Absence of BLM leads to accumulation of chromosomal DNA breaks during both unperturbed and disrupted S phases

Journal of Cell Biology

Volumn 165, Issue 6, 2004, Pages 801-812

  Li, Wenhui ^a   Kim, Soo Mi ^a   Lee, Joon ^a   Dunphy, William G ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

ATR; DNA damage; DNA replication; Rad17; RecQ helicase

Indexed keywords

BLM PROTEIN; CLASPIN; PROTEIN; TOPOISOMERASE IIIALPHA; UNCLASSIFIED DRUG; XATR PROTEIN; XRAD17 PROTEIN;

ANIMAL CELL; ARTICLE; CANCER SUSCEPTIBILITY; CELL CYCLE S PHASE; CHROMOSOME; CHROMOSOME ABERRATION; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; GENOME; GENOMIC INSTABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SISTER CHROMATID EXCHANGE; XENOPUS;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BLOOM SYNDROME; CELL NUCLEUS; CHROMATIN; DNA DAMAGE; DNA HELICASES; FEMALE; HUMANS; MALE; METHIONINE; OVUM; S PHASE; SPERMATOZOA; XENOPUS;

ANIMALIA;

EID: 3042597013     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200402095     Document Type: Article

References (44)

1. Ababou, M., S. Dutertre, Y. Lecluse, R. Onclercq, B. Chatton, and M. Amor-Gueret. 2000. ATM-dependent phosphorylation and accumulation of endogenous BLM protein in response to ionizing radiation. Oncogene. 19: 5955-5963.
2. Abraham, R.T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
3. Adams, M.D., M. McVey, and J.J. Sekelsky. 2003. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science. 299: 265-267.
4. Bachrati, C.Z., and I.D. Hickson. 2003. RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J. 374:577-606.
5. Bartek, J., J. Falck, and J. Lukas. 2001. CHK2 kinase-a busy messenger. Nat. Rev. Mol. Cell Biol. 2:877-886.
6. Beamish, H., P. Kedar, H. Kaneko, P. Chen, T. Fukao, C. Peng, S. Beresten, N. Gueven, D. Purdie, S. Lees-Miller, et al. 2002. Functional link between BLM defective in Bloom's syndrome and the ataxia-telangiectasia-mutated protein, ATM. J. Biol. Chem. 277:30515-30523.
7. Casper, A.M., P. Nghiem, M.F. Arlt, and T.W. Glover. 2002. ATR regulates fragile site stability. Cell. 111:779-789.
8. Cobb, J.A., L. Bjergbaek, K. Shimada, C. Frei, and S.M. Gasser. 2003. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22:4325-4336.
9. Costanzo, V., K. Robertson, M. Bibikova, E. Kim, D. Grieco, M. Gottesman, D. Carroll, and J. Gautier. 2001. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell. 8:137-147.
10. Davies, S.L., P.S. North, A. Dart, N.D. Lakin, and I.D. Hickson. 2004. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24:1279-1291.
11. Duno, M., B. Thomsen, O. Westergaard, L. Krejci, and C. Bendixen. 2000. Genetic analysis of the Saccharomyces cerevisiae Sgs1 helicase defines an essential function for the Sgs1-Top3 complex in the absence of SRS2 or TOP1. Mol. Gen. Genet. 264:89-97.
12. Enomoto, T. 2001. Functions of RecQ family helicases: possible involvement of Bloom's and Werner's syndrome gene products in guarding genome integrity during DNA replication. J. Biochem. (Tokyo). 129:501-507.
13. Franchitto, A., and P. Pichierri. 2002. Bloom's syndrome protein is required for correct relocalization of RAD50/MRE11/NBs1 complex after replication fork arrest. J. Cell Biol. 157:19-30.
14. Frei, C., and S.M. Gasser. 2000. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev. 14:81-96.
15. Guo, Z., and W.G. Dunphy. 2000. Response of Xenopus Cds1 in cell-free extracts to DNA templates with double-stranded ends. Mol. Biol. Cell. 11:1535-1546.
16. Guo, Z., A. Kumagai, S.X. Wang, and W.G. Dunphy. 2000. Requirement for Air 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.
17. Hekmat-Nejad, M., Z. You, M.C. Yee, J.W. Newport, and K.A. Cimprich. 2000. Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol. 10:1565-1573.
18. Hu, P., S.F. Beresten, A.J. van Brabant, T.Z. Ye, P.P. Pandolfi, F.B. Johnson, L. Guarente, and N.A. Ellis. 2001. Evidence for BLM and topoisomerase IIIα interaction in genomic stability. Hum. Mol. Genet. 10:1287-1298.
19. Imamura, O., and J.L. Campbell. 2003. The human Bloom syndrome gene suppresses the DNA replication and repair defects of yeast dna2 mutants. Proc. Natl. Acad. Sci. USA. 100:8193-8198.
20. Imamura, O., K. Fujita, A. Shimamoto, H. Tanabe, S. Takeda, Y. Furuichi, and T. Matsumoto. 2001. Bloom helicase is involved in DNA surveillance in early S phase in vertebrate cells. Oncogene. 20:1143-1151.
21. Johnson, F.B., D.B. Lombard, N.F. Neff, M.A. Mastrangelo, W. Dewolf, N.A. Ellis, R.A. Marciniak, Y. Yin, R. Jaenisch, and L. Guarente. 2000. Association of the Bloom syndrome protein with topoisomerase IIIα in somatic and meiotic cells. Cancer Res. 60:1162-1167.
22. 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.
23. Kobayashi, T., S. Tada, T. Tsuyama, H. Murofushi, M. Seki, and T. Enomoto. 2002. Focus-formation of replication protein A, activation of checkpoint system and DNA repair synthesis induced by DNA double-strand breaks in Xenopus egg extract. J. Cell Sci. 115:3159-3169.
24. Kumagai, A., and W.G. Dunphy. 2000. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell. 6:839-849.
25. Kumagai, A., and W.G. Dunphy. 2003. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell Biol. 5:161-165.
26. Kumagai, A., Z. Guo, K.H. Emami, S.X. Wang, and W.G. Dunphy. 1998. The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J. Cell Biol. 142:1559-1569.
27. 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.
28. Liao, S., J. Graham, and H. Yan. 2000. The function of Xenopus Bloom's syndrome protein homolog (xBLM) in DNA replication. Genes Dev. 14:2570-2575.
29. Liu, Q., S. Guntuku, X.S. Cui, S. Matsuoka, D. Cortez, K. Tamai, G. Luo, S. Carattini-Rivera, F. DeMayo, A. Bradley, et al. 2000. Chk1 is an essential kinase that is regulated by Atr and required for the G2/M DNA damage checkpoint. Genes Dev. 14:1448-1459.
30. 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.
31. McGarry, T.J., and M.W. Kirschner. 1998. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell. 93:1043-1053.
32. Melo, J., and D. Toczyski. 2002. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14:237-245.
33. Myung, K., and R.D. Kolodner. 2002. Suppression of genome instability by redundant S-phase checkpoint pathways in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 99:4500-4507.
34. O'Connell, M.J., N.C. Walworth, and A.M. Carr. 2000. The G2-phase DNA-damage checkpoint. Trends Cell Biol. 10:296-303.
35. 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.
36. Rassool, F.V., P.S. North, G.J. Mufti, and I.D. Hickson. 2003. Constitutive DNA damage is linked to DNA replication abnormalities in Bloom's syndrome cells. Oncogene. 22:8749-8757.
37. Sharma, S., J.A. Sommers, L. Wu, V.A. Bohr, I.D. Hickson, and R.M. Brosh, Jr. 2004. Stimulation of flap endonuclease-1 by the Bloom's syndrome protein. J. Biol. Chem. 279:9847-9856.
38. 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.
39. Walter, J., and J. Newport. 2000. Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase α. Mol. Cell. 5:617-627.
40. Wang, Y., D. Cortez, P. Yazdi, N. Neff, S.J. Elledge, and J. Qin. 2000. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:927-939.
41. Wu, L., and I.D. Hickson. 2002. The Bloom's syndrome helicase stimulates the activity of human topoisomerase IIIα. Nucleic Acids Res. 30:4823-4829.
42. Wu, L., S.L. Davies, P.S. North, H. Goulaouic, J.F. Riou, H. Turley, K.C. Gatter, and I.D. Hickson. 2000. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275:9636-9644.
43. Yanow, S.K., D.A. Gold, H.Y. Yoo, and W.G. Dunphy. 2003. Xenopus Drf1, a regulator of Cdc7, displays checkpoint-dependent accumulation on chromatin during an S-phase arrest. J. Biol. Chem. 278:41083-41092.
44. You, Z., L. Kong, and J. Newport. 2002. The role of single-stranded DNA and polymerase α in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem. 277:27088-27093.