Down-regulation of MHC class II expression through inhibition of CIITA transcription by lytic transactivator Zta during Epstein-Barr virus reactivation

Journal of Immunology

Volumn 182, Issue 4, 2009, Pages 1799-1809

  Dan, Li ^a,b   Lu, Qian ^a   Changguo, Chen ^a,c   Ming, Shi ^a   Ming, Yu ^a   Meiru, Hu ^a   Lun, Song ^a   Beifen, Shen ^a   Ning, Guo ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b 306 HOSPITAL OF PLA   (China)

^c NAVY GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

IMMEDIATE EARLY PROTEIN BZLF1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN CIITA; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; BZLF1 PROTEIN, HERPESVIRUS 4, HUMAN; HLA ANTIGEN CLASS 2; MHC CLASS II TRANSACTIVATOR PROTEIN; NUCLEAR PROTEIN;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; EPSTEIN BARR VIRUS; GENE MUTATION; GENE SILENCING; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN MOTIF; RAJI CELL; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; VIRUS REACTIVATION; ANIMAL; ANTIGEN PRESENTATION; BIOSYNTHESIS; CELL LINE; DOWN REGULATION; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS ACTIVATION; VIRUS INFECTION; WESTERN BLOTTING;

ANIMALS; ANTIGEN PRESENTATION; BLOTTING, WESTERN; CELL LINE; DOWN-REGULATION; EPSTEIN-BARR VIRUS INFECTIONS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 4, HUMAN; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC; TRANSFECTION; VIRUS ACTIVATION;

EID: 61449105702     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802686     Document Type: Article

References (53)

1. Knipe, D. M., P. M. Howley, D. E. Griffin, R. A. Lamb, and M. A. Martin, eds. 2007. Fields Virology. Lippincott, Williams, and Wilkins, Philadelphia.
2. Klein, E., L. L. Kis, and G. Klein. 2007. Epstein-Barr virus infection in humans: from harmless to life endangering virus-lymphocyte interactions. Oncogene 26: 1297-1305.
3. Williams, H., and D. H. Crawford. 2006. Epstein-Barr virus: the impact of scientific advances on clinical practice. Blood 107: 862-869.
4. Thorley-Lawson, D. A., and A. Gross. 2004. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N. Engl. J. Med. 350: 1328-1337.
5. Takada, K., and Y. Ono. 1989. Synchronous and sequential activation of latently infected Epstein-Barr virus genomes. J. Virol. 63: 445-449.
6. Countryman, J., and G. Miller. 1985. Activation of expression of latent Epstein-Barr herpesvirus after gene transfer with a small cloned subfragment of heterogeneous viral DNA. Proc. Natl. Acad. Sci. USA 82: 4085-4089.
7. 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.
8. Liao, G., F. Y. Wu, and S. D. Hayward. 2001. Interaction with the Epstein-Barr virus helicase targets Zta to DNA replication compartments. J. Virol. 75: 8792-8802.
9. Chang, Y., H. H. Lee, Y. T. Chen, J. Lu, S. Y. Wu, C. W. Chen, K. Takada, and C. H. Tsai. 2006. Induction of the early growth response 1 gene by Epstein-Barr virus lytic transactivator Zta. J. Virol. 80: 7748-7755.
10. Morrison, T. E., A. Mauser, A. Klingelhutz, and S. C. Kenney. 2004. Epstein-Barr virus immediate-early protein BZLF1 inhibits tumor necrosis factor α-induced signaling and apoptosis by down-regulating tumor necrosis factor receptor 1. J. Virol. 78: 544-549.
11. Adamson, A. L., and S. Kenney. 1999. The Epstein-Barr virus BZLF1 protein interacts physically and functionally with the histone acetylase CREB-binding protein. J. Virol. 73: 6551-6558.
12. Hsu, M., S. Y. Wu, S. S. Chang, I. J. Su, C. H. Tsai, S. J. Lai, A. L. Shiau, K. Takada, and Y. Chang. 2008. Epstein-Barr virus lytic transactivator Zta enhances chemotactic activity through induction of interleukin-8 in nasopharyngeal carcinoma cells. J. Virol. 82: 3679-3688.
13. 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.
14. Dreyfus, D. H., M. Nagasawa, J. C. Pratt, C. A. Kelleher, and E. W. Gelfand. 1999. Inactivation of NF-κB by EBV BZLF-1-encoded ZEBRA protein in human T cells. J. Immunol. 163: 6261-6268.
15. Morrison, T. E., A. Mauser, A. Wong, J. P. Ting, and S. C. Kenney. 2001. Inhibition of IFN-γ signaling by an Epstein-Barr virus immediate-early protein. Immunity 15: 787-799.
16. Miller, D. M., B. M. Rahill, J. M. Boss, M. D. Lairmore, J. E. Durbin, J. W. Waldman, and D. D. Sedmak. 1998. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the Jak/Stat pathway. J. Exp. Med. 187: 675-683.
17. Heise, M. T., M. Connick, and H. W. Virgin IV. 1998. Murine cytomegalovirus inhibits interferon γ-induced antigen presentation to CD4 T cells by macrophages via regulation of expression of major histocompatibility complex class II-associated genes. J. Exp. Med. 187: 1037-1046.
18. + T cells. Nat. Med. 5: 1039-1043.
19. Chevalier, M. S., and D. C. Johnson. 2003. Human cytomegalovirus US3 chimeras containing US2 cytosolic residues acquire major histocompatibility class I and II protein degradation properties. J. Virol. 77: 4731-4738.
20. Hegde, N. R., R. A. Tomazin, T. W. Wisner, C. Dunn, J. M. Boname, D. M. Lewinsohn, and D. C. Johnson. 2002. Inhibition of HLA-DR assembly, transport, and loading by human cytomegalovirus glycoprotein US3: a novel mechanism for evading major histocompatibility complex class II antigen presentation. J. Virol. 76: 10929-10941.
21. Ressing, M. E., D. van Leeuwen, F. A. Verreck, R. Gomez, B. Heemskerk, M. Toebes, M. M. Mullen, T. S. Jardetzky, R. Longnecker, M. W. Schilham, et al. 2003. Interference with T cell receptor-HLA-DR interactions by Epstein-Barr virus gp42 results in reduced T helper cell recognition. Proc. Natl. Acad. Sci. USA 100: 11583-11588.
22. Ressing, M. E., D. van Leeuwen, F. A. Verreck, S. Keating, R. Gomez, K. L. Franken, T. H. Ottenhoff, M. Spriggs, T. N. Schumacher, L. M. Hutt-Fletcher, et al. 2005. Epstein-Barr virus gp42 is posttranslationally modified to produce soluble gp42 that mediates HLA class II immune evasion. J. Virol. 79: 841-852.
23. Drozina, G., J. Kohoutek, N. Jabrane-Ferrat, and B. M. Peterlin. 2005. Expression of MHC II genes. Curr. Top. Microbiol. Immunol. 290: 147-170.
24. Chang, C. H., T. S. Gourley, and T. J. Sisk. 2002. Function and regulation of class II transactivator in the immune system. Immunol. Res. 25: 131-142.
25. Callard, R. E., Y. L. Lau, J. G. Shields, S. H. Smith, J. Cairns, L. Flores-Romo, and J. Gordon. 1988. The marmoset B-lymphoblastoid cell line (B95-8) produces and responds to B-cell growth and differentiation factors: role of shed CD23 (sCD23). Immunology 65: 379-384.
26. Miller, G., T. Shope, H. Lisco, D. Stitt, and M. Lipman. 1972. Epstein-Barr virus: transformation, cytopathic changes, and viral antigens in squirrel monkey and marmoset leukocytes. Proc. Natl. Acad. Sci. USA 69: 383-387.
27. Decaussin, G., V. Leclerc, and T. Ooka. 1995. The lytic cycle of Epstein-Barr virus in the nonproducer Raji line can be rescued by the expression of a 135-kilodalton protein encoded by the BALF2 open reading frame. J. Virol. 69: 7309-7314.
28. Daniel, L. W., G. Bauer, and H. zur Hausen. 1984. Effect of indomethacin on Epstein-Barr virus early antigen induction. Cancer Res. 44: 981-983.
29. Gradoville, L., D. Kwa, A. El-Guindy, and G. Miller. 2002. Protein kinase C-independent activation of the Epstein-Barr virus lytic cycle. J. Virol. 76: 5612-5626.
30. Countryman, J. K., L. Gradoville, and G. Miller. 2008. Histone hyperacetylation occurs on promoters of lytic cycle regulatory genes in Epstein-Barr virus-infected cell lines which are refractory to disruption of latency by histone deacetylase inhibitors. J. Virol. 82: 4706-4719.
31. Carra, G., and R. S. Accolla. 1987. Structural analysis of human Ia antigens reveals the existence of a fourth molecular subset distinct from DP, DQ, and DR molecules. J. Exp. Med. 165: 47-63.
32. Ting, J. P., and J. Trowsdale. 2002. Genetic control of MHC class II expression. Cell 109(Suppl.): S21-S33.
33. Van der Stoep, N., E. Quinten, M. Marcondes Rezende, and P. J. van den Elsen. 2004. E47, IRF-4, and PU.1 synergize to induce B-cell-specific activation of the class II transactivator promoter III (CIITA-PIII). Blood 104: 2849-2857.
34. Muhlethaler-Mottet, A., L. A. Otten, V. Steimle, and B. Mach. 1997. Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO J. 16: 2851-2860.
35. Masternak, K., and W. Reith. 2002. Promoter-specific functions of CIITA and the MHC class II enhanceosome in transcriptional activation. EMBO J. 21: 1379-1388.
36. Haque, A., L. M. Hajiaghamohseni, P. Li, K. Toomy, and J. S. Blum. 2007. Invariant chain modulates HLA class II protein recycling and peptide presentation in nonprofessional antigen presenting cells. Cell. Immunol. 249: 20-29.
37. Hicks, M. R., S. S. Al-Mehairi, and A. J. Sinclair. 2003. The zipper region of Epstein-Barr virus bZIP transcription factor Zta is necessary but not sufficient to direct DNA binding. J. Virol. 77: 8173-8177.
38. Giot, J. F., I. Mikaelian, M. Buisson, E. Manet, I. Joab, J. C. Nicolas, and A. Sergeant. 1991. Transcriptional interference between the EBV transcription factors EB1 and R: both DNA-binding and activation domains of EB1 are required. Nucleic Acids Res. 19: 1251-1258.
39. Lieberman, P. M., J. M. Hardwick, J. Sample, G. S. Hayward, and S. D. Hayward. 1990. The zta transactivator involved in induction of lytic cycle gene expression in Epstein-Barr virus-infected lymphocytes binds to both AP-1 and ZRE sites in target promoter and enhancer regions. J. Virol. 64: 1143-1155.
40. Ellwood, K., W. Huang, R. Johnson, and M. Carey. 1999. Multiple layers of cooperativity regulate enhanceosome-responsive RNA polymerase II transcription complex assembly. Mol. Cell. Biol. 19: 2613-2623.
41. Zhao, M., F. L. Flynt, M. Hong, H. Chen, C. A. Gilbert, N. T. Briley, S. C. Bolick, K. L. Wright, and J. F. Piskurich. 2007. MHC class II transactivator (CIITA) expression is up-regulated in multiple myeloma cells by IFN-γ. Mol. Immunol. 44: 2923-2932.
42. Kolman, J. L., N. Taylor, L. Gradoville, J. Countryman, and G. Miller. 1996. Comparing transcriptional activation and autostimulation by ZEBRA and ZEBRA/ c-Fos chimeras. J. Virol. 70: 1493-1504.
43. Francis, A., T. Ragoczy, L. Gradoville, L. Heston, A. El-Guindy, Y. Endo, and G. Miller. 1999. Amino acid substitutions reveal distinct functions of serine 186 of the ZEBRA protein in activation of early lytic cycle genes and synergy with the Epstein-Barr virus R transactivator. J. Virol. 73: 4543-4551.
44. Malnati, M. S., M. Marti, T. LaVaute, D. Jaraquemada, W. Biddison, R. DeMars, and E. O. Long. 1992. Processing pathways for presentation of cytosolic antigen to MHC class II-restricted T cells. Nature 357: 702-704.
45. Aichinger, G., L. Karlsson, M. R. Jackson, M. Vestberg, J. H. Vaughan, L. Teyton, R. I. Lechler, and P. A. Peterson. 1997. Major histocompatibility complex class II-dependent unfolding, transport, and degradation of endogenous proteins. J. Biol. Chem. 272: 29127-29136.
46. Paludan, C., D. Schmid, M. Landthaler, M. Vockerodt, D. Kube, T. Tuschl, and C. Munz. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307: 593-596.
47. Hegde, N. R., M. S. Chevalier, and D. C. Johnson. 2003. Viral inhibition of MHC class II antigen presentation. Trends Immunol. 24: 278-285.
48. Goodbourn, S., L. Didcock, and R. E. Randall. 2000. Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 81: 2341-2364.
49. Flemington, E., and S. H. Speck. 1990. Epstein-Barr virus BZLF1 trans activator induces the promoter of a cellular cognate gene, c-fos. J. Virol. 64: 4549 - 4552.
50. Cayrol, C., and E. K. Flemington. 1995. Identification of cellular target genes of the Epstein-Barr virus transactivator Zta: activation of transforming growth factor β igh3 (TGF-β igh3) and TGF-β1. J. Virol. 69: 4206-4212.
51. Gutsch, D. E., E. A. Holley-Guthrie, Q. Zhang, B. Stein, M. A. Blanar, A. S. Baldwin, and S. C. Kenney. 1994. The bZIP transactivator of Epstein-Barr virus, BZLF1, functionally and physically interacts with the p65 subunit of NF-κB. Mol. Cell. Biol. 14: 1939-1948.
52. Mahot, S., A. Sergeant, E. Drouet, and H. Gruffat. 2003. A novel function for the Epstein-Barr virus transcription factor EB1/Zta: induction of transcription of the hIL-10 gene. J. Gen. Virol. 84: 965-974.
53. 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.