Induction and utilization of an ATM signaling pathway by polyomavirus

Journal of Virology

Volumn 79, Issue 20, 2005, Pages 13007-13017

  Dahl, Jean ^a   You, John ^a   Benjamin, Thomas L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CAFFEINE; CELL DNA; COHESIN; PROTEIN P53; RETINOBLASTOMA PROTEIN; VIRUS DNA;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FIBROBLAST; GENE ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; VIRUS INFECTION; VIRUS REPLICATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BALB 3T3 CELLS; CELL CYCLE; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; MICE; POLYOMAVIRUS; POLYOMAVIRUS INFECTIONS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; TUMOR VIRUS INFECTIONS;

ATAXIA TELANGIECTASIA; POLYOMAVIRUS;

EID: 26444433215     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.20.13007-13017.2005     Document Type: Article

References (56)

1. Ahn, J. Y., J. K. Schwarz, H. Piwnica-Worms, and C. E. Canman. 2000. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 60:5934-5936.
2. Atencio, I. A., F. F. Shadan, X. J. Zhou, N. D. Vaziri, and L. P. Villarreal. 1993. Adult mouse kidneys become permissive to acute polyomavirus infection and reactivate persistent infections in response to cellular damage and regeneration. J. Virol. 67:1424-1432.
3. Berkovich, E., and D. Ginsberg. 2003. ATM is a target for positive regulation by E2F-1. Oncogene 22:161-167.
4. Bracken, A. P., M. Ciro, A. Cocito, and K. Helin. 2004. E2F target genes: unraveling the biology. Trends Biochem. Sci. 29:409-417.
5. Carson, C. T., R. A. Schwartz, T. H. Stracker, C. E. Lilley, D. V. Lee, and M. D. Weitzman. 2003. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22:6610-6620.
6. Chang, T. H., F. A. Ray, D. A. Thompson, and R. Schlegel. 1997. Disregulation of mitotic checkpoints and regulatory proteins following acute expression of SV40 large T antigen in diploid human cells. Oncogene 14:2383-2393.
7. Chatterjee, A., B. J. Bockus, O. V. Gjorup, and B. S. Schaffhausen. 1997. Phosphorylation sites in polyomavirus large T antigen that regulate its function in viral, but not cellular, DNA synthesis. J. Virol. 71:6472-6478.
8. Dahl, J., A. Jurczak, L. A. Cheng, D. C. Baker, and T. L. Benjamin. 1998. Evidence of a role for phosphatidylinositol 3-kinase activation in the blocking of apoptosis by polyomavirus middle T antigen. J. Virol. 72:3221-3226.
9. Daniel, R., J. G. Greger, R. A. Katz, K. D. Taganov, X. Wu, J. C. Kappes, and A. M. Skalka. 2004. Evidence that stable retroviral transduction and cell survival following DNA integration depend on components of the nonhomologous end joining repair pathway. J. Virol. 78:8573-8581.
10. Daniel, R., G. Kao, K. Taganov, J. G. Greger, O. Favorova, G. Merkel, T. J. Yen, R. A. Katz, and A. M. Skalka. 2003. Evidence that the retroviral DNA integration process triggers an ATR-dependent DNA damage response. Proc. Natl. Acad. Sci. USA 100:4778-4783.
11. Davis, F. M., T. Y. Tsao, S. K. Fowler, and P. N. Rao. 1983. Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA 80:2926-2930.
12. Dey, D., J. Dahl, S. Cho, and T. L. Benjamin. 2002. Induction and bypass of p53 during productive infection by polyomavirus. J. Virol. 76:9526-9532.
13. Dey, D. C., R. P. Bronson, J. Dahl, J. P. Carroll, and T. L. Benjamin. 2000. Accelerated development of polyoma tumors and embryonic lethality: different effects of p53 loss on related mouse backgrounds. Cell Growth Differ. 11:231-237.
14. Digweed, M., I. Demuth, S. Rothe, R. Scholz, A. Jordan, C. Grotzinger, D. Schindler, M. Grompe, and K. Sperling. 2002. SV40 large T-antigen disturbs the formation of nuclear DNA-repair foci containing MRE11. Oncogene 21:4873-4878.
15. Doherty, J., and R. Freund. 1997. Polyomavirus large T antigen overcomes p53 dependent growth arrest. Oncogene 14:1923-1931.
16. Feunteun, J., L. Sompayrac, M. Fluck, and T. L. Benjamin. 1976. Localization of gene functions in polyoma virus DNA. Proc. Natl. Acad. Sci. USA 73:4169-4173.
17. Freund, R., P. H. Bauer, H. A. Crissman, E. M. Bradbury, and T. L. Benjamin. 1994. Host range and cell cycle activation properties of polyomavirus large T-antigen mutants defective in pRB binding. J. Virol. 68:7227-7234.
18. Garg, R., S. Callens, D. S. Lim, C. E. Canman, M. B. Kastan, and B. Xu. 2004. Chromatin association of rad17 is required for an ataxia telangiectasia and rad-related kinase-mediated S-phase checkpoint in response to low-dose ultraviolet radiation. Mol. Cancer Res. 2:362-369.
19. Gerace, L., and G. Blobel. 1980. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19:277-287.
20. Gilbert, J. M., and T. L. Benjamin. 2000. Early steps of polyomavirus entry into cells. J. Virol. 74:8582-8588.
21. Goldman, E., and T. L. Benjamin. 1975. Analysis of host range of nontransforming polyoma virus mutants. Virology 66:372-384.
22. Hirt, B. 1967. Selective extraction of polyoma DNA from infected mouse cell cultures. J. Mol. Biol. 26:365-369.
23. Kastan, M. B. 2001. Cell cycle. Checking two steps. Nature 410:766-767.
24. Kim, S. T., D. S. Lim, C. E. Canman, and M. B. Kastan. 1999. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274:37538-37543.
25. Kim, S. T., B. Xu, and M. B. Kastan. 2002. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 16:560-570.
26. Kitagawa, R., C. J. Bakkenist, P. J. McKinnon, and M. B. Kastan. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18:1423-1438.
27. Kudoh, A., M. Fujita, L. Zhang, N. Shirata, T. Daikoku, Y. Sugaya, H. Isomura, Y. Nishiyama, and T. Tsurumi. 2005. Epstein-Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phase-like cellular environment. J. Biol. Chem. 280:8156-8163.
28. Lavialle, C., A. G. Morris, H. G. Suaarez, S. Estrade, J. Stevenet, and R. Cassingena. 1977. Simian virus 40-Chinese hamster kidney cell interaction. IV. Enhanced virus replication in infected cells upon treatment with mitomycin C. J. Gen. Virol. 36:137-149.
29. Lehman, J. M., J. Laffin, and T. D. Friedrich. 1994. DNA content distribution of mouse cells following infection with polyoma virus. Cytometry 16:138-143.
30. Lehman, J. M., J. Laffin, J. W. Jacobberger, and D. Fogleman. 1988. Analysis of simian virus 40 infection of CV-1 cells by quantitative two-color fluorescence with flow cytometry. Cytometry 9:52-59.
31. Lehmann, A. R. 2005. The role of SMC proteins in the responses to DNA damage. DNA Repair (Amsterdam) 4:309-314.
32. Li, D., Y. Tian, Y. Ma, and T. Benjamin. 2004. p150(Sal2) is a p53-independent regulator of p21(WAF1/CIP). Mol. Cell. Biol. 24:3885-3893.
33. Liao, M. J., C. Yin, C. Barlow, A. Wynshaw-Boris, and T. van Dyke. 1999. Atm is dispensable for p53 apoptosis and tumor suppression triggered by cell cycle dysfunction. Mol. Cell. Biol. 19:3095-3102.
34. Lilley, C. E., C. T. Carson, A. R. Muotri, F. H. Gage, and M. D. Weitzman. 2005. DNA repair proteins affect the lifecycle of herpes simplex virus I. Proc. Natl. Acad. Sci. USA 102:5844-5849.
35. Lin, W. C., F. T. Lin, and J. R. Nevins. 2001. Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev. 15:1833-1844.
36. Mezzina, M., H. G. Suarez, R. Cassingena, and A. Sarasin. 1982. Increased activity of polynucleotide ligase in 5-iodo-2′-deoxyuridine and mitomycin C-pretreated simian virus 40 (SV40)-infected monkey kidney cells. Nucleic Acids Res. 10:5073-5084.
37. Miao, H., J. A. Seiler, and W. C. Burhans. 2003. Regulation of cellular and SV40 virus origins of replication by Chk1-dependent intrinsic and UVC radiation-induced checkpoints. J. Biol. Chem. 278:4295-4304.
38. Okubo, E., J. M. Lehman, and T. D. Friedrich. 2003. Negative regulation of mitotic promoting factor by the checkpoint kinase chk1 in simian virus 40 lytic infection. J. Virol. 77:1257-1267.
39. Osborn, A. J., S. J. Elledge, and L. Zou. 2002. Checking on the fork: the DNA-replication stress-response pathway. Trends Cell Biol. 12:509-516.
40. Roshal, M., B. Kim, Y. Zhu, P. Nghiem, and V. Planelles. 2003. Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J. Biol. Chem. 278:25879-25886.
41. Sarkaria, J. N., E. C. Busby, R. S. Tibbetts, P. Roos, Y. Taya, L. M. Karnitz, and R. T. Abraham. 1999. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59:4375-4382.
42. Schar, P., M. Fasi, and R. Jessberger. 2004. SMC1 coordinates DNA double-strand break repair pathways. Nucleic Acids Res. 32:3921-3929.
43. Schlegel, R., and T. L. Benjamin. 1978. Cellular alterations dependent upon the polyoma virus Hr-t function: separation of mitogenic from transforming capacities. Cell 14:587-599.
44. Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155-168.
45. Silver, J. B., B. S. Schaffhausen, and T. L. Benjamin. 1978. Tumor antigens induced by nontransforming mutants of polyoma virus. Cell 15:485-496.
46. Simmons, D. 2000. SV40 large T antigen-functions in DNA replication and transformation. Adv. Virus Res. 55:75-134.
47. Spink, K. M., and M. M. Fluck. 2003. Polyomavirus hr-t mutant-specific induction of a G2/M cell-cycle arrest that is not overcome by the expression of middle T and/or small T. Virology 307:191-203.
48. Weaver, D. T., S. C. Fields-Berry, and M. L. DePamphilis. 1985. The termination region for SV40 DNA replication directs the mode of separation for the two sibling molecules. Cell 41:565-575.
49. Westphal, C. H., C. Schmaltz, S. Rowan, A. Elson, D. E. Fisher, and P. Leder. 1997. Genetic interactions between atm and p53 influence cellular proliferation and irradiation-induced cell cycle checkpoints. Cancer Res. 57:1664-1667.
50. Winocour, E. 1963. Purification of polyoma virus. Virology 19:158-168.
51. Wu, X., D. Avni, T. Chiba, F. Van, Q. Zhao, Y. Lin, H. Heng, and D. Livingston. 2004. SV40 T antigen interacts with Nbs1 to disrupt DNA replication control. Genes Dev. 18:1305-1316.
52. Xiong, Y., G. J. Hannon, H. Zhang, D. Casso, R. Kobayashi, and D. Beach. 1993. p21 is a universal inhibitor of cyclin kinases. Nature 366:701-704.
53. Yazdi, P. T., Y. Wang, S. Zhao, N. Patel, E. Y. Lee, and J. Qin. 2002. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev. 16:571-582.
54. Zhao, H., and H. Piwnica-Worms. 2001. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21:4129-4139.
55. Zhou, B. B., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
56. Ziv, Y., S. Banin, D. S. Lim, C. E. Canman, M. B. Kastan, and Y. Shiloh. 2000. Expression and assay of recombinant ATM. Methods Mol. Biol. 99:99-108.