Chk1 in the DNA damage response: Conserved roles from yeasts to mammals

DNA Repair

Volumn 3, Issue 8-9, 2004, Pages 1025-1032

  Chen, Yinhuai ^a   Sanchez, Yolanda ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Cell cycle; Checkpoint; DNA damage response; Genomic integrity; Kinase; Transduction

Indexed keywords

CHECKPOINT KINASE 1; PROTEIN KINASE; UNCLASSIFIED DRUG;

CELL CYCLE S PHASE; DNA DAMAGE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENOME; GENOTOXICITY; HUMAN; INFRARED RADIATION; MAMMAL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; ULTRAVIOLET RADIATION; YEAST;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; DNA DAMAGE; DNA-BINDING PROTEINS; FUNGAL PROTEINS; HUMANS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; S PHASE; TUMOR SUPPRESSOR PROTEINS; ULTRAVIOLET RAYS;

MAMMALIA;

EID: 3242879828     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2004.03.003     Document Type: Review

References (77)

1. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature. 408(6811):2000;433-439
2. Walworth N., Davey S., Beach D. Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2. Nature. 363(6427):1993;368-371
3. Sanchez Y., et al. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science. 277(5331):1997;1497-1501
4. Fogarty P., et al. The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr. Biol. 7(6):1997;418-426
5. Kumagai A., et al. The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J. Cell. Biol. 142(6):1998;1559-1569
6. Zachos G., Rainey M.D., Gillespie D.A. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO J. 22(3):2003;713-723
7. Garvik B., Carson M., Hartwell L. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 15(11):1995;6128-6138
8. Sanchez Y., et al. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science. 286(5442):1999;1166-1171
9. Liu Q., et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/MDNA damage checkpoint. Genes Dev. 14(12):2000;1448-1459
10. Takai H., et al. Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev. 14(12):2000;1439-1447
11. Chen Z., et al. Human Chk1 expression is dispensable for somatic cell death and critical for sustaining G2 DNA damage checkpoint. Mol. Cancer Ther. 2(6):2003;543-548
12. Zhou Z., Elledge S.J. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell. 75(6):1993;1119-1127
13. Zhao X., Rothstein R. The Dun1 checkpoint kinase phosphorylates and regulates the ribonucleotide reductase inhibitor Sml1. Proc. Natl. Acad. Sci. U.S.A. 99(6):2002;3746-3751
14. K. Schollaert, J.M. Poisson, J.S. Searle, J.A. Scwanekamp, C.R. Tomlinson, Y. Sanchez, A role for Saccharomyces cerevisiae Chk1 in the response to replication blocks. Mol. Biol. Cell. in revision.
15. Boddy M.N., et al. Replication checkpoint enforced by kinases Cds1 and Chk1. Science. 280(5365):1998;909-912
16. Lindsay H.D., et al. S-phase-specific activation of Cds1 kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe. Genes Dev. 12(3):1998;382-395
17. Brondello J.M., et al. Basis for the checkpoint signal specificity that regulates Chk1 and Cds1 protein kinases. Mol. Cell. Biol. 19(6):1999;4262-4269
18. Guo Z., Dunphy W.G. Response of Xenopus Cds1 in cell-free extracts to DNA templates with double-stranded ends. Mol. Biol. Cell. 11(5):2000;1535-1546
19. Feijoo C., et al. Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J. Cell. Biol. 154(5):2001;913-923
20. Gatei M., et al. Ataxia-telangiectasia-mutated (ATM) and NBS1-dependent phosphorylation of Chk1 on Ser-317 in response to ionizing radiation. J. Biol. Chem. 278(17):2003;14806-14811
21. Matsuoka S., Huang M., Elledge S.J. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science. 282(5395):1998;1893-1897
22. Falck J., et al. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature. 410(6830):2001;842-847
23. Matsuoka S., et al. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. U.S.A. 97(19):2000;10389-10394
24. Hirao A., et al. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science. 287(5459):2000;1824-1827
25. Takai H., et al. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21(19):2002;5195-5205
26. Kim S.T., et al. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274(53):1999;37538-37543
27. Guo Z., et al. 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(21):2000;2745-2756
28. Lopez-Girona A., et al. Serine-345 is required for Rad3-dependent phosphorylation and function of checkpoint kinase Chk1 in fission yeast. Proc. Natl. Acad. Sci. U.S.A. 98(20):2001;11289-11294
29. Zhao H., Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21(13):2001;4129-4139
30. Jiang K., et al. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J. Biol. Chem. 278(27):2003;25207-25217
31. Capasso H., et al. Phosphorylation activates Chk1 and is required for checkpoint-mediated cell cycle arrest. J. Cell. Sci. 115(Pt 23):2002;4555-4564
32. Chen P., et al. The 1.7 A crystal structure of human cell cycle checkpoint kinase Chk1: implications for Chk1 regulation. Cell. 100(6):2000;681-692
33. Oe T., et al. Cytoplasmic occurrence of the Chk1/Cdc25 pathway and regulation of Chk1 in Xenopus oocytes. Dev. Biol. 229(1):2001;250-261
34. Shann Y.J., Hsu M.T. Cloning and characterization of liver-specific isoform of Chk1 gene from rat. J. Biol. Chem. 276(52):2001;48863-48870
35. Chen L., Liu T.H., Walworth N.C. Association of Chk1 with 14-3-3 proteins is stimulated by DNA damage. Genes Dev. 13(6):1999;675-685
36. Sun Z., et al. Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science. 281(5374):1998;272-274
37. Schwartz M.F., et al. Rad9 phosphorylation sites couple Rad53 to the Saccharomyces cerevisiae DNA damage checkpoint. Mol. Cell. 9(5):2002;1055-1065
38. Saka Y., et al. Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chk1. Genes Dev. 11(24):1997;3387-3400
39. Osborn A.J., Elledge S.J. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17(14):2003;1755-1767
40. Tanaka K., Russell P. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell. Biol. 3(11):2001;966-972
41. Alcasabas A.A., et al. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell. Biol. 3(11):2001;958-965
42. Kumagai A., Dunphy W.G. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell. Biol. 5(2):2003;161-165
43. Jeong S.Y., Kumagai A., Lee J., Dunphy W.G. Phosphorylated claspin interacts with a phosphate-binding site in the kinase domain of Chk1 during ATR-mediated activation. J Biol. Chem. 278:2003;46782-46788
44. Chini C.C., Chen J. Human claspin is required for replication checkpoint control. J. Biol. Chem. 278(32):2003;30057-30062
45. You Z., Kong L., Newport J. The role of single-stranded DNA and polymerase alpha in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem. 277(30):2002;27088-27093
46. Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 300(5625):2003;1542-1548
47. Kim H.S., Brill S.J. Rfc4 interacts with Rpa1 and is required for both DNA replication and DNA damage checkpoints in Saccharomyces cerevisiae. Mol. Cell. Biol. 21(11):2001;3725-3737
48. Parrilla-Castellar E.R., Karnitz L.M. Cut5 is required for the binding of Atr and DNA polymerase {alpha} to genotoxin-damaged chromatin. J. Biol. Chem. 278(46):2003;45507-45511
49. Lupardus P.J., et al. A requirement for replication in activation of the ATR-dependent DNA damage checkpoint. Genes Dev. 16(18):2002;2327-2332
50. Zou L., Liu D., Elledge S.J. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. U.S.A. 100:2003;13827-13832
51. Weiss R.S., Enoch T., Leder P. Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev. 14(15):2000;1886-1898
52. Grenon M., Gilbert C., Lowndes N.F. Checkpoint activation in response to double-strand breaks requires the Mre11Rad50/Xrs2 complex. Nat. Cell. Biol. 3(9):2001;844-847
53. Costanzo V., et al. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell. 8(1):2001;137-147
54. Stewart G.S., et al. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature. 421(6926):2003;961-966
55. Goldberg M., et al. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature. 421(6926):2003;952-956
56. Xu X., Stern D.F. NFBD1/MDC1 regulates ionizing radiation-induced focus formation by DNA checkpoint signaling and repair factors. FASEB J. 17(13):2003;1842-1848
57. Michael W.M., et al. Activation of the DNA replication checkpoint through RNA synthesis by primase. Science. 289(5487):2000;2133-2137
58. Cohen-Fix O., et al. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev. 10(24):1996;3081-3093
59. Wang H., et al. Pds1 phosphorylation in response to DNA damage is essential for its DNA damage checkpoint function. Genes Dev. 15(11):2001;1361-1372
60. Agarwal R., et al. Two distinct pathways for inhibiting pds1 ubiquitination in response to DNA damage. J. Biol. Chem. 278(45):2003;45027- 45033
61. Furnari B., et al. Cdc25 inhibited in vivo and in vitro by checkpoint kinases Cds1 and Chk1. Mol. Biol. Cell. 10(4):1999;833-845
62. Zeng Y., et al. Replication checkpoint requires phosphorylation of the phosphatase Cdc25 by Cds1 or Chk1. Nature. 395(6701):1998;507-510
63. Peng C.Y., et al. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science. 277(5331):1997;1501-1505
64. Zhao H., Watkins J.L., Piwnica-Worms H. Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc. Natl. Acad. Sci. U.S.A. 99(23):2002;14795-14800
65. Chen M.S., Ryan C.E., Piwnica-Worms H. Chk1 kinase negatively regulates mitotic function of Cdc25A phosphatase through 14-3-3 binding. Mol. Cell. Biol. 23(21):2003;7488-7497
66. Sorensen C.S., et al. Chk1 regulates the S-phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell. 3(3):2003;247-258
67. Mailand N., et al. Rapid destruction of human Cdc25A in response to DNA damage. Science. 288(5470):2000;1425-1429
68. Xiao Z., et al. Chk1 mediates S and G2 arrests through Cdc25A degradation in response to DNA-damaging agents. J. Biol. Chem. 278(24):2003;21767-21773
69. Hassepass I., Voit R., Hoffmann I. Phosphorylation at serine 75 is required for UV-mediated degradation of human Cdc25A phosphatase at the S-phase checkpoint. J. Biol. Chem. 278(32):2003;29824-29829
70. O'Connell M.J., et al. Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J. 16(3):1997;545-554
71. Raleigh J.M., O'Connell M.J. The G(2) DNA damage checkpoint targets both Wee1 and Cdc25. J. Cell. Sci. 113(Pt 10):2000;1727-1736
72. Baber-Furnari B.A., et al. Regulation of mitotic inhibitor Mik1 helps to enforce the DNA damage checkpoint. Mol. Biol. Cell. 11(1):2000;1-11
73. Shieh S.Y., et al. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14(3):2000;289-300
74. Chehab N.H., et al. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 14(3):2000;278-288
75. Jallepalli P.V., et al. The Chk2 tumor suppressor is not required for p53 responses in human cancer cells. J. Biol. Chem. 278(23):2003;20475-20479
76. Ahn J., Urist M., Prives C. Questioning the role of checkpoint kinase 2 in the p53 DNA damage response. J. Biol. Chem. 278(23):2003;20480-20489
77. Esashi F., Yanagida M. Cdc2 phosphorylation ofCrb2 is required for reestablishing cell cycle progression after the damage checkpoint. Mol. Cell. 4(2):1999;167-174