The ATM/ATR signaling effector Chk2 is targeted by Epstein-Barr virus nuclear antigen 3C to release the G2/M cell cycle block

Journal of Virology

Volumn 81, Issue 12, 2007, Pages 6718-6730

  Choudhuri, Tathagata ^a   Verma, Subhash C ^a   Lan, Ke ^a   Murakami, Masanao ^a   Robertson, Erle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 2; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS NUCLEAR ANTIGEN 3C; NOCODAZOLE; PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CONTROLLED STUDY; EPSTEIN BARR VIRUS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS GENE;

14-3-3 PROTEINS; ANTIGENS, VIRAL; B-LYMPHOCYTES; CDC25 PHOSPHATASE; CELL CYCLE PROTEINS; CELL DIVISION; CYTOPLASM; DNA-BINDING PROTEINS; EPSTEIN-BARR VIRUS NUCLEAR ANTIGENS; G2 PHASE; GENE EXPRESSION REGULATION, VIRAL; HUMANS; MODELS, BIOLOGICAL; NOCODAZOLE; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 34249947000     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00053-07     Document Type: Article

References (41)

1. Borgne, A., and L. Meyer. 1996. Sequential dephosphorylation of p34(cdc2) on Thr-14 and Tyr-15 at the prophase/metaphase transition. J. Biol. Chem. 271:27847-27854.
2. Bulavin, D. V., Y. Higashimoto, Z. N. Demidenko, S. Meek, P. Graves, C. Phillips, H. Zhao, S. A. Moody, E. Appella, H. Piwnica-Worms, and A. J. Fornace, Jr. 2003. Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat. Cell Biol. 5:545-551.
3. Canned, E. J., P. J. Farrell, and A. J. Sinclair. 1996. Epstein-Barr virus exploits the normal cell pathway to regulate Rb activity during the immortalisation of primary B-cells. Oncogene 13:1413-1421.
4. Chehab, N. H., A. Malikzay, M. Appel, and T. D. Halazonetis. 2000. Chk2/ hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 14:278-288.
5. Choudhuri, T., S. Pal, T. Das, and G. Sa. 2005. Curcumin selectively induces apoptosis in deregulated cyclin D1-expressed cells at G2 phase of cell cycle in a p53-dependent manner. J. Biol. Chem. 280:20059-20068.
6. Choudhuri, T., S. C. Verma, K. Lan, and E. S. Robertson. 2006. Expression of alpha V integrin is modulated by Epstein-Barr virus nuclear antigen 3C and the metastasis suppressor Nm23-H1 through interaction with the GATA-1 and Sp1 transcription factors. Virology 351:58-72.
7. Cohen, J. I., F. Wang, J. Mannick, and E. Kieff. 1989. Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation. Proc. Natl. Acad. Sci. USA 86:9558-9562.
8. Darbon, J. M., M. Penary, N. Escalas, F. Casagrande, F. Goubin-Gramatica, C. Baudouin, and B. Ducommun. 2000. Distinct Chk2 activation pathways are triggered by genistein and DNA-damaging agents in human melanoma cells. J. Biol. Chem. 275:15363-15369.
9. Elledge, S. J. 1996. Cell cycle checkpoints: preventing an identity crisis. Science 274:1664-1672.
10. Enoch, T., and P. Nurse. 1990. Mutation of fission yeast cell cycle control genes abolishes dependence of mitosis on DNA replication. Cell 60:665-673.
11. Floettmann, J. E., K. Ward, A. B. Rickinson, and M. Rowe. 1996. Cytostatic effect of Epstein-Barr virus latent membrane protein-1 analyzed using tetracycline-regulated expression in B cell lines. Virology 223:29-40.
12. Goodwin, E. C., and D. DiMaio. 2000. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc. Natl. Acad. Sci. USA 97: 12513-12518.
13. Hirao, A., Y. Y. Kong, S. Matsuoka, A. Wakeham, J. Ruland, H. Yoshida, D. Liu, S. J. Elledge, and T. W. Mak. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824-1827.
14. Kaye, K. M., K. M. Izumi, and E. Kieff. 1993. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation. Proc. Natl. Acad. Sci. USA 90:9150-9154.
15. Kieff, E. 1996. Epstein-Barr virus and its replication, p. 2343-2395. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed., vol. 2. Lippincott-Raven, Philadelphia, PA.
16. Knight, J. S., M. A. Cotter II, and E. S. Robertson. 2001. The latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus transactivates the telomerase reverse transcriptase promoter. J. Biol. Chem. 276: 22971-22978.
17. Knight, J. S., K. Lan, C. Subramanian, and E. S. Robertson. 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.
18. Knight, J. S., and E. S. Robertson. 2004. Epstein-Barr virus nuclear antigen 3C regulates cyclin A/p27 complexes and enhances cyclin A-dependent kinase activity. J. Virol. 78:1981-1991.
19. Krauer, K. G., A. Burgess, M. Buck, J. Flanagan, T. B. Sculley, and B. Gabrielli. 2004. The EBNA-3 gene family proteins disrupt the G2/M checkpoint. Oncogene 23:1342-1353.
20. Kumagai, A., and W. G. Dunphy. 1991. The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. Cell 64:903-914.
21. Lin, J., E. Johannsen, E. Robertson, and E. Kieff. 2002. Epstein-Barr virus nuclear antigen 3C putative repression domain mediates coactivation of the LMP1 promoter with EBNA-2. J. Virol. 76:232-242.
22. Marshall, D., and C. Sample. 1995. Epstein-Barr virus nuclear antigen 3C is a transcriptional regulator. J. Virol. 69:3624-3630.
23. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
24. Nghiem, P., P. K. Park, Y. Kim, C. Vaziri, and S. L. Schreiber. 2001. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092-9097.
25. Parker, G. A., T. Crook, M. Bain, E. A. Sara, P. J. Farrell, and M. J. Allday. 1996. Epstein-Barr virus nuclear antigen (EBNA)3C is an immortalizing oncoprotein with similar properties to adenovirus E1A and papillomavirus E7. Oncogene 13:2541-2549.
26. Parker, G. A., R. Touitou, and M. J. Allday. 2000. Epstein-Barr virus EBNA3C can disrupt multiple cell cycle checkpoints and induce nuclear division divorced from cytokinesis. Oncogene 19:700-709.
27. Qiu, L., A. Burgess, D. P. Fairlie, H. Leonard, P. G. Parsons, and B. G. Gabrielli. 2000. Histone deacetylase inhibitors trigger a G2 checkpoint in normal cells that is defective in tumor cells. Mol. Biol. Cell 11:2069-2083.
28. Radkov, S. A., R. Touitou, A. Brehm, M. Rowe, M. West, T. Kouzarides, and M. J. Allday. 1999. Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription. J. Virol. 73:5688-5697.
29. Rickinson, A. B., and E. Kieff. 1996. Epstein-Barr virus. Lippincott-Raven, Philadelphia, PA.
30. Robertson, E. S., J. Lin, and E. Kieff. 1996. The amino-terminal domains of Epstein-Barr virus nuclear proteins 3A, 3B, and 3C interact with RBPJκ. J. Virol. 70:3068-3074.
31. Sinclair, A. J., M. Fenton, and S. Delikat. 1998. Interactions between Epstein-Barr virus and the cell cycle control machinery. Histol. Histopathol. 13:461-467.
32. Sinclair, A. J., I. Palmero, G. Peters, and P. J. Farrell. 1994. EBNA-2 and EBNA-LP cooperate to cause G0 to G1 transition during immortalization of resting human B lymphocytes by Epstein-Barr virus. EMBO J. 13:3321-3328.
33. Subramanian, C., M. A. Cotter II, and E. S. Robertson. 2001. Epstein-Barr virus nuclear protein EBNA-3C interacts with the human metastatic suppressor Nm23-H1: a molecular link to cancer metastasis. Nat. Med. 7:350-355.
34. Subramanian, C., S. Hasan, M. Rowe, M. Hottiger, R. Orre, and E. S. Robertson. 2002. Epstein-Barr virus nuclear antigen 3C and prothymosin alpha interact with the p300 transcriptional coactivator at the CH1 and CH3/HAT domains and cooperate in regulation of transcription and histone acetylation. J. Virol. 76:4699-4708.
35. Tomkinson, B., E. Robertson, and E. Kieff. 1993. Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation. J. Virol. 67:2014-2025.
36. Verma, S. C., K. Lan, T. Choudhuri, and E. S. Robertson. 2006. Kaposi's sarcoma-associated herpesvirus-encoded latency-associated nuclear antigen modulates K1 expression through its cis-acting elements within the terminal repeats. J. Virol. 80:3445-3458.
37. Villa, L. L. 1997. Human papillomaviruses and cervical cancer. Adv. Cancer Res. 71:321-341.
38. Wade, M., and M. J. Allday. 2000. Epstein-Barr virus suppresses a G(2)/M checkpoint activated by genotoxins. Mol. Cell. Biol. 20:1344-1360.
39. Warrener, R., H. Beamish, A. Burgess, N. J. Waterhouse, N. Giles, D. Fairlie, and B. Gabrielli. 2003. Tumor cell-selective cytotoxicity by targeting cell cycle checkpoints. FASEB J. 17:1550-1552.
40. Zhao, B., D. R. Marshall, and C. E. Sample. 1996. A conserved domain of the Epstein-Barr virus nuclear antigens 3A and 3C binds to a discrete domain of Jκ. J. Virol. 70:4228-4236.
41. Zhao, B., and C. E. Sample. 2000. Epstein-Barr virus nuclear antigen 3C activates the latent membrane protein 1 promoter in the presence of Epstein-Barr virus nuclear antigen 2 through sequences encompassing an Spi-1/Spi-B binding site. J. Virol. 74:5151-5160.