Checkpoint kinase 1 in DNA damage response and cell cycle regulation

Cellular and Molecular Life Sciences

Volumn 70, Issue 21, 2013, Pages 4009-4021

  Patil, Mallikarjun ^a   Pabla, Navjotsingh ^a,c   Dong, Zheng ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Cell cycle; Checkpoint; Chk1; DNA damage

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 1 INHIBITOR; CHECKPOINT KINASE 2; CYCLINE; DNA; DNA POLYMERASE; DOUBLE STRANDED DNA; FANCONI ANEMIA GROUP E PROTEIN; GEMCITABINE; HISTONE H2AX; MRE11 PROTEIN; PROTEIN SERINE THREONINE KINASE INHIBITOR; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DEATH; CELL SURVIVAL; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DRUG TARGETING; EMBRYO DEVELOPMENT; ENDOMETRIUM CANCER; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE MUTATION; GENETIC VARIABILITY; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR INTERACTION; NONHUMAN; PHASE TRANSITION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; STOMACH CANCER; TRIPLE NEGATIVE BREAST CANCER; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE CHECKPOINTS; DNA DAMAGE; DNA REPAIR; HUMANS; MOLECULAR SEQUENCE DATA; NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASES; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84887116753     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1307-3     Document Type: Review

References (101)

1. Walworth N, Davey S, Beach D (1993) Fission yeast Chk1-protein kinase links the rad checkpoint pathway to Cdc2. Nature 363:368-371
2. Kumagai A, Guo Z, Emami KH, Wang SX, Dunphy WG (1998) The Xenopus Chk1 protein kinase mediates a caffeine-sensitive pathway of checkpoint control in cell-free extracts. J Cell Biol 142:1559-1569
3. Fogarty P, Kalpin RF, Sullivan W (1994) The Drosophila maternal-effect mutation grapes causes a metaphase arrest at nuclear cycle 13. Development 120:2131-2142
4. Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS, Piwnica-Worms H (1997) Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277:1501-1505
5. Elledge SJ (1996) Cell cycle checkpoints: preventing an identity crisis. Science 274:1664-1672
6. Nurse P (2000) A long twentieth century of the cell cycle and beyond. Cell 100:71-78
7. Cimprich KA, Cortez D (2008) ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 9:616-627
8. Dai Y, Grant S (2010) New insights into checkpoint kinase 1 in the DNA damage response signaling network. Clin Cancer Res 16:376-383
9. Bartek J, Lukas J (2007) DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19:238-245
10. Lee JH, Paull TT (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551-554
11. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506
12. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39-85
13. Nam EA, Cortez D (2011) ATR signalling: more than meeting at the fork. Biochem J 436:527-536
14. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548
15. Cortez D, Guntuku S, Qin J, Elledge SJ (2001) ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716
16. Parrilla-Castellar ER, Arlander SJ, Karnitz L (2004) Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair 3:1009-1014
17. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM (2007) The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev 21:1472-1477
18. Lee J, Kumagai A, Dunphy WG (2007) The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. J Biol Chem 282:28036-28044
19. Pabla N, Ma Z, McIlhatton MA, Fishel R, Dong Z (2011) hMSH2 recruits ATR to DNA damage sites for activation during DNA damage-induced apoptosis. J Biol Chem 286:10411-10418
20. Kumagai A, Dunphy WG (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
21. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8:37-45
22. Stiff T, Walker SA, Cerosaletti K, Goodarzi AA, Petermann E, Concannon P, O'Driscoll M, Jeggo PA (2006) ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 25:5775-5782
23. Pabla N, Huang S, Mi QS, Daniel R, Dong Z (2008) ATR-Chk2 signaling in p53 activation and DNA damage response during cisplatin-induced apoptosis. J Biol Chem 283:6572-6583
24. Enders GH (2008) Expanded roles for Chk1 in genome maintenance. J Biol Chem 283:17749-17752
25. Sorensen CS, Syljuasen RG (2012) Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res 40:477-486
26. Brown EJ, Baltimore D (2000) ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 14:397-402
27. de Klein A, Muijtjens M, van Os R, Verhoeven Y, Smit B, Carr AM, Lehmann AR, Hoeijmakers JH (2000) Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr Biol 10:479-482
28. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, Luo G, Carattini-Rivera S, DeMayo F, Bradley A, Donehower LA, Elledge SJ (2000) Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 14:1448-1459
29. Takai H, Tominaga K, Motoyama N, Minamishima YA, Nagahama H, Tsukiyama T, Ikeda K, Nakayama K, Nakanishi M (2000) Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev 14:1439-1447
30. Fogarty P, Campbell SD, Abu-Shumays R, Phalle BS, Yu KR, Uy GL, Goldberg ML, Sullivan W (1997) The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr Biol 7:418-426
31. Purdy A, Uyetake L, Cordeiro MG, Su TT (2005) Regulation of mitosis in response to damaged or incompletely replicated DNA require different levels of Grapes (Drosophila Chk1). J Cell Sci 118:3305-3315
32. Royou A, McCusker D, Kellogg DR, Sullivan W (2008) Grapes(Chk1) prevents nuclear CDK1 activation by delaying cyclin B nuclear accumulation. J Cell Biol 183:63-75
33. Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, Johansson F, Helleday T, Sehested M, Lukas J, Bartek J (2005) Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 25:3553-3562
34. Zachos G (2003) Chk1-defcient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO Rep 22(3):713-723
35. Sorensen CS, Syljuasen RG, Falck J, Schroeder T, Ronnstrand L, Khanna KK, Zhou BB, Bartek J, Lukas J (2003) Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3:247-258
36. Carrassa L, Damia G (2011) Unleashing Chk1 in cancer therapy. Cell Cycle 10:2121-2128
37. Carrassa L, Sanchez Y, Erba E, Damia G (2009) U2OS cells lacking Chk1 undergo aberrant mitosis and fail to activate the spindle checkpoint. J Cell Mol Med 13:1565-1576
38. Lam MH, Liu Q, Elledge SJ, Rosen JM (2004) Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell 6:45-59
39. Petermann E, Woodcock M, Helleday T (2010) Chk1 promotes replication fork progression by controlling replication initiation. Proc Natl Acad Sci USA 107:16090-16095
40. Maya-Mendoza A (2007) Chk1 regulates the density of active replication origins during the vertebrate S phase. EMBO Rep 26(11):2719-2731
41. Kramer A, Mailand N, Lukas C, Syljuasen RG, Wilkinson CJ, Nigg EA, Bartek J, Lukas J (2004) Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 6:884-891
42. Zachos G, Black EJ, Walker M, Scott MT, Vagnarelli P, Earnshaw WC, Gillespie DA (2007) Chk1 is required for spindle checkpoint function. Dev Cell 12:247-260
43. Peddibhotla S, Lam MH, Gonzalez-Rimbau M, Rosen JM (2009) The DNA-damage effector checkpoint kinase 1 is essential for chromosome segregation and cytokinesis. Proc Natl Acad Sci USA 106:5159-5164
44. Guervilly JH, Mace-Aime G, Rosselli F (2008) Loss of CHK1 function impedes DNA damage-induced FANCD2 monoubiquitination but normalizes the abnormal G2 arrest in Fanconi anemia. Hum Mol Genet 17:679-689
45. Tapia-Alveal C, Calonge TM, O'Connell MJ (2009) Regulation of chk1. Cell Div 4:8
46. Zhao H, Piwnica-Worms H (2001) ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 21:4129-4139
47. Blasius M, Forment JV, Thakkar N, Wagner SA, Choudhary C, Jackson SP (2011) A phospho-proteomic screen identifies substrates of the checkpoint kinase Chk1. Genome Biol 12:R78
48. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28:739-745
49. Chen Y, Poon RY (2008) The multiple checkpoint functions of CHK1 and CHK2 in maintenance of genome stability. Front Biosci 13:5016-5029
50. Donzelli M, Draetta GF (2003) Regulating mammalian checkpoints through Cdc25 inactivation. EMBO Rep 4:671-677
51. Uto K, Inoue D, Shimuta K, Nakajo N, Sagata N (2004) Chk1, but not Chk2, inhibits Cdc25 phosphatases by a novel common mechanism. EMBO J 23:3386-3396
52. Sanchez Y, Wong C, Thoma RS, Richman R, Wu Z, Piwnica-Worms H, Elledge SJ (1997) Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277:1497-1501
53. Mailand N, Falck J, Lukas C, Syljuasen RG, Welcker M, Bartek J, Lukas J (2000) Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425-1429
54. Melixetian M, Klein DK, Sorensen CS, Helin K (2009) NEK11 regulates CDC25A degradation and the IR-induced G2/M checkpoint. Nat Cell Biol 11:1247-1253
55. O'Connell MJ, Raleigh JM, Verkade HM, Nurse P (1997) Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J 16:545-554
56. Lee J, Kumagai A, Dunphy WG (2001) Positive regulation of Wee1 by Chk1 and 14-3-3 proteins. Mol Biol Cell 12:551-563
57. Tang J, Erikson RL, Liu X (2006) Checkpoint kinase 1 (Chk1) is required for mitotic progression through negative regulation of polo-like kinase 1 (Plk1). Proc Natl Acad Sci USA 103:11964-11969
58. Shimada M, Niida H, Zineldeen DH, Tagami H, Tanaka M, Saito H, Nakanishi M (2008) Chk1 is a histone H3 threonine 11 kinase that regulates DNA damage-induced transcriptional repression. Cell 132:221-232
59. Liu P, Barkley LR, Day T, Bi X, Slater DM, Alexandrow MG, Nasheuer HP, Vaziri C (2006) The Chk1-mediated S-phase checkpoint targets initiation factor Cdc45 via a Cdc25A/Cdk2-independent mechanism. J Biol Chem 281:30631-30644
60. Yang XH, Shiotani B, Classon M, Zou L (2008) Chk1 and Claspin potentiate PCNA ubiquitination. Genes Dev 22:1147-1152
61. Kannouche PL, Wing J, Lehmann AR (2004) Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol Cell 14:491-500
62. Freudenthal BD, Gakhar L, Ramaswamy S, Washington MT (2010) Structure of monoubiquitinated PCNA and implications for translesion synthesis and DNA polymerase exchange. Nat Struct Mol Biol 17:479-484
63. Prakash S, Johnson RE, Prakash L (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 74:317-353
64. Wang X, Kennedy RD, Ray K, Stuckert P, Ellenberger T, D'Andrea AD (2007) Chk1-mediated phosphorylation of FANCE is required for the Fanconi anemia/BRCA pathway. Mol Cell Biol 27:3098-3108
65. Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, Bartek J, Helleday T (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7:195-201
66. Groth A, Lukas J, Nigg EA, Sillje HH, Wernstedt C, Bartek J, Hansen K (2003) Human Tousled like kinases are targeted by an ATM- and Chk1-dependent DNA damage checkpoint. EMBO J 22:1676-1687
67. Gonzalez S, Prives C, Cordon-Cardo C (2003) p73 alpha regulation by Chk1 in response to DNA damage. Mol Cell Biol 23:8161-8171
68. Urist M, Tanaka T, Poyurovsky MV, Prives C (2004) p73 induction after DNA damage is regulated by checkpoint kinases Chk1 and Chk2. Genes Dev 18:3041-3054
69. Myers K, Gagou ME, Zuazua-Villar P, Rodriguez R, Meuth M (2009) ATR and Chk1 suppress a caspase-3-dependent apoptotic response following DNA replication stress. PLoS Genet 5:e1000324
70. Sidi S, Sanda T, Kennedy RD, Hagen AT, Jette CA, Hoffmans R, Pascual J, Imamura S, Kishi S, Amatruda JF, Kanki JP, Green DR, D'Andrea AA, Look AT (2008) Chk1 suppresses a caspase-2 apoptotic response to DNA damage that bypasses p53, Bcl-2, and caspase-3. Cell 133:864-877
71. Katsuragi Y, Sagata N (2004) Regulation of Chk1 kinase by autoinhibition and ATR-mediated phosphorylation. Mol Biol Cell 15:1680-1689
72. Capasso H, Palermo C, Wan S, Rao H, John UP, O'Connell MJ, Walworth NC (2002) Phosphorylation activates Chk1 and is required for checkpoint-mediated cell cycle arrest. J Cell Sci 115:4555-4564
73. Chen P, Luo C, Deng Y, Ryan K, Register J, Margosiak S, Tempczyk-Russell A, Nguyen B, Myers P, Lundgren K, Kan CC, O'Connor PM (2000) The 1.7 A crystal structure of human cell cycle checkpoint kinase Chk1: implications for Chk1 regulation. Cell 100:681-692
74. Shann YJ, Hsu MT (2001) Cloning and characterization of liver-specific isoform of Chk1 gene from rat. J Biol Chem 276:48863-48870
75. Kosoy A, O'Connell MJ (2008) Regulation of Chk1 by its C-terminal domain. Mol Biol Cell 19:4546-4553
76. Okita N, Minato S, Ohmi E, Tanuma S, Higami Y (2012) DNA damage-induced CHK1 autophosphorylation at Ser296 is regulated by an intramolecular mechanism. FEBS Lett 586:3974-3979
77. Kasahara K, Goto H, Enomoto M, Tomono Y, Kiyono T, Inagaki M (2010) 14-3-3gamma mediates Cdc25A proteolysis to block premature mitotic entry after DNA damage. EMBO J 29:2802-2812
78. Walker M, Black EJ, Oehler V, Gillespie DA, Scott MT (2009) Chk1 C-terminal regulatory phosphorylation mediates checkpoint activation by de-repression of Chk1 catalytic activity. Oncogene 28:2314-2323
79. Rodriguez-Bravo V, Guaita-Esteruelas S, Florensa R, Bachs O, Agell N (2006) Chk1- and claspin-dependent but ATR/ATM- and Rad17-independent DNA replication checkpoint response in HeLa cells. Cancer Res 66:8672-8679
80. Pabla N, Bhatt K, Dong Z (2011) Checkpoint kinase 1 (Chk1)-short is a splice variant and endogenous inhibitor of Chk1 that regulates cell cycle and DNA damage checkpoints. Proc Natl Acad Sci 109:197-202
81. Zhang YW, Otterness DM, Chiang GG, Xie W, Liu YC, Mercurio F, Abraham RT (2005) Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol Cell 19:607-618
82. Zhang YW, Brognard J, Coughlin C, You Z, Dolled-Filhart M, Aslanian A, Manning G, Abraham RT, Hunter T (2009) The F box protein Fbx6 regulates Chk1 stability and cellular sensitivity to replication stress. Mol Cell 35:442-453
83. Hutchins JR, Hughes M, Clarke PR (2000) Substrate specificity determinants of the checkpoint protein kinase Chk1. FEBS Lett 466:91-95
84. Bertoni F, Codegoni AM, Furlan D, Tibiletti MG, Capella C, Broggini M (1999) CHK1 frameshift mutations in genetically unstable colorectal and endometrial cancers. Gene Chromosome Canc 26:176-180
85. Menoyo A (2001) Somatic mutations in the DNA damage-response genes ATR and CHK1 in sporadic stomach tumors with microsatellite instability. Cancer Res 61(21):7727-7730
86. Codegoni AM, Bertoni F, Colella G, Caspani G, Grassi L, D'Incalci M, Broggini M (1999) Microsatellite instability and frameshift mutations in genes involved in cell cycle progression or apoptosis in ovarian cancer. Oncol Res 11:297-301
87. Vassileva V (2002) Genes involved in DNA repair are mutational targets in endometrial cancers with microsatellite instability. Cancer Res 62(14):4095-4099
88. Bartek J, Lukas J (2003) Chk1 and Chk2 kinases in checkpoint control and cancer. Canc Cell 3:421-429
89. Fishler T, Li YY, Wang RH, Kim HS, Sengupta K, Vassilopoulos A, Lahusen T, Xu X, Lee MH, Liu Q, Elledge SJ, Ried T, Deng CX (2010) Genetic instability and mammary tumor formation in mice carrying mammary-specific disruption of Chk1 and p53. Oncogene 29:4007-4017
90. Tho LM, Libertini S, Rampling R, Sansom O, Gillespie DA (2012) Chk1 is essential for chemical carcinogen-induced mouse skin tumorigenesis. Oncogene 31:1366-1375
91. Verlinden L, Vanden Bempt I, Eelen G, Drijkoningen M, Verlinden I, Marchal K, De Wolf-Peeters C, Christiaens MR, Michiels L, Bouillon R, Verstuyf A (2007) The E2F-regulated gene Chk1 is highly expressed in triple-negative estrogen receptor/progesterone receptor/HER-2 breast carcinomas. Cancer Res 67:6574-6581
92. Zhou BB, Anderson HJ, Roberge M (2003) Targeting DNA checkpoint kinases in cancer therapy. Cancer Biol Ther 2:S16-S22
93. Zhou BB, Bartek J (2004) Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat Rev Cancer 4:216-225
94. Lieberman HB (2008) DNA damage repair and response proteins as targets for cancer therapy. Curr Med Chem 15:360-367
95. Tenzer A, Pruschy M (2003) Potentiation of DNA-damage-induced cytotoxicity by G2 checkpoint abrogators. Curr Med Chem Anticancer Agents 3:35-46
96. Koniaras K (2001) Inhibition of Chk1-dependent G2 DNA damage checkpoint radiosensitizes p53 mutant human cells. Oncogene 20(51):7453-7463
97. Zenvirt S, Kravchenko-Balasha N, Levitzki A (2010) Status of p53 in human cancer cells does not predict efficacy of CHK1 kinase inhibitors combined with chemotherapeutic agents. Oncogene 29:6149-6159
98. Blagosklonny MV (2002) Sequential activation and inactivation of G2 checkpoints for selective killing of p53-deficient cells by microtubule-active drugs. Oncogene 21:6249-6254
99. Xiao Z, Xue J, Semizarov D, Sowin TJ, Rosenberg SH, Zhang H (2005) Novel indication for cancer therapy: Chk1 inhibition sensitizes tumor cells to antimitotics. Int J Cancer 115:528-538
100. Arlander SJ, Eapen AK, Vroman BT, McDonald RJ, Toft DO, Karnitz LM (2003) Hsp90 inhibition depletes Chk1 and sensitizes tumor cells to replication stress. J Biol Chem 278:52572-52577
101. Guertin AD, Martin MM, Roberts B, Hurd M, Qu X, Miselis NR, Liu Y, Li J, Feldman I, Benita Y, Bloecher A, Toniatti C, Shumway SD (2012) Unique functions of CHK1 and WEE1 underlie synergistic anti-tumor activity upon pharmacologic inhibition. Cancer cell Int 12:45