Human CD8+ T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing

Immunity

Volumn 7, Issue 6, 1997, Pages 791-802

  Blake, Neil ^a   Lee, Steven ^a   Redchenko, Irina ^a   Thomas, Wendy ^a   Steven, Neil ^a   Leese, Alison ^a   Steigerwald Mullen, Patty ^b   Kurilla, Michael G ^b   Frappier, Lori ^c   Rickinson, Alan ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; VIRUS ANTIGEN;

ANTIGEN PRESENTATION; ARTICLE; BACULOVIRUS; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EPSTEIN BARR VIRUS; HLA SYSTEM; HUMAN; HUMAN CELL; LYMPHOCYTE CLONE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; VIRUS REPLICATION;

EID: 0031414705     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80397-0     Document Type: Article

References (52)

1. Ahn, K., Angulo, A, Ghazal, P., Peterson, P.A., Yang, Y., and Früh, K. (1996). Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. USA 93, 10990-10995.
2. Ahn, K., Gruhler, A., Galocha, B., Jones, T.R., Wiertz, E.J.H.J., Ploegh, H.L., Peterson, P.A., Yang, Y., and Früh, K. (1997). The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6, 613-621.
3. Baer, R., Bankier, A.T., Biggin, M.D., Deininger, P.L., Farrell, P.J., Gibson, T.G., Hatfull, G., Hudson, G.S., Satchwell, S.C., Séguin, C., et al. (1984). DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310, 207-211.
4. Ball, L.A. (1987). High-frequency homologous recombination in vaccinia virus DNA. J. Virol. 61, 1788-1795.
5. Burrows, S.R., Rodda, S.J., Suhrbier, A., Geysen, H.M., and Moss, D.J. (1992a). The specificity of recognition of acytotoxic T lymphocyte epitope. Eur. J. Immunol. 22, 191-195.
6. Burrows, S.R., Suhrbier, A., Khanna, R., and Moss, D.J. (1992b). Rapid visual assay of cytotoxic T-cell specificity utilizing synthetic peptide induced T-cell-T-cell killing. Immunology 76, 174-175.
7. Chen, F., Zou, J.Z., di Renzo, L., Winberg, G., Hu, L.F., Klein, E., Klein, G., and Ernberg, I. (1995). A subpopulation of latently EBV-infected normal B cells resemble Burkitt lymphoma (BL) cell in expressing EBNA1 but not EBNA2 or LMP1. J. Virol. 69, 3752-3758.
8. Falk, K., Gratama, J.W., Rowe, M., Zou, J.Z., Khanim, F., Young, L.S., Oosterveer, M.A.P., and Ernberg, I. (1995). The role of repetitive DNA sequences in the size variation of Epstein-Barr virus (EBV) nuclear antigens and the identification of different EBV isolates using RFLP and PCR analysis. J. Gen. Virol. 76, 779-790.
9. Floettmann, J.E., Ward, K., Rickinson, A.B., and Rowe, M. (1996). Cytostatic effect of Epstein-Barr virus latent membrane protein-1 analyzed using tetracycline-regulated expression in B cell lines. Virology 223, 29-40.
10. Früh, K., Ahn, A., Djaballah, H., Sempé, P., van Endert, P.M., Tampé, R., Peterson, P.A., and Yang, Y. (1995). A viral inhibitor of peptide transporters for antigen presentation. Nature 375, 415-418.
11. Gavioli, R., de Campos-Lima, P.O., Kurilla, M.G., Kieff, E., Klein, G., and Masucci, M.G. (1992). Recognition of the Epstein-Barr virus-encoded nuclear antigen EBNA4 and EBNA6 by HLA-A11-restricted cytotoxic T lymphocytes: implications for down-regulation of HLA-A11 in Burkitt lymphoma. Proc. Natl. Acad. Sci. USA 89, 5862-5866.
12. Gavioli, R., Kurilla, M.G., de Campos-Lima, P.O., Wallace, L.E., Dolcetti, R., Murray, R.J., Rickinson, A.B., and Masucci, M.G. (1993). Multiple HLA A11-restricted cytotoxic T-lymphocyte epitopes of different immunogenicities in the Epstein-Barr virus-encoded nuclear antigen 4. J. Virol. 67, 1572-1578.
13. Gilbert, M.J., Riddell, S.R., Plachter, B., and Greenberg, P.D. (1996). Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature 383, 720-722.
14. Goldsmith, K., Bendell, L., and Frappier, L. (1993). Identification of EBNA1 amino acid sequences required for the interaction of the functional elements of the Epstein-Barr virus latent origin of DNA replication. J. Virol. 67, 3418-3426.
15. Grässer, F.A., Murray, P.G., Kremmer, E., Klein, K., Remberger, K., Feiden, W., Reynolds, G., Niedobitek, G., Young, L.S., and Mueller-Lantzsch, N. (1994). Monoclonal antibodies directed against the Epstein-Barr virus-encoded nuclear antigen 1 (EBNA1): immunohistologic detection of EBNA1 in the mailignant cells of Hodgkin's disease. Blood 84, 3792-3798.
16. Grunhaus, A., and Horwitz, M.S. (1992). Adenoviruses as cloning vectors. Semin. Virol. 3, 237-252.
17. Hengel, H., Koopmann, J-O., Flohr, T., Muranyi, W., Goulmy, E., Hämmerling, G.J., Koszinowski, U.H., and Momburg, F. (1997). A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6, 623-632.
18. Henle, W., Henle, G., Anderson, J., Ernberg, I., Klein, G., Horwitz, C. A., Marklund, G., Rymo, L., Wellinder, C., and Straus, S.E. (1987). Antibody responses to Epstein-Barr virus-determined nuclear antigen (EBNA)-1 and EBNA 2 in acute and chronic Epstein-Barr virus infection. Proc. Natl. Acad. Sci. USA 84, 570-574.
19. Hennessy, K., and Kieff, E. (1983). One of two Epstein-Barr virus nuclear antigens contains a glycine-alanine copolymer domain. Proc. Natl. Acad. Sci. USA 80, 5665-5669.
20. Hill, A., Jugovic, P., York, I., Russ, G., Bennink, J., Yewdell, J., Ploegh, H., and Johnson, D. (1995). Herpes simplex virus turns off the TAP to evade host immunity. Nature 375, 411-415.
21. Jones, T.R., Wiertz, E.J.H.J., Sun, L., Fish, K.N., Nelson, J.A., and Ploegh, H.L. (1996). Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. USA 93, 11327-11333.
22. Kay, R., and McPherson, J. (1987). Hybrid pUC vectors for the addition of new restriction enzyme sites to the ends of DNA fragments. Nucleic Acids Res. 15, 2778.
23. Khanna, R., Burrows, S.R., Kurilla., M.G., Jacob, C.A., Misko, I.S., Sculley, T.B., Kieff, E., and Moss, D.J. (1992). Localization of Epstein-Barr virus cytotoxic T cell epitopes using recombinany vaccinia: implications for vaccine development. J. Exp. Med. 176, 169-176.
24. Khanna, R., Burrows, S.R., Steigerwald-Mullen, P.M., Thomson, S.A., Kurilla., M.G., and Moss, D.J. (1995). Isolation of cytotoxic T lymphocytes from healthy seropositive individuals specific for peptide epitopes from Epstein-Barr virus nuclear antigen 1: implications for viral persistence and tumor surveillance. Virology 214, 633-637.
25. Khanna, R., Burrows, S.R., Steigerwald, P.M., Moss, D.J., Kurilla, M.G., and Cooper, L. (1997). Targeting Epstein-Barr virus (EBV) nuclear antigen 1 (EBNA1) through the class II pathway restores immune recognition by EBNA1-specific CD4+ cytotoxic T lymphocytes: An evidence for HLA DM-independant processing. Int. Immunol. 9, 1537-1543.
26. Kovacsovics-Bankowski, M., Clark, K., Benacerraf, B., and Rock, K.L. (1993). Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc. Natl. Acad. Sci. USA 90, 4924-4964.
27. Lee, S.P., Morgan, S., Skinner, J., Thomas, W.A., Jones, S.R., Sutton, J., Khanna, R., Whittle, H.C., and Rickinson, A.B. (1995). Epstein-Barr virus isolates with the major HLA B35.01-restricted cytotoxic T-lymphocyte epitope are prevalent in a highly B35.01 -positive African population. Eur. J. Immunol. 25, 102-110.
28. Lee, S.P., Tierney, R.J., Thomas, W.A., Brooks, J.M., and Rickinson, A.B. (1997). Conserved CTL epitopes within EBV latent membrane protein 2: a potential target for CTL-based tumor therapy. J. Immunol. 158, 3325-3334.
29. Levitskaya, J., Coram, M., Levitsky, V., Imreh, S., Steigerwald-Mullen, P.M., Klein, G., Kurilla., M.G., and Masucci, M. (1995). Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375, 685-688.
30. Liu, T., Zhou, A., Overall, C., Lederer, E., Ljunggren, H-G., and Jondal, M. (1995). Heat-inactivated Sendai virus can enter multiple MHC class I processing pathways and generate cytotoxic T lymphocyte responses in vivo. J. Immunol. 154, 3147-3155.
31. McGrory, W.J., Bautista, D.S., and Graham, F.G. (1988). A simple technique for the rescue of early region I mutations into infectious human adenovirus type 5. Virology 163, 614-617.
32. Murray, R.J., Kurilla., M.G., Brooks, J.M., Thomas, W.A., Rowe, M., Kieff, E., and Rickinson, A.B. (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, 157-168.
33. Norbury, C.C., Hewlett, L.J., Prescott, A., Shastri, N., and Watts, C. (1995). Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 3, 783-791.
34. Pfeifer, J.D., Wick, M.J., Roberts, R.L., Findlay, K., Normark, S.J., and Harding, C.V. (1993). Phagocytic processing of bacterial antigens for class I MHC presentation to T cells. Nature 361, 359-362.
35. Rammensee, H-G., Fride, T., and Stenvanovic, S. (1995). MHC ligands and peptide motifs: first listing. Immunogenetics 41, 178-228.
36. Rickinson, A.B., and Kieff, E. (1996). Epstein-Barr Virus. In Fields Virology, B.N. Fields, D.M. Knipe, P.M. Howley, R.M. Chanock, J.L. Melnick, T.P. Monath, B. Roizman, and S.E. Straus, eds. (Philadelphia: Lippincott-Raven Publishers), pp. 2397-2446.
37. Rickinson, A.B., and Moss, D.J. (1997). Human cytotoxic T lymphocyte responses to Epstein-Barr virus infection. Annu. Rev. Immunol. 15, 405-431.
38. Riddell, S.R., Rabin, M, Geballe, A.P., Britt, W.J., and Greenberg, P.D. (1991). Class I MHC-restricted cytotoxic T lymphocyte recognition of cells infected with human cytomegalovius does not reduire endogenous viral gene expression. J. Immunol. 146, 2795-2804.
39. Rock, K.L. (1996). A new foreign policy: MHC class I molecules monitor the outside world. Immunol. Today 17, 131-137.
40. Salter, R.D., Howell, D.N., and Cresswell, P. (1985). Genes regulation HLA class-I antigen expression in T-B lymphoblast hybrids. Immunogenetics 21, 235-246.
41. Schirmbeck, R., Melber, K., and Reimann, J. (1995). Hepatitis B virus small surface antigen particles are processed in a novel endosomal pathway for major histocompatibility complex class I-restricted epitope presentation. Eur. J. Immunol. 25, 1063-1070.
42. Steven, N.M., Leese, A.M., Annels, N.E., Lee, S.P., and Rickinson, A.B. (1996). Epitope focusing in the primary cytotoxic T cell response to Epstein-Barr virus and its relationship to T cell memory. J. Exp. Med. 184, 1801-1813.
43. Steven, N.M., Annels, N.E., Kumar, A., Leese, A.M., Kurilla, M.G., and Rickinson, A.B. (1997). Immediate early and early lytic cycle proteins are frequent targets of the Epstein-Barr virus-induced cytotoxic T cell response. J. Exp. Med. 185, 1605-1617.
44. Takiguchi, M., Kawaguchi, G., Sekimata, M., Hiraiwa, M., Kariyone, A., and Takamiya (1994). The role of the conserved residue in the pocket A and the polymorhic residue in pocket E of HLA-B35.01 in presentation of human minor histocompatibility peptides to T cells. Int. Immunol. 6, 1345-1352.
45. Tamaki, H., Beaulieu, B.L., Somasundaran, M., and Sullivan, J.L. (1995). Major histocompatibility complex class-I restricted cytotoxic T lymphocyte response to Epstein-Barr virus in children. J. Infect. Dis. 172, 739-746.
46. Tierney, R.J., Steven, N., Young, L.S., and Rickinson, A.B. (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, 7374-7385.
47. Tigges, M.A., Koelle, D., Hartog, K., Sekulovich, R.E., Corey, L., and Burke, R.L. (1992). Human CD8+ herpes simplex virus-specific cytotoxic T-lymphocyte clones recognize diverse virion protein antigens. J. Virol. 66, 1622-1634.
48. Ulmer, J.B., Donnelly, J.J., and Liu, M.A. (1994). Presentation of an exogenous antigen by major histocompatibility complex class I molecules. Eur. J. Immunol. 24, 1590-1596.
49. Wiertz, E.J.H.J., Jones, T.R., Sun, L., Bogyo, M., Geuze, H.J., and Ploegh, H.L. (1996a). The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779.
50. Wiertz, E.J.H.J., Tortorella, D., Bogyo, M., Yu, J., Mothes, W., Jones, T. R., Rapoport, T.A., and Ploegh, H.L. (1996b). Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438.
51. Wilkinson, G.W., and Akrigg, A. (1992). Constitutive and enhanced expression from the CMV major IE promoter in a defective adenovirus. Nucleic Acids Res. 20, 2233-2239.
52. York, I.A., and Rock, K.L. (1996). Antigen processing and presentation by the class I major histocompatibility complex. Annu. Rev. Immunol. 14, 369-396.