Epstein-Barr virus nuclear antigen (EBNA) 3A induces the expression of and interacts with a subset of chaperones and co-chaperones

Journal of General Virology

Volumn 89, Issue 4, 2008, Pages 866-877

  Young, Paul R ^a   Anderton, Emma ^a   Paschos, Kostas ^a   White, Rob ^a   Allday, Martin J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CELL PROTEIN; CHAPERONE; COMPLEMENTARY DNA; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN 3A; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70B/B'; MESSENGER RNA; PROTEIN BAG3; PROTEIN DNAJA1; BAG3 PROTEIN, HUMAN; DNAJA1 PROTEIN, HUMAN; EBNA 3A ANTIGEN; EBNA-3A ANTIGEN; HEAT SHOCK PROTEIN 72; HSPA7 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; CELL IMMORTALIZATION; CONTROLLED STUDY; CYTOPLASM; DIPLOIDY; EPSTEIN BARR VIRUS; FIBROBLAST; GENE CONTROL; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL LINE; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; VIRUS INFECTION; ACTIVE TRANSPORT; CELL LINE; CELL NUCLEUS; GENETICS; METABOLISM; PROMOTER REGION; TRANSACTIVATION; UPREGULATION; VIRUS CELL TRANSFORMATION;

ADENOVIRIDAE; HUMAN HERPESVIRUS 4;

ACTIVE TRANSPORT, CELL NUCLEUS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; CELL NUCLEUS; CELL TRANSFORMATION, VIRAL; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HSP72 HEAT-SHOCK PROTEINS; HUMANS; PROMOTER REGIONS (GENETICS); TRANS-ACTIVATION (GENETICS); UP-REGULATION;

EID: 45549083730     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.83414-0     Document Type: Article

References (50)

1. Antoku, K., Maser, R. S., Scully, W. J., Jr, Delach, S. M. & Johnson, D. E. (2001). Isolation of Bcl-2 binding proteins that exhibit homology with BAG-1 and suppressor of death domains protein. Biochem Biophys Res Commun 286, 1003-1010.
2. Bain, M., Watson, R. J., Farrell, P. J. & Allday, M. J. (1996). Epstein-Barr virus nuclear antigen 3C is a powerful repressor of transcription when tethered to DNA. J Virol 70, 2481-2489.
3. Beere, H. M. & Green, D. R. (2001). Stress management - heat shock protein-70 and the regulation of apoptosis. Trends Cell Biol 11, 6-10.
4. Bornkamm, G. W. & Hammerschmidt W. (2001). Molecular virology of Epstein-Barr virus. Philos Trans R Soc Lond B Biol Sci 356, 437-459.
5. Bornkamm, G. W., Berens, C., Kuklik-Roos, C., Bechet, J. M., Laux, G., Bachl, J., Korndoerfer, M., Schlee, M., Holzel, M. & other authors (2005). Stringent doxycycline-dependent control of gene activities using an episomal one-vector system. Nucleic Acids Res 33, e137.
6. Bukau, B. & Horwich, A. L. (1998). The Hsp70 and Hsp60 chaperone machines. Cell 92, 351-366.
7. Calderwood, S. K., Khaleque, M. A., Sawyer, D. B. & Ciocca, D. R. (2006). Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem Sci 31, 164-172.
8. Chinnadurai, G. (2002). CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Mol Cell 9, 213-224.
9. Cludts, I. & Farrell, P. J. (1998). Multiple functions within the Epstein-Barr virus EBNA-3A protein. J Virol 72, 1862-1869.
10. Demand, J., Luders, J. & Hohfeld, J. (1998). The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Mol Cell Biol 18, 2023-2028.
11. Doong, H., Rizzo, K., Fang, S., Kulpa, V., Weissman, A. M. & Kohn, E. C. (2003). CAIR-1/BAG-3 abrogates heat shock protein-70 chaperone complex-mediated protein degradation: accumulation of poly-ubiquitinated Hsp90 client proteins. J Biol Chem 278, 28490-28500.
12. Esser, C., Alberti, S. & Hohfeld, J. (2004). Cooperation of molecular chaperoncs with the ubiquitin/proteasome system. Biochim Biophys Acta 1695, 171-188.
13. Gabai, V. L., Meriin, A. B., Mosser, D. D., Caron, A. W., Rits, S., Shifrin, V. I. & Sherman, M. Y. (1997). Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermo tolerance. J Biol Chem 272, 18033-18037.
14. Greene, L. E., Zinner, R., Naficy, S. & Eisenberg, E. (1995). Effect of nucleotide on the binding of peptides to 70-kDa heat shock protein. J Biol Chem 270, 2967-2973.
15. Hart, S. L., Arancibia-Carcamo, C. V., Wolfert, M. A., Mailhos, C., O'Reilly, N. J., Ali, R. R., Coutelle, C., George, A. J., Harbottle, R. P. & other authors (1998). Lipid-mediated enhancement of transfection by a nonviral integrin-targeting vector. Hum Gene Ther 9, 575-585.
16. He, T. C., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W. & Vogelstein, B. (1998). A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 95, 2509-2514.
17. He, H., Soncin, F., Grammatikakis, N., Li, Y., Siganou, A., Gong, J., Brown, S. A., Kingston, R. E. & Calderwood, S. K. (2003). Elevated expression of heat shock factor (HSF) 2A stimulates HSF1-induced transcription during stress. J Biol Chem 278, 35465-35475.
18. Hickabottom, M., Parker, G. A., Freemont, P., Crook, T. & Allday, M. J. (2002). Two nonconsensus sites in the Epstein-Barr virus oncoprotein EBNA3A cooperate to bind the co-reprcssor carboxyl-terminal-binding protein (CtBP). J Biol Chem 277, 47197-47204.
19. Kashuba, E., Pokrovskaja, K., Klein, G. & Szekely, L. (1999). Epstein-Barr virus-encoded nuclear protein EBNA-3 interacts with the epsilon-subunit of the T-complex protein 1 chaperonin complex. J Hum Virol 2, 33-37.
20. Kelly, G. L., Milner, A. E., Tierney, R. J., Croom-Carter, D. S., Altmann, M., Hammerschmidt, W., Bell, A. I. & Rickinson, A. B. (2005). Epstein-Barr virus nuclear antigen 2 (EBNA2) gene deletion is consistently linked with EBNA3A, -3B, and -3C expression in Burldtt's lymphoma cells and with increased resistance to apoptosis. J Virol 79, 10709-10717.
21. Knight, J. S., Lan, K., Subramanian, C. & Robertson, E. S. (2003). Epstein-Barr virus nuclear antigen 3C recruits histone deacetylase activity and associates with the corepressors mSin3A and NCoR in human B-cell lines. J Virol 77, 4261-4272.
22. Le Roux, A., Kerdiles, B., Walls, D, Dedieu, J. F. & Perricaudet, M. (1994). The Epstein-Barr virus determined nuclear antigens EBNA-3A, -3B, and -3C repress EBNA-2-mediated transactivation of the viral terminal protein 1 gene promoter. Virology 205, 596-602.
23. Leao, M., Anderton, E., Wade, M., Meekings, K. & Allday, M. J. (2007). Epstein-Barr virus-induced resistance to drugs that activate the mitotic spindle assembly checkpoint in Burkitt's lymphoma cells. J Virol 81, 248-260.
24. Lee, J. H., Takahashi, T., Yasuhara, N., Inazawa, J., Kamada, S. & Tsujimoto, Y. (1999). Bis, a Bcl-2-binding protein that synergizes with Bcl-2 in preventing cell death. Oncogene 18, 6183-6190.
25. Leung, T. K., Rajendran, M. Y., Monfries, C., Hall, C. & Lim, L. (1990). The human heat-shock protein family. Expression of a novel heat-inducible HSP70 (HSP70B') and isolation of its cDNA and genomic DNA. Biochem J 267, 125-132.
26. Maruo, S., Johannsen, E., Illanes, D., Cooper, A. & Kieff, E. (2003). Epstein-Barr virus nuclear protein EBNA3A is critical for maintaining lymphoblastoid cell line growth. J Virol 77, 10437-10447.
27. Mayer, M. P. (2005). Recruitment of Hsp70 chaperones: a crucial part of viral survival strategies. Rev Physiol Biochem Pharmacol 153, 1-46.
28. McCarty, J. S., Buchberger, A., Reinstein, J. & Bukau, B. (1995). The role of ATP in the functional cycle of the DnaK chaperone system. J Mol Biol 249, 126-137.
29. Morimoto, R. I. (1998). Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12, 3788-3796.
30. Mosser, D. D. & Morimoto, R. I. (2004). Molecular chaperones and the stress of oncogenesis. Oncogene 23, 2907-2918.
31. Mosser, D. D., Caron, A. W., Bourget, L., Denis-Larose, C. & Massie, B. (1997). Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol Cell Biol 17, 5317-5327.
32. Mosser, D. D., Caron, A. W., Bourget L., Meriin, A. B., Sherman, M. Y., Morimoto, R. I. & Massie, B. (2000). The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 20, 7146-7159.
33. O'Nions, J. & Allday, M. J. (2004). Proliferation and differentiation in isogenic populations of peripheral B cells activated by Epstein-Barr virus or T cell-derived mitogens. J Gen Virol 85, 881-895.
34. + but not ATP hydrolysis. Nature 365, 664-666.
35. Radkov, S. A., Bain, M., Farrell, P. J., West M., Rowe, M. & Allday, M. J. (1997). Epstein-Barr virus EBNA3C represses Cp, the major promoter for EBNA expression, but has no effect on the promoter of the cell gene CD21. J Virol 71, 8552-8562.
36. Radkov, S. A., Touitou, R., Brehm, A., Rowe, M., West, M., Kouzarides, T. & Allday, M. J. (1999). Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J Virol 73, 5688-5697.
37. Rickinson, A. B. & Kieff, E. (2007). Epstein-Barr virus. In Fields Virology, 5th edn, pp. 2655-2700. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
38. Robertson, E. S., Lin, J. & Kieff, E. (1996). The amino-terminal domains of Epstein-Barr virus nuclear proteins 3A, 3B, and 3C interact with RBPJκ. J Virol 70, 3068-3074.
39. Spender, L. C., Cannell, E. J., Hollyoake, M., Wensing, B., Gawn, J. M., Brimmell, M., Packham, G. & Farrell, P. J. (1999). Control of cell cycle entry and apoptosis in B lymphocytes infected by Epstein-Barr virus. J Virol 73, 4678-4688.
40. Srivastava, P. (2002). Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2, 185-194.
41. vall2-transformed cells. Oncogene 25, 1485-1495.
42. Takayama, S., Sato, T., Krajewski, S., Kochel, K, Irie, S., Millan, J. A. & Reed, J. C. (1995). Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80, 279-284.
43. Takayama, S., Xie, Z. & Reed, J. C. (1999). An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J Biol Chem 274, 781-786.
44. Tomkinson, B. & Kieff, E. (1992). Second-site homologous recombination in Epstein-Barr virus: insertion of type 1 EBNA 3 genes in place of type 2 has no effect on in vitro infection. J Virol 66, 780-789.
45. Tomkinson, B., Robertson, E. & Kieff, E. (1993). Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J Virol 67, 2014-2025.
46. Touitou, R., Hickabottom, M., Parker, G., Crook, T. & Allday, M. J. (2001). Physical and functional interactions between the corepressor CtBP and the Epstein-Barr virus nuclear antigen EBNA3C. J Virol 75, 7749-7755.
47. Touitou, R., O'Nions, J., Heaney, J. & Allday, M. J. (2005). Epstein-Barr virus EBNA3 proteins bind to the C8/α7 subunit of the 20S proteasome and are degraded by 20S proteasomes in vitro, but are very stable in latently infected B cells. J Gen Virol 86, 1269-1277.
48. Trinklein, N. D., Murray, J. I., Hartman, S. J., Botstein, D. & Myers, R. M. (2004). The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol Biol Cell 15, 1254-1261.
49. White, R. E., Wade-Martins, R., Hart, S. L., Frampton, J., Huey, B., Desai-Mehta, A., Cerosaletti, K. M., Concannon, P. & James, M. R. (2003). Functional delivery of large genomic DNA to human cells with a peptide-lipid vector. J Gene Med 5, 883-892.
50. Zeng, M., Smith, S. K., Siegel, F., Shi, Z, Van Kampen, K. R., Elmets, C. A. & Tang, D. C. (2001). AdEasy system made easier by selecting the viral backbone plasmid preceding homologous recombination. Biotechniques 31, 260-262.