and virus evolution: loss of HLA A11-restricted CTL epitopes in Epstein-Barr virus isolates from highly A11-positive populations by selective mutation of anchor residues. J. Exp. Med. 179:1297.