The CD8+ T-cell response to an Epstein-Barr virus-related gammaherpesvirus infecting rhesus macaques provides evidence for immune evasion by the EBNA-1 homologue

Journal of Virology

Volumn 79, Issue 20, 2005, Pages 12681-12691

  Fogg, Mark H ^a   Kaur, Amitinder ^b   Cho, Young Gyu ^a,d   Wang, Fred ^a,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c CHANNING LABORATORY   (United States)

^d The Catholic University of Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CD8 ANTIGEN; EPITOPE; EPSTEIN BARR VIRUS ANTIGEN; GAMMA INTERFERON; GLYCINE; RHESUS LYMPHOCRYPTOVIRUS EPSTEIN BARR VIRUS NUCLEAR ANTIGEN 1; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSPOT ASSAY; EPSTEIN BARR VIRUS; EVALUATION; GENUS; HERPES VIRUS; INFECTION CONTROL; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CLONE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHESUS MONKEY; VIRUS INFECTION;

ALANINE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; EPITOPES, T-LYMPHOCYTE; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; GLYCINE; HERPESVIRIDAE INFECTIONS; LYMPHOCRYPTOVIRUS; MACACA MULATTA; SPECIES SPECIFICITY; T-LYMPHOCYTES, CYTOTOXIC; TUMOR VIRUS INFECTIONS; VIRUS LATENCY;

ANIMALIA; HUMAN HERPESVIRUS 4; LYMPHOCRYPTOVIRUS; MACACA MULATTA; PRIMATES;

EID: 26444487604     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.20.12681-12691.2005     Document Type: Article

References (35)

1. Anonymous. 1996. Guide for the Care and Use of Laboratory Animals, p. 86-123. The Institute of Laboratory Animal Resources, National Research Council, Washington, D.C.
2. Bickham, K., K. Goodman, C. Paludan, S. Nikiforow, M. L. Tsang, R. M. Steinman, and C. Munz. 2003. Dendritic cells initiate immune control of Epstein-Barr virus transformation of B lymphocytes in vitro. J. Exp. Med. 198:1653-1663.
3. Blake, N., T. Haigh, G. Shaka'a. D. Croom-Carter, and A. Rickinson. 2000. The importance of exogenous antigen in priming the human CD8+ T-cell response: lessons from the EBV nuclear antigen EBNA1. J. Immunol. 165:7078-7087.
4. Blake, N., S. Lee, I. Redchenko, W. Thomas, N. Steven, A. Leese, P. Steigerwald-Mullen, M. G. Kurilla, L. Frappier, and A. Rickinson. 1997. Hum. CD8+ T-cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity 7:791-802.
5. Blake, N. W., A. Moghaddam, P. Rao, A. Kaur, R. Glickman, Y. G. Cho, A. Marchini, T. Haigh, R. P. Johnson, A. B. Rickinson, and F. Wang. 1999. Inhibition of antigen presentation by the glycine/alanine repeat domain is not conserved in simian homologues of Epstein-Barr virus nuclear antigen 1. J. Virol. 73:7381-7389.
6. Cleary, M. L., R. F. Dorfman, and J. Sklar. 1986. Failure in immunological control of the virus infection: post-transplant lymphomas, p. 163-181. In M. A. Epstein and B. G. Achong (ed.), The Epstein-Barr virus: recent advances. Heinemann Medical Books, London, England.
7. Franken, M., O. Devergne, M. Rosenzweig, B. Annis, E. Kieff, and F. Wang. 1996. Comparative analysis identities conserved tumor necrosis factor receptor-associated factor 3 binding sites in the human and simian Epstein-Barr virus oncogene LMP1. J. Virol. 70:7819-7826.
8. Fuentes-Panana, E. M., S. Swaminathan, and P. D. Ling. 1999. Transcriptional activation signals found in the Epstein-Barr virus (EBV) latency C promoter are conserved in the latency C promoter sequences from baboon and rhesus monkey EBV-like lymphocryptoviruses (cercopithicine herpesviruses 12 and 15). J. Virol. 73:826-833.
9. 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-6 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.
10. Jiang, H., Y. G. Cho, and F. Wang. 2000. Structural, functional, and genetic comparisons of Epstein-Barr virus nuclear antigen 3A, 3B, and 3C homologues encoded by the rhesus lymphocryptovirus. J. Virol. 74:5921-5932.
11. 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. 176:169-176.
12. Lee, S. P., J. M. Brooks, H. Al-Jarrah, W. A. Thomas, T. A. Haigh, G. S. Taylor, S. Humme, A. Schepers, W. Hammerschmidt, J. L. Yates, A. B. Rickinson, and N. W. Blake. 2004. CD8 T-cell recognition of endogenously expressed Epstein-Barr virus nuclear antigen 1. J. Exp. Med. 199:1409-1420.
13. 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 375:685-688.
14. Levitskaya, J., A. Sbaripo, A. Lennebiks, A. Ciechanover, and M. G. Masucci. 1997. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc. Natl. Acad. Sci. USA 94:12616-12621.
15. Mazzara, G. P., A. Destree, and A. Mahr. 1993. Generation and analysis of vaccinia virus recombinants. Methods Enzymol. 217:557-581.
16. McCann, E. M., G. L. Kelly, A. B. Rickinson, and A. I. Bell. 2001. Genetic analysis of the Epstein-Barr virus-coded leader protein EBNA-LP as a coactivator of EBNA2 function. J. Gen. Virol. 82:3067-3079.
17. Moghaddam, A., M. Rosenzweig, D. Lee-Parritz, B. Annis, R. P. Johnson, and F. Wang. 1997. An animal model for acute and persistent Epstein-Barr virus infection. Science 276:2030-2033.
18. Moss, D. J., A. B. Rickinson, and J. H. Pope. 1978. Long-term T-Cell-mediated immunity 10 Epstein-Barr virus in man. I. Complete regression of virus-induced transformation in cultures of seropositive donor leukocytes. Int. J. Cancer 22:662-668.
19. 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. 176:157-168.
20. Peng, R., A. V. Gordadze, E. M. Fuentes Panana, F. Wang, J. Zong, G. S. Hayward, J. Tan, and P. D. Ling. 2000. Sequence and functional analysis of EBNA-LP and EBNA2 proteins from nonhuman primate lymphocryptoviruses. J. Virol. 74:379-389.
21. Rahin, H., R. H. Neubauer, R. F. Hopkins, 3rd, and M. Nonoyama. 1978. Further characterization of a herpesvirus-positive orang-utan cell line and comparative aspects of in vitro transformation with lymphotropic old world primate herpesviruses. Int. J. Cancer 21:762-767.
22. Rangan, S. R., L. N. Martin, B. E. Bozelka, N. Wang, and B. J. Gormus. 1986. Epstein-Barr virus-related herpesvirus from a rhesus monkey (Macaca mulatta) with malignant lymphoma. Int. J. Cancer 38:425-432.
23. Rao, P., H. Jiang, and F. Wang. 2000. Cloning of the rhesus lymphocryptovirus viral capsid antigen and Epstein-Barr virus-encoded small RNA homologues and use in diagnosis of acute and persistent infections. J. Clin. Microbiol. 38:3219-3225.
24. Rickinson, A., and E. Kieff. 2001. Epstein-Barr virus. p. 2575-2627. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams and Wilkins, Philadelphia, Pa.
25. Rivailler, P., A. Carville, A. Kaur, P. Rao, C. Quink, J. L. Kutok, S. Westmoreland, S. Klumpp, M. Simon, J. C. Aster, and F. Wang. 2004. Experimental rhesus lymphocryptovirus infection in immunosuppressed macaques: an animal model for Epstein-Barr virus pathogenesis in the immunosuppressed host. Blood 104:1482-1489.
26. Rivailler, P., H. Jiang, Y. G. Cho, C. Quink, and F. Wang. 2002. Complete nucleotide sequence of the rhesus lymphocryptovirus: genetic validation for an Epstein-Barr virus animal model. J. Virol. 76:421-426.
27. Rivailler, P., C. Quink, and F. Wang. 1999. Strong selective pressure for evolution of an Epstein-Barr virus LMP2B homologue in the rhesus lymphocryptovirus. J. Virol. 73:8867-8872.
28. Rooney, C. M., C. A. Smith, C. Y. Ng, S. K. Loftin, J. W. Sixbey, Y. Gan, D. K. Srivastava, L. C. Bowman, R. A. Krance, M. K. Brenner, and H. E. Heslop. 1998. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients. Blood 92:1549-1555.
29. Rowe, M., D. T. Rowe, C. D. Gregory, L. S. Young, P. J. Farrell, H. Rupani, and A. B. Rickinson. 1987. Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells. EMBO J. 6:2743-2751.
30. Subklewe, M., A. Chahroudi, K. Bickham, M. Larsson, M. G. Kurilla, N. Bhardwaj, and R. M. Steinman. 1999. Presentation of Epstein-Barr virus latency antigens to CD8+, interferon-gamma-secreting, T lymphocytes. Eur. J. Immunol. 29:3995-4001.
31. Tellam, J., G. Connolly, K. J. Green, J. J. Miles, D. J. Moss, S. R. Burrows, and R. Khanna. 2004. Endogenous presentation of CD8+ T-cell epitopes from Epstein-Barr virus-encoded nuclear antigen I. J. Exp. Med. 199:1421-1431.
32. Voo, K. S., T. Fu, H. Y. Wang, J. Tellam, H. E. Heslop, M. K. Brenner, C. M. Rooney, and R. F. Wang. 2004. Evidence for the presentation of major histocompatibility complex class I-restricted Epstein-Barr virus nuclear antigen 1 peptides to CD8+ T lymphocytes. J. Exp. Med. 199:459-470.
33. Wang, F., P. Rivailler, P. Rao, and Y. Cho. 2001. Simian homologues of Epstein-Barr virus. Phil. Trans. R. Soc. London B Biol. Sci. 356:489-497.
34. Yewdell, J. W., L. C. Anton, and J. R. Bennink. 1996. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J. Immunol. 157:1823-1826.
35. Zhao, B., R. Dalbies-Tran, H. Jiang, I. K. Ruf, J. T. Sample, F. Wang, and C. E. Sample. 2003. Transcriptional regulatory properties of Epstein-Barr virus nuclear antigen 3C are conserved in simian lymphocryptoviruses. J. Virol. 77:5639-5648.