Cytotoxic CD4+ T cell responses to EBV contrast with CD8 responses in breadth of lytic cycle antigen choice and in lytic cycle recognition

Journal of Immunology

Volumn 187, Issue 1, 2011, Pages 92-101

  Long, Heather M ^a   Leese, Alison M ^a   Chagoury, Odette L ^a   Connerty, Shawn R ^a   Quarcoopome, Jared ^a   Quinn, Laura L ^a   Shannon Lowe, Claire ^a   Rickinson, Alan B ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; EARLY PROTEIN; EPITOPE; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; IMMEDIATE EARLY PROTEIN; LATE PROTEIN; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS PROTEIN;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSPOT ASSAY; EPSTEIN BARR VIRUS; EX VIVO STUDY; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; VIRUS CELL INTERACTION; VIRUS CELL TRANSFORMATION; VIRUS REPLICATION;

ANTIGENS, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CLONE CELLS; CYTOTOXICITY TESTS, IMMUNOLOGIC; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERFERON-GAMMA; PHOSPHOPROTEINS; TRANS-ACTIVATORS; VIRUS REPLICATION;

EID: 79960409791     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100590     Document Type: Article

References (50)

1. Hislop, A. D., G. S. Taylor, D. Sauce, and A. B. Rickinson. 2007. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu. Rev. Immunol. 25: 587-617.
2. Gottschalk, S., C. M. Rooney, and H. E. Heslop. 2005. Post-transplant lymphoproliferative disorders. Annu. Rev. Med. 56: 29-44.
3. Katz, B. Z., N. Raab-Traub, and G. Miller. 1989. Latent and replicating forms of Epstein-Barr virus DNA in lymphomas and lymphoproliferative diseases. J. Infect. Dis. 160: 589-598.
4. Rea, D., C. Fourcade, V. Leblond, M. Rowe, I. Joab, L. Edelman, M. O. Bitker, I. Gandjbakhch, C. Suberbielle, J. P. Farcet, et al. 1994. Patterns of Epstein-Barr virus latent and replicative gene expression in Epstein-Barr virus B cell lymphoproliferative disorders after organ transplantation. Transplantation 58: 317-324. (Pubitemid 24252285)
5. Rickinson, A., and E. Kieff. 2007. Epstein-Barr virus. In Fields Virology. B. Fields, D. Knipe, P. Howley, R. Chanock, and J. Melnick, eds. Lippincott, Williams & Wilkins, Philadelphia, p. 2655-2700.
6. Brooks, J. M., S. P. Lee, A. M. Leese, W. A. Thomas, M. Rowe, and A. B. Rickinson. 2009. Cyclical expression of EBV latent membrane protein 1 in EBV-transformed B cells underpins heterogeneity of epitope presentation and CD8+ T cell recognition. J. Immunol. 182: 1919-1928.
7. Long, H. M., T. A. Haigh, N. H. Gudgeon, A. M. Leen, C. W. Tsang, J. Brooks, E. Landais, E. Houssaint, S. P. Lee, A. B. Rickinson, and G. S. Taylor. 2005. CD4+ T-cell responses to Epstein-Barr virus (EBV) latent-cycle antigens and the recognition of EBV-transformed lymphoblastoid cell lines. J. Virol. 79: 4896-4907.
8. Mautner, J., D. Pich, F. Nimmerjahn, S. Milosevic, D. Adhikary, H. Christoph, K. Witter, G. W. Bornkamm, W. Hammerschmidt, and U. Behrends. 2004. Epstein-Barr virus nuclear antigen 1 evades direct immune recognition by CD4+ T helper cells. Eur. J. Immunol. 34: 2500-2509.
9. Khanna, R., S. R. Burrows, P. M. Steigerwald-Mullen, S. A. Thomson, M. G. Kurilla, and D. J. Moss. 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.
10. Paludan, C., K. Bickham, S. Nikiforow, M. L. Tsang, K. Goodman, W. A. Hanekom, J. F. Fonteneau, S. Stevanović, and C. Münz. 2002. Epstein-Barr nuclear antigen 1-specific CD4(+) Th1 cells kill Burkitt's lymphoma cells. J. Immunol. 169: 1593-1603. (Pubitemid 34809208)
11. Leung, C. S., T. A. Haigh, L. K. Mackay, A. B. Rickinson, and G. S. Taylor. 2010. Nuclear location of an endogenously expressed antigen, EBNA1, restricts access to macroautophagy and the range of CD4 epitope display. Proc. Natl. Acad. Sci. USA 107: 2165-2170.
12. Pudney, V. A., A. M. Leese, A. B. Rickinson, and A. D. Hislop. 2005. CD8+ immunodominance among Epstein-Barr virus lytic cycle antigens directly reflects the efficiency of antigen presentation in lytically infected cells. J. Exp. Med. 201: 349-360.
13. Sauce, D., M. Larsen, R. J. Abbott, A. D. Hislop, A. M. Leese, N. Khan, L. Papagno, G. J. Freeman, and A. B. Rickinson. 2009. Upregulation of interleukin 7 receptor alpha and programmed death 1 marks an epitope-specific CD8+ T-cell response that disappears following primary Epstein-Barr virus infection. J. Virol. 83: 9068-9078.
14. Rowe, M., and J. Zuo. 2010. Immune responses to Epstein-Barr virus: molecular interactions in the virus evasion of CD8+ T cell immunity. Microbes Infect. 12: 173-181.
15. Croft, N. P., C. Shannon-Lowe, A. I. Bell, D. Horst, E. Kremmer, M. E. Ressing, E. J. Wiertz, J. M. Middeldorp, M. Rowe, A. B. Rickinson, and A. D. Hislop. 2009. Stage-specific inhibition of MHC class I presentation by the Epstein-Barr virus BNLF2a protein during virus lytic cycle. PLoS Pathog. 5: e1000490.
16. Zuo, J., A. Currin, B. D. Griffin, C. Shannon-Lowe, W. A. Thomas, M. E. Ressing, E. J. Wiertz, and M. Rowe. 2009. The Epstein-Barr virus G-protein-coupled receptor contributes to immune evasion by targeting MHC class I molecules for degradation. PLoS Pathog. 5: e1000255.
17. Zuo, J., W. Thomas, D. van Leeuwen, J. M. Middeldorp, E. J. Wiertz, M. E. Ressing, and M. Rowe. 2008. The DNase of gammaherpesviruses impairs recognition by virus-specific CD8+ T cells through an additional host shutoff function. J. Virol. 82: 2385-2393. (Pubitemid 351293539)
18. Sylwester, A. W., B. L. Mitchell, J. B. Edgar, C. Taormina, C. Pelte, F. Ruchti, P. R. Sleath, K. H. Grabstein, N. A. Hosken, F. Kern, et al. 2005. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 202: 673-685.
19. Adhikary, D., U. Behrends, A. Moosmann, K. Witter, G. W. Bornkamm, and J. Mautner. 2006. Control of Epstein-Barr virus infection in vitro by T helper cells specific for virion glycoproteins. J. Exp. Med. 203: 995-1006.
20. Wallace, L. E., J. Wright, D. O. Ulaeto, A. J. Morgan, and A. B. Rickinson. 1991. Identification of two T-cell epitopes on the candidate Epstein-Barr virus vaccine glycoprotein gp340 recognized by CD4+ T-cell clones. J. Virol. 65: 3821-3828.
21. Adhikary, D., U. Behrends, H. Boerschmann, A. Pfünder, S. Burdach, A. Moosmann, K. Witter, G. W. Bornkamm, and J. Mautner. 2007. Immunodominance of lytic cycle antigens in Epstein-Barr virus-specific CD4+ T cell preparations for therapy. PLoS ONE 2: e583.
22. Landais, E., X. Saulquin, E. Scotet, L. Trautmann, M. A. Peyrat, J. L. Yates, W. W. Kwok, M. Bonneville, and E. Houssaint. 2004. Direct killing of Epstein-Barr virus (EBV)-infected B cells by CD4 T cells directed against the EBV lytic protein BHRF1. Blood 103: 1408-1416. (Pubitemid 38168656)
23. Leen, A., P. Meij, I. Redchenko, J. Middeldorp, E. Bloemena, A. Rickinson, and N. Blake. 2001. Differential immunogenicity of Epstein-Barr virus latent-cycle proteins for human CD4(+) T-helper 1 responses. J. Virol. 75: 8649-8659. (Pubitemid 32768969)
24. Shannon-Lowe, C., G. Baldwin, R. Feederle, A. Bell, A. Rickinson, and H. J. Delecluse. 2005. Epstein-Barr virus-induced B-cell transformation: quantitating events from virus binding to cell outgrowth. J. Gen. Virol. 86: 3009-3019.
25. Shannon-Lowe, C., E. Adland, A. I. Bell, H. J. Delecluse, A. B. Rickinson, and M. Rowe. 2009. Features distinguishing Epstein-Barr virus infections of epithelial cells and B cells: viral genome expression, genome maintenance, and genome amplification. J. Virol. 83: 7749-7760.
26. Gudgeon, N. H., G. S. Taylor, H. M. Long, T. A. Haigh, and A. B. Rickinson. 2005. Regression of Epstein-Barr virus-induced B-cell transformation in vitro involves virus-specific CD8+ T cells as the principal effectors and a novel CD4+ T-cell reactivity. J. Virol. 79: 5477-5488.
27. Tan, L. C., N. Gudgeon, N. E. Annels, P. Hansasuta, C. A. O'Callaghan, S. Rowland-Jones, A. J. McMichael, A. B. Rickinson, and M. F. Callan. 1999. A re-evaluation of the frequency of CD8+ T cells specific for EBV in healthy virus carriers. J. Immunol. 162: 1827-1835.
28. Taylor, G. S., H. M. Long, T. A. Haigh, M. Larsen, J. Brooks, and A. B. Rickinson. 2006. A role for intercellular antigen transfer in the recognition of EBV-transformed B cell lines by EBV nuclear antigen-specific CD4+ T cells. J. Immunol. 177: 3746-3756.
29. Feederle, R., M. Kost, M. Baumann, A. Janz, E. Drouet, W. Hammerschmidt, and H. J. Delecluse. 2000. The Epstein-Barr virus lytic program is controlled by the co-operative functions of two transactivators. EMBO J. 19: 3080-3089.
30. Betts, M. R., and R. A. Koup. 2004. Detection of T-cell degranulation: CD107a and b. Methods Cell Biol. 75: 497-512.
31. Paludan, C., D. Schmid, M. Landthaler, M. Vockerodt, D. Kube, T. Tuschl, and C. Münz. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307: 593-596. (Pubitemid 40165684)
32. Mackay, L. K., H. M. Long, J. M. Brooks, G. S. Taylor, C. S. Leung, A. Chen, F. Wang, and A. B. Rickinson. 2009. T cell detection of a B-cell tropic virus infection: newly-synthesised versus mature viral proteins as antigen sources for CD4 and CD8 epitope display. PLoS Pathog. 5: e1000699.
33. Landais, E., X. Saulquin, M. Bonneville, and E. Houssaint. 2005. Long-term MHC class II presentation of the EBV lytic protein BHRF1 by EBV latently infected b cells following capture of BHRF1 antigen. J. Immunol. 175: 7939-7946. (Pubitemid 41798354)
34. Elion, G. B., P. A. Furman, J. A. Fyfe, P. de Miranda, L. Beauchamp, and H. J. Schaeffer. 1977. Selectivity of action of an antiherpetic agent, 9-(2-hydroxyethoxymethyl) guanine. Proc. Natl. Acad. Sci. USA 74: 5716-5720.
35. Amyes, E., C. Hatton, D. Montamat-Sicotte, N. Gudgeon, A. B. Rickinson, A. J. McMichael, and M. F. Callan. 2003. Characterization of the CD4+ T cell response to Epstein-Barr virus during primary and persistent infection. J. Exp. Med. 198: 903-911.
36. Scherrenburg, J., E. R. Piriou, N. M. Nanlohy, and D. van Baarle. 2008. Detailed analysis of Epstein-Barr virus-specific CD4+ and CD8+ T cell responses during infectious mononucleosis. Clin. Exp. Immunol. 153: 231-239.
37. Merlo, A., R. Turrini, S. Bobisse, R. Zamarchi, R. Alaggio, R. Dolcetti, J. Mautner, P. Zanovello, A. Amadori, and A. Rosato. 2010. Virus-specific cytotoxic CD4+ T cells for the treatment of EBV-related tumors. J. Immunol. 184: 5895-5902.
38. Bhaduri-McIntosh, S., M. J. Rotenberg, B. Gardner, M. Robert, and G. Miller. 2008. Repertoire and frequency of immune cells reactive to Epstein-Barr virus-derived autologous lymphoblastoid cell lines. Blood 111: 1334-1343. (Pubitemid 351213420)
39. Haigh, T. A., X. Lin, H. Jia, E. P. Hui, A. T. Chan, A. B. Rickinson, and G. S. Taylor. 2008. EBV latent membrane proteins (LMPs) 1 and 2 as immunotherapeutic targets: LMP-specific CD4+ cytotoxic T cell recognition of EBV-transformed B cell lines. J. Immunol. 180: 1643-1654.
40. Suri, A., S. B. Lovitch, and E. R. Unanue. 2006. The wide diversity and complexity of peptides bound to class II MHC molecules. Curr. Opin. Immunol. 18: 70-77.
41. Draenert, R., M. Altfeld, C. Brander, N. Basgoz, C. Corcoran, A. G. Wurcel, D. R. Stone, S. A. Kalams, A. Trocha, M. M. Addo, et al. 2003. Comparison of overlapping peptide sets for detection of antiviral CD8 and CD4 T cell responses. J. Immunol. Methods 275: 19-29. (Pubitemid 36351539)
42. Callan, M. F. 2004. The immune response to Epstein-Barr virus. Microbes Infect. 6: 937-945. (Pubitemid 39061216)
43. Omiya, R., C. Buteau, H. Kobayashi, C. V. Paya, and E. Celis. 2002. Inhibition of EBV-induced lymphoproliferation by CD4(+) T cells specific for an MHC class II promiscuous epitope. J. Immunol. 169: 2172-2179. (Pubitemid 34857685)
44. Mautner, J., and G. W. Bornkamm. 2011. The role of virus-specific CD4+ T cells in the control of Epstein-Barr virus infection. Eur. J. Cell Biol. .
45. Feederle, R., C. Shannon-Lowe, G. Baldwin, and H. J. Delecluse. 2005. Defective infectious particles and rare packaged genomes produced by cells carrying terminal-repeat-negative epstein-barr virus. J. Virol. 79: 7641-7647.
46. Adhikary, D., U. Behrends, R. Feederle, H. J. Delecluse, and J. Mautner. 2008. Standardized and highly efficient expansion of Epstein-Barr virus-specific CD4+ T cells by using virus-like particles. J. Virol. 82: 3903-3911. (Pubitemid 351521227)
47. Keating, S., S. Prince, M. Jones, and M. Rowe. 2002. The lytic cycle of Epstein-Barr virus is associated with decreased expression of cell surface major histocompatibility complex class I and class II molecules. J. Virol. 76: 8179-8188. (Pubitemid 34809072)
48. Li, D., L. Qian, C. Chen, M. Shi, M. Yu, M. Hu, L. Song, B. Shen, and N. Guo. 2009. Down-regulation of MHC class II expression through inhibition of CIITA transcription by lytic transactivator Zta during Epstein-Barr virus reactivation. J. Immunol. 182: 1799-1809.
49. Montone, K. T., R. L. Hodinka, K. E. Salhany, E. Lavi, A. Rostami, and J. E. Tomaszewski. 1996. Identification of Epstein-Barr virus lytic activity in post-transplantation lymphoproliferative disease. Mod. Pathol. 9: 621-630.
50. Haque, T., G. M. Wilkie, M. M. Jones, C. D. Higgins, G. Urquhart, P. Wingate, D. Burns, K. McAulay, M. Turner, C. Bellamy, et al. 2007. Allogeneic cytotoxic T-cell therapy for EBV-positive posttransplantation lymphoproliferative disease: results of a phase 2 multicenter clinical trial. Blood 110: 1123-1131. (Pubitemid 47281407)