TopBP1 and DNA polymerase-α directly recruit the 9-1-1 complex to stalled DNA replication forks

Journal of Cell Biology

Volumn 184, Issue 6, 2009, Pages 793-804

  Yan, Shan ^a   Michael, W Matthew ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE ALPHA; PROTEIN HUS1; PROTEIN RAD1; PROTEIN RAD9; PROTEIN TOPBP1; UNCLASSIFIED DRUG; ATM PROTEIN; ATR PROTEIN, XENOPUS; ATRIP PROTEIN, XENOPUS; CARRIER PROTEIN; DNA; DNA DIRECTED DNA POLYMERASE BETA; HUS1 PROTEIN, XENOPUS; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; PROTEIN SERINE THREONINE KINASE; RAD1 PROTEIN, XENOPUS; TOPBP1 PROTEIN, XENOPUS; TUMOR SUPPRESSOR PROTEIN; XENOPUS PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPLICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; XENOPUS LAEVIS; ANIMAL; CHROMATIN; GENETICS; METABOLISM; MOLECULAR CLONING; PHYSIOLOGICAL STRESS; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TIME;

ATAXIA TELANGIECTASIA; XENOPUS LAEVIS;

ANIMALS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CLONING, MOLECULAR; DNA; DNA POLYMERASE I; DNA REPLICATION; DNA-BINDING PROTEINS; MULTIPROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS; XENOPUS LAEVIS; XENOPUS PROTEINS;

EID: 64049105391     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200810185     Document Type: Article

References (50)

1. Ball, H.L., J.S. Myers, and D. Cortez. 2005. ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chkl phosphorylation. Mol. Biol. Cell. 16:2372-2381.
2. Ball, H.L., M.R. Ehrhardt, D.A. Mordes, G.G. Glick, W.J. Chazin, and D. Cortez. 2007. Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol. 27:3367-3377.
3. Bermudez, V.P., L.A. Lindsey-Boltz, A.J. Cesare, Y. Maniwa, J.D. Griffith, J. Hurwitz, and A. Sancar. 2003. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc. Natl. Acad. Sci. USA. 100:1633-1638.
4. Burrows, A.E., and S.J. Elledge. 2008. How ATR turns on: TopBP1 goes on ATRIP with ATR. Genes Dev. 22:1416-1421.
5. Byun, T.S., M. Pacek, M.C. Yee, J.C. Walter, and K.A. Cimprich. 2005. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19:1040-1052.
6. Chen, Y., and Y. Sanchez. 2004. Chk1 in the DNA damage response: conserved roles from yeasts to mammals. DNA Repair (Amst.). 3:1025-1032.
7. Cimprich, K.A., and D. Cortez. 2008. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9:616-627.
8. Cortez, D., S. Guntuku, J. Qin, and S.J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science. 294:1713-1716.
9. Delacroix, S., J.M. Wagner, M. Kobayashi, K. Yamamoto, and L.M. Karnitz. 2007. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev. 21:1472-1477.
10. Ellison, V., and B. Stillman . 2003. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol. 1:e33.
11. Errico, A., V. Costanzo, and T. Hunt. 2007. Tipin is required for stalled replication forks to resume DNA replication after removal of aphidicolin in Xenopus egg extracts. Proc. Natl. Acad. Sci. USA. 104:14929-14934.
12. Furuya, K., M. Poitelea, L. Guo, T. Caspari, and A.M. Carr. 2004 . Chk1 activation requires Rad9 S/TQ-site phosphorylation to promote association with C-terminal BRCT domains of Rad4TOPBP1. Genes Dev. 18:1154-1164.
13. Garcia, V., K. Furuya, and A.M. Carr. 2005. Identification and functional analysis of TopBP1 and its homologs. DNA Repair (Amst.). 4:1227-1239.
14. Guo, Z., A. Kumagai, S.X. Wang, and W.G. Dunphy. 2000. Requirement for Atr in phosphorylation of Chk1 and cell cycle regulation in response to DNA replication blocks and UV-damaged DNA in Xenopus egg extracts. Genes Dev. 14:2745-2756.
15. Hashimoto, Y., and H. Takisawa.2003. Xenopus Cut5 is essential for a CDK-dependent process in the initiation of DNA replication. EMBO J. 22:2526-2535.
16. Hashimoto, Y., T. Tsujimura, A. Sugino, and H. Takisawa. 2006. The phosphory-lated C-terminal domain of Xenopus Cut5 directly mediates ATR-dependent activation of Chk1. Genes Cells. 11:993-1007.
17. Hubscher, U., G. Maga, and S. Spadari. 2002. Eukaryotic DNA polymerases. Annu. Rev. Biochem. 71:133-163.
18. Jones, R.E., J.R. Chapman, C. Puligilla, J.M. Murray, A.M. Car, C.C. Ford, and H.D. Lindsay. 2003. XRad17 is required for the activation of XChk1 but not XCds1 during checkpoint signaling in Xenopus. Mol. Biol. Cell. 14:3898-3910.
19. Kanoh, Y., K. Tamai, and K. Shirahige. 2006. Different requirements for the association of ATR-ATRIP and 9-1-1 to the stalled replication forks. Gene. 377:88-95.
20. Kondo, T., T. Wakayama, T. Naiki, K. Matsumoto, and K. Sugimoto. 2001. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science. 294:867-870.
21. Kumagai, A., J. Lee, H.Y. Yoo, and W.G. Dunphy. 2006 . TopBP1 activates the ATR-ATRIP complex. Cell. 124:943-955.
22. Lee, J., A. Kumagai, and W.G. Dunphy. 2003. Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol. Cell. 11:329-340.
23. Lee, J., A. Kumagai, and W.G. Dunphy. 2007 . The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. J. Biol. Chem. 282:28036-28044.
24. Lopes, M., M. Foiani, and J.M. Sogo. 2006 . Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell. 21:15-27.
25. Luciani, M.G., M. Oehlmann, and J.J. Blow. 2004. Characterization of a novel ATR-dependent, Chk1-independent, intra-S-phase checkpoint that suppresses initiation of replication in Xenopus. J. Cell Sci. 117:6019-6030.
26. Lupardus, P.J., and K.A. Cimprich. 2006. Phosphorylation of Xenopus Rad1 and Hus1 defines a readout for ATR activation that is independent of Claspin and the Rad9 carboxy terminus. Mol. Biol. Cell. 17:1559-1569.
27. Lupardus, P.J., T. Byun, M.C. Yee, M. Hekmat-Nejad, and K.A. Cimprich . 2002. A requirement for replication in activation of the ATR-dependent DNA damage checkpoint. Genes Dev. 16:2327-2332.
28. MacDougall, C.A., T.S. Byun, C. Van, M.C. Yee, and K.A. Cimprich. 2007. The structural determinants of checkpoint activation. Genes Dev. 21:898-903.
29. Majka, J., S.K. Binz, M.S. Wold, and P.M. Burgers. 2006. Replication protein A directs loading of the DNA damage checkpoint clamp to 5′ -DNA junctions. J. Biol. Chem. 281:27855-27861.
30. Melo, J.A., J. Cohen, and D.P. Toczyski. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15:2809-2821.
31. Michael, W.M., R. Ott, E. Fanning, and J. Newport. 2000. Activation of the DNA replication checkpoint through RNA synthesis by primase. Science. 289:2133-2137.
32. Mimura, S., T. Masuda, T. Matsui, and H. Takisawa . 2000 . Central role for cdc45 in establishing an initiation complex of DNA replication in Xenopus eggextracts. Genes Cells. 5:439-452.
33. Mordes, D.A., G.G. Glick, R. Zhao, and D. Cortez . 2008 . TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev. 22:1478-1489.
34. Namiki, Y., and L. Zou . 2006 . ATRIP associates with replication protein A-coated ssDNA through multiple interactions. Proc. Natl. Acad. Sci. USA. 103:580-585.
35. Parrilla-Castellar, E.R., and L.M. Karnitz. 2003. Cut5 is required for the binding of Atr and DNA polymerase alpha to genotoxin-damaged chromatin. J. Biol. Chem. 278:45507-45511.
36. Parrilla-Castellar, E.R., S.J. Arlander, and L. Karnitz. 2004. Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair (Amst.). 3:1009-1014.
37. Paulsen, R.D., and K.A. Cimprich. 2007. The ATR pathway: fine-tuning the fork. DNA Repair (Amst.). 6:953-966.
38. Rowles, A., S. Tada, and J.J. Blow. 1999. Changes in association of the Xenopus origin recognition complex with chromatin on licensing of replication origins.J. CellSci. 112:2011-2018.
39. Stokes, M.P., R. Van Hatten, H.D. Lindsay, and W.M. Michael. 2002. DNA replication is required for the checkpoint response to damaged DNA in Xenopus egg extracts. J. Cell Biol. 158:863-872.
40. Trenz, K., E. Smith, S. Smith, and V. Costanzo. 2006. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25:1764-1774.
41. Unsal-Kacmaz, K., and A. Sancar. 2004. Quaternary structure of ATR and effects of ATRIP and replication protein A on its DNA binding and kinase activities. Mol. Cell. Biol. 24:1292-1300.
42. Van Hatten, R.A., A.V. Tutter, A.H. Holway, A.M. Khederian, J.C. Walter, and W.M. Michael. 2002. The Xenopus Xmus101 protein is required for the recruitment of Cdc45 to origins of DNA replication. J. Cell Biol. 159:541-547.
43. Walter, J., and J. Newport. 1999. The use of Xenopus laevis interphaseegg extractsto study genomic DNA replication. In Eukaryotic DNA Replication: A Practical Approach. S. Cotterill, editor. Oxford University Press, Oxford. 201-222.
44. Yan, S., H.D. Lindsay, and W.M. Michael. 2006. Direct requirement for Xmus101 in ATR-mediated phosphorylation of Claspin bound Chk1 during checkpoint signaling. J. Cell Biol. 173:181-186.
45. You, Z., L. Kong, and J. Newport. 2002. The role of single-stranded DNA and polymerase alpha in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem. 277:27088-27093.
46. Zhang, Y.W., T. Hunter, and R.T. Abraham . 2006 . Turning the replication checkpoint on and off. Cell Cycle. 5:125-128.
47. Zhu, W., C. Ukomadu, S. Jha, T. Senga, S.K. Dhar, J.A. Wohlschlegel, L.K. Nutt, S. Kornbluth, and A. Dutta. 2007. Mcm10 and And-1/CTF4 recruit DNA polymerase alpha to chromatin for initiation of DNA replication. Genes Dev. 21:2288-2299.
48. Zou, L., and S.J. Elledge . 2003 . Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 300:1542-1548.
49. Zou, L., D. Cortez, and S.J. Elledge. 2002. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev.16:198-208.
50. Zou, L., D. Liu, and S.J. Elledge. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. USA. 100:13827-13832.