ATR-dependent phosphorylation of DNA-dependent protein kinase catalytic subunit in response to UV-induced replication stress

Molecular and Cellular Biology

Volumn 26, Issue 20, 2006, Pages 7520-7528

  Yajima, Hirohiko ^a,b   Lee, Kyung Jong ^a   Chen, Benjamin P C ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CAMPTOTHECIN; DNA DEPENDENT PROTEIN KINASE; SERINE; THREONINE;

ANIMAL CELL; ARTICLE; CELL DIVISION; CONTROLLED STUDY; DNA DOUBLE STRAND BREAK REPAIR; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME SUBUNIT; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; IONIZING RADIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RADIATION STRESS; RADIOSENSITIVITY; REPLICATION FORK; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STRESS; ULTRAVIOLET IRRADIATION;

CATALYTIC DOMAIN; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; HUMANS; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN-SERINE-THREONINE KINASES; S PHASE; TUMOR SUPPRESSOR PROTEINS;

ATAXIA;

EID: 33749611701     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00048-06     Document Type: Article

References (40)

1. Bartek, J., C. Lukas, and J. Lukas. 2004. Checking on DNA damage in S phase. Nat. Rev. Mol. Cell. Biol. 5:792-804.
2. Binz, S. K., A. M. Sheehan, and M. S. Wold. 2004. Replication protein A phosphorylation and the cellular response to DNA damage. DNA Repair (Amsterdam) 3:1015-1024.
3. Block, W. D., Y. Yu, D. Merkle, J. L. Gifford, Q. Ding, K. Meek, and S. P. Lees-Miller. 2004. Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends. Nucleic Acids Res. 32:4351-4357.
4. Boubnov, N. V., and D. T. Weaver. 1995. scid cells are deficient in Ku and replication protein A phosphorylation by the DNA-dependent protein kinase. Mol. Cell. Biol. 15:5700-5706.
5. Brush, G. S., C. W. Anderson, and T. J. Kelly. 1994. The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication. Proc. Natl. Acad. Sci. USA 91: 12520-12524.
6. Carty, M. P., M. Zernik-Kobak, S. McGrath, and K. Dixon. 1994. UV light-induced DNA synthesis arrest in HeLa cells is associated with changes in phosphorylation of human single-stranded DNA-binding protein. EMBO J. 13:2114-2123.
7. Chan, D. W., B. P. Chen, S. Prithivirajsingh, A. Kurimasa, M. D. Story, J. Qin, and D. J. Chen. 2002. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev. 16:2333-2338.
8. Chen, B. P., D. W. Chan, J. Kobayashi, S. Burma, A. Asaithamby, K. Morotomi-Yano, E. Botvinick, J. Qin, and D. J. Chen. 2005. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem. 280:14709-14715.
9. Chen, B. P., J. Kobayashi, A. Krempler, H. Yajima, N. Uematsu, M. Lobrich, and D. J. Chen. ATM phosphorylates DNA-PKcs at T2609 cluster of phosphorylation sites after IR. Submitted for publication.
10. Ding, Q., Y. V. Reddy, W. Wang, T. Woods, P. Douglas, D. A. Ramsden, S. P. Lees-Miller, and K. Meek. 2003. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol. Cell. Biol. 23: 5836-5848.
11. Douglas, P., G. P. Sapkota, N. Morrice, Y. Yu, A. A. Goodarzi, D. Merkle, K. Meek, D. R. Alessi, and S. P. Lees-Miller. 2002. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem. J. 368:243-251.
12. Elbashir, S. M., J. Harborth, W. Lendeckel, A. Yalcin, K. Weber, and T. Tuschl. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
13. Garinis, G. A., J. R. Mitchell, M. J. Moorhouse, K. Hanada, H. de Waard, D. Vandeputte, J. Jans, K. Brand, M. Smid, P. J. van der Spek, J. H. Hoeijmakers, R. Kanaar, and G. T. van der Horst. 2005. Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks. EMBO J. 24:3952-3962.
14. Gottifredi, V., and C. Prives. 2005. The S phase checkpoint: when the crowd meets at the fork. Semin. Cell Dev. Biol. 16:355-368.
15. Hall-Jackson, C. A., D. A. Cross, N. Morrice, and C. Smythe. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18:6707-6713.
16. Katsumi, S., N. Kobayashi, K. Imoto, A. Nakagawa, Y. Yamashina, T. Muramatsu, T. Shirai, S. Miyagawa, S. Sugiura, F. Hanaoka, T. Matsunaga, O. Nikaido, and T. Mori. 2001. In situ visualization of ultraviolet-light-induced DNA damage repair in locally irradiated human fibroblasts. J. Investig. Dermatol. 117:1156-1161.
17. 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.
18. Kurimasa, A., S. Kumano, N. V. Boubnov, M. D. Story, C. S. Tung, S. R. Peterson, and D. J. Chen. 1999. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol. Cell. Biol. 19:3877-3884.
19. Lee, K. J., X. Dong, J. Wang, Y. Takeda, and W. S. Dynan. 2002. Identification of human autoantibodies to the DNA ligase IV/XRCC4 complex and mapping of an autoimmune epitope to a potential regulatory region. J. Immunol. 169:3413-3421.
20. Lou, Z., B. P. Chen, A. Asaithamby, K. Minter-Dykhouse, D. J. Chen, and J. Chen. 2004. MDC1 regulates DNA-PK autophosphorylation in response to DNA damage. J. Biol. Chem. 279:46359-46362.
21. Ma, Y., U. Pannicke, H. Lu, D. Niewolik, K. Schwarz, and M. R. Lieber. 2005. The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J. Biol. Chem. 280:33839-33846.
22. Mori, T., M. Nakane, T. Hattori, T. Matsunaga, M. Ihara, and O. Nikaido. 1991. Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4) photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem. Photobiol. 54:225-232.
23. Mullenders, L. H., and M. Berneburg. 2001. Photoimmunology and nucleotide excision repair: impact of transcription coupled and global genome excision repair. J. Photochem. Photobiol. B 65:97-100.
24. Muller, C., P. Calsou, P. Frit, C. Cayrol, T. Carter, and B. Salles. 1998. UV sensitivity and impaired nucleotide excision repair in DNA-dependent protein kinase mutant cells. Nucleic Acids Res. 26:1382-1389.
25. 1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98:9092-9097.
26. Nghiem, P., P. K. Park, Y. Kim, B. N. Desai, and S. L. Schreiber. 2002. ATR is not required for p53 activation but synergizes with p53 in the replication checkpoint. J. Biol. Chem. 277:4428-4434.
27. Park, J. S., S. J. Park, X. Peng, M. Wang, M. A. Yu, and S. H. Lee. 1999. Involvement of DNA-dependent protein kinase in UV-induced replication arrest. J. Biol. Chem. 274:32520-32527.
28. 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.
29. Sarkaria, J. N., R. S. Tibbetts, E. C. Busby, A. P. Kennedy, D. E. Hill, and R. T. Abraham. 1998. Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res. 58:4375-4382.
30. Shechter, D., V. Costanzo, and J. Gautier. 2004. Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Repair (Amsterdam) 3:901-908.
31. Shiloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155-168.
32. Soubeyrand, S., L. Pope, B. Pakuts, and R. J. Hache. 2003. Threonines 2638/2647 in DNA-PK are essential for cellular resistance to ionizing radiation. Cancer Res. 63:1198-1201.
33. Thoma, F. 1999. Light and dark in chromatin repair: repair of UV-induced DNA lesions by photolyase and nucleotide excision repair. EMBO J. 18: 6585-6598.
34. Tibbetts, R. S., K. M. Brumbaugh, J. M. Williams, J. N. Sarkaria, W. A. Cliby, S. Y. Shieh, Y. Taya, C. Prives, and R. T. Abraham. 1999. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13:152-157.
35. Traven, A., and J. Heierhorst. 2005. SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays 27:397-407.
36. Wang, Y., X. Y. Zhou, H. Wang, M. S. Huq, and G. Iliakis. 1999. Roles of replication protein A and DNA-dependent protein kinase in the regulation of DNA replication following DNA damage. J. Biol. Chem. 274:22060-22064.
37. Ward, I. M., and J. Chen. 2001. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276:47759-47762.
38. Ward, I. M., K. Minn, and J. Chen. 2004. UV-induced ataxia- telangiectasia-mutated and Rad3-related (ATR) activation requires replication stress. J. Biol. Chem. 279:9677-9680.
39. Weterings, E., N. S. Verkaik, H. T. Bruggenwirth, J. H. Hoeijmakers, and D. C. van Gent. 2003. The role of DNA dependent protein kinase in synapsis of DNA ends. Nucleic Acids Res. 31:7238-7246.
40. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.