Chk1 and Chk2 kinases in checkpoint control and cancer

Cancer Cell

Volumn 3, Issue 5, 2003, Pages 421-429

  Bartek, Jiri ^a   Lukas, Jiri ^a  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; PROTEIN KINASE; PROTEIN P53; UNCLASSIFIED DRUG; PROTEIN SERINE THREONINE KINASE;

BIOACCUMULATION; BREAST CANCER; CANCER; CANCER CELL; CANCER SUSCEPTIBILITY; CELL CYCLE; CHROMOSOME ABERRATION; COLON CANCER; DNA DAMAGE; DNA REPAIR; GENE MUTATION; GENETIC DISORDER; GENETIC VARIABILITY; GENOME; HUMAN; MUTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; BREAST TUMOR; COLON TUMOR; ENZYMOLOGY; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; NEOPLASM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

MAMMALIA;

ANIMALS; BREAST NEOPLASMS; CELL CYCLE; COLONIC NEOPLASMS; DNA REPAIR; HUMANS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTATION; NEOPLASMS; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0038418869     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1535-6108(03)00110-7     Document Type: Review

References (87)

1. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2001;2177-2196.
2. Ahn J.Y., Li X., Davis H.L., Canman C.E. Phosphorylation of threonine 68 promotes oligomerization and autophosphorylation of the Chk2 protein kinase via the forkhead-associated domain. Biol. Chem. 277:2002;19389-19395.
3. Ahn J., Urist M., Prives C. Questioning the role of Chk2 in the p53 DNA damage response. J. Biol. Chem. in press:2003;. Published online March 24, 2003. 10.1074/jbc.M213185200.
4. Allinen M., Huusko P., Mäntyniemi S., Launonen V., Winqvist R. Mutation analysis of the CHK2 gene in families with hereditary breast cancer. Br. J. Cancer. 85:2001;209-212.
5. Bartek J., Lukas J. Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr. Opin. Cell Biol. 13:2001;738-747.
6. Bartek J., Falck J., Lukas J. CHK2 kinase - a busy messenger. Nat. Rev. Mol. Cell Biol. 2:2001;877-886.
7. Bartkova J., Falck J., Rajpert-De Meyts E., Skakkebaek N.E., Lukas J., Bartek J. Chk2 tumour suppressor protein in human spermatogenesis and testicular germ-cell tumours. Oncogene. 20:2001;5897-5902.
8. Bell D.W., Varley J.M., Szydlo T.E., Kang D.H., Wahrer D.C., Shannon K.E., Lubratovich M., Verselis S.J., Isselbacher K.J., Fraumeni J.F., et al. Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science. 286:1999;2528-2531.
9. Bertoni F., Codegoni A.M., Furlan D., Tibiletti M.G., Capella C., Broggini M. CHK1 frameshift mutations in genetically unstable colorectal and endometrial cancers. Genes Chromosomes Cancer. 26:1999;176-180.
10. Chehab N.H., Malikzay A., Stavridi E.S., Halazonetis T.D. Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc. Natl. Acad. Sci. USA. 96:1999;13777-13782.
11. Chehab N.H., Malikzay A., Appel M., Halazonetis T.D. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 14:2000;278-288.
12. Cortez D., Guntuku S., Qin J., Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science. 294:2001;1713-1716.
13. DiTullio R.A., Mochan T.A., Venere M., Bartkova J., Sehested M., Bartek J., Halazonetis T.D. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 4:2002;998-1002.
14. Dixon H., Norbury C.J. Therapeutic exploitation of checkpoint defects in cancer cells lacking p53 function. Cell Cycle. 1:2002;362-368.
15. Dornan D., Shimizu H., Perkins N.D., Hupp T.R. DNA-dependent acetylation of p53 by the transcription coactivator p300. J. Biol. Chem. 278:2003;13431-13441. Published online December 23, 2002. 10.1074/jbc. M211460200.
16. Falck J., Mailand N., Syljuåsen R.G., Bartek J., Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature. 410:2001a;842-847.
17. Falck J., Lukas C., Protopopova M., Lukas J., Selivanova G., Bartek J. Functional impact of concomitant versus alternative defects in the Chk2-p53 tumour suppressor pathway. Oncogene. 20:2001b;5503-5510.
18. Falck J., Petrini J.H., Williams B.R., Lukas J., Bartek J. The DNA damage-dependent intra-S phase checkpoint is regulated by parallel pathways. Nat. Genet. 30:2002;290-294.
19. Feijoo C., Hall-Jackson C., Wu R., Jenkins D., Leitch J., Gilbert D.M., Smythe C. 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. 154:2001;913-923.
20. Fernandez-Capetillo O., Chen H.T., Celeste A., Ward I., Romanienko P.J., Morales J.C., Naka K., Xia Z., Camerini-Otero R.D., Motoyama N., et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:2002;993-997.
21. Gatei M., Sloper K., Sørensen C.S., Syljuåsen R., Falck J., Hobson J., Zhou B.-B., Bartek J., Khanna K.K. ATM and DBS1 dependent phosphorylation of CHK1 on S317 in response to IR. J. Biol. Chem. 278:2003;14806-14811. Published online February 14, 2003. 10.1074/jbc. M210862200.
22. Goldberg M., Stucki M., Falck J., D'Amours D., Rahman D., Pappin D., Bartek J., Jackson S.P. The MDC1 protein is required for the intra-S-phase DNA damage checkpoint. Nature. 421:2003;952-956.
23. Groth A., Hansen K., Nigg E.A., Sillje H.H.W., Lukas J., Bartek J. Human tousled like kinases are targeted by an ATM and Chk1 dependent DNA damage checkpoint. EMBO J. 22:2003;1676-1687.
24. Hangaishi A., Ogawa S., Qiao Y., Wang L., Hosoya N., Yuji K., Imai Y., Takeuchi K., Miyawaki S., Hirai H. Mutations of Chk2 in primary hematopoietic neoplasms. Blood. 99:2002;3075-3077.
25. Haruki N., Saito H., Tatematsu Y., Konishi H., Harano T., Masuda A., Osada H., Fujii Y., Takahashi T. Histological type-selective, tumor-predominant expression of a novel CHK1 isoform and infrequent in vivo somatic CHK2 mutation in small cell lung cancer. Cancer Res. 60:2000;4689-4692.
26. Heffernan T.P., Simpson D.A., Frank A.R., Heinloth A.N., Paules R.S., Cordeiro-Stone M., Kaufmann W.K. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol. Cell. Biol. 22:2002;8552-8561.
27. Hirao A., Kong Y.Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S.J., Mak T.W. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science. 287:2000;1824-1827.
28. Hirao A., Cheung A., Duncan G., Girard P.M., Elia A.J., Wakeham A., Okada H., Sarkissian T., Wong J.A., Sakai T., et al. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol. Cell. Biol. 22:2002;6521-6532.
29. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature. 411:2001;366-374.
30. Hofman W.-K., Miller C.W., Tsukasaki K., Tavor S., Ikezoe T., Hoelzer D., Takeuchi S., Koeffler H.P. Mutation analysis of the DNAdamage checkpoint gene CHK2 in myelodysplastic syndromes and acute myeloid leukemias. Leuk. Res. 25:2001;333-338.
31. Ingvarsson S., Sigbjornsdottir B.I., Huiping C., Hafsteinsdottir S.H., Ragnarsson G., Barkadottir R.B., Arason A., Egilsson V., Bergthorsson J.T. Mutation analysis of the CHK2 gene in breast carcinoma and other cancers. Breast Cancer Res. 4:2002;R4.
32. Jack M.T., Woo R.A., Hirao A., Cheung A., Mak T.W., Lee P.W. Chk2 is dispensable for p53-mediated G1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA. 99:2002;9825-9829.
33. Jallepalli P.V., Lengauer C., Vogelstein B., Bunz F. The Chk2 tumor suppressor is not required for p53 responses in human cancer cells. J. Biol. Chem. in press:2003;. Published online March 24, 2003. 10.1074/jbc.M213159200.
34. Kaneko Y.S., Watanabe N., Morisaki H., Akita H., Fujimoto A., Tominaga K., Terasawa M., Tachibana A., Ikeda K., Nakanishi M., Kaneko Y. Cell-cycle-dependent and ATM-independent expression of human Chk1 kinase. Oncogene. 18:1999;3673-3681.
35. Kastan M.B., Lim D.S. The many substrates and functions of ATM. Nat. Rev. Mol. Cell. Biol. 1:2000;179-186.
36. Khanna K.K., Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:2001;247-254.
37. Kumagai A., Dunphy W.G. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell. 6:2000;839-849.
38. Lee C.H., Chung J.H. The hCds1 (Chk2)-FHA domain is essential for a chain of phosphorylation events on hCds1 that is induced by ionizing radiation. J. Biol. Chem. 276:2001;30537-30541.
39. Lee J.S., Collins K.M., Brown A.L., Lee C.H., Chung J.H. hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature. 404:2000;201-204.
40. Lee S.B., Kim S.H., Bell D.W., Wahrer D.C., Schiripo T.A., Jorczak M.M., Sgroi D.C., Garber J.E., Li F.P., Nichols K.E., et al. Destabilization of CHK2 by a missense mutation associated with Li-Fraumeni syndrome. Cancer Res. 61:2001;8062-8067.
41. Li J., Williams B.L., Haire L.F., Goldberg M., Wilker E., Durocher D., Yaffe M.B., Jackson S.P., Smerdon S.J. Structural and functional versatility of the FHA domain in DNA-damage signaling by the tumor suppressor kinase Chk2. Mol. Cell. 9:2002;1045-1054.
42. Liu Q., Guntuku S., Cui X.S., Matsuoka S., Cortez D., Tamai K., Luo G., Carattini-Rivera S., DeMayo F., Bradley A., et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14:2000;1448-1459.
43. Li Y., Sun X., LaMont J.T., Pardee A.B., Li C.J. Selective killing of cancer cells by beta-lapachone: direct checkpoint activation as a strategy against cancer. Proc. Natl. Acad. Sci. USA. 100:2003;2674-2678.
44. Lou Z., Minter-Dykhouse K., Wu X., Chen J. MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature. 421:2003;957-961.
45. Lukas C., Falck J., Bartkova J., Bartek J., Lukas J. Distinct spatio-temporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 421:2003;952-960.
46. Lukas C., Bartkova J., Latella L., Falck J., Mailand N., Schroeder T., Sehested M., Lukas J., Bartek J. DNA damage-activated kinase Chk2 is independent of proliferation or differentiation yet correlates with tissue biology. Cancer Res. 61:2001;4990-4993.
47. Mailand N., Falck J., Lukas C., Syljuasen R.G., Welcker M., Bartek J., Lukas J. Rapid destruction of human Cdc25A in response to DNA damage. Science. 288:2000;1425-1429.
48. Mailand N., Podtelejnikov A.V., Groth A., Mann M., Bartek J., Lukas J. Regulation of G2/M events by Cdc25A phosphatase through phosphorylation- dependent modulation of its stability. EMBO J. 21:2002;5921-5929.
49. Matsuoka S., Nakagawa T., Masuda A., Haruki N., Elledge S.J., Takahashi T. Reduced expression and impaired kinase activity of a Chk2 mutant identified in human lung cancer. Cancer Res. 61:2001;5362-5365.
50. McGowan C.H. Checking in on Cds1 (Chk2): A checkpoint kinase and tumor suppressor. Bioessays. 24:2002;502-511.
51. * 1100delC in noncarriers of BRCA1 or BRCA2 mutations. Nat. Genet. 31:2002;55-59.
52. Menoyo A., Alazzouzi H., Espin E., Armengol M., Yamamoto H., Schwartz S. Jr. Somatic mutations in the DNA damage-response genes ATR and CHK1 in sporadic stomach tumors with microsatellite instability. Cancer Res. 61:2001;7727-7730.
53. Miller C.W., Ikezoe T., Krug U., Hofmann W.K., Tavor S., Vegesna V., Tsukasaki K., Takeuchi S., Koeffler H.P. Mutations of the CHK2 gene are found in some osteosarcomas, but are rare in breast, lung, and ovarian tumors. Genes Chromosomes Cancer. 33:2002;17-21.
54. O'Neill T., Giarratani L., Chen P., Iyer L., Lee C.H., Bobiak M., Kanai F., Zhou B.B., Chung J.H., Rathbun G.A. Determination of substrate motifs for human Chk1 and hCds1/Chk2 by the oriented peptide library approach. J. Biol. Chem. 277:2002;16102-16115.
55. Reddy A., Yuille M., Sullivan A., Repellin C., Bell A., Tidy J.A., Evans D.J., Farrell P.J., Gusterson B., Gasco M., Crook T. Analysis of CHK2 in vulval neoplasia. Br. J. Cancer. 86:2002;756-760.
56. Schon O., Friedler A., Bycroft M., Freund S.M., Fersht A.R. Molecular mechanism of the interaction between MDM2 and p53. J. Mol. Biol. 323:2002;491-501.
57. Scully R., Livingston D.M. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature. 408:2000;429-432.
58. Schutte M., Seal S., Barfoot R., Meijers-Heijboer H., Wasielewski M., Evans D.G., Eccles D., Meijers C., Lohman F., Klijn J., et al. Variants in CHEK2 other than 1100delC do not make a major contribution to breast cancer susceptibility. Am. J. Hum. Genet. 72:2003;1023-1028.
59. Shieh S.Y., Ahn J., Tamai K., Taya Y., Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14:2000;289-300.
60. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer. 3:2003;155-168.
61. Sodha N., Bullock S., Taylor R., Mitchell G., Guertl-Lackner B., Williams R.D., Bevan S., Bishop K., McGuire S., Houlston R.S., Eeles R.A. CHEK2 variants in susceptibility to breast cancer and evidence of retention of the wild type allele in tumours. Br. J. Cancer. 87:2002;1445-1448.
62. Sørensen C.S., Syljuåsen R.G., Falck J., Schroeder T., Rönnstrand L., Zhou B.-B., Bartek J., Lukas J. Chk1 regulates the S-phase checkpoint by coupling the physiological turnover and ionizing radiationinduced accelerated proteolysis of Cdc25A. Cancer Cell. 3:2003;247-258.
63. Stevens C., Smith L., LaThangue N.B. Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol. 5:2003;401-409. Published online April 22, 2003 10.1038/ncb974.
64. Stewart G.S., Wang B., Bignell C.R., Taylor A.M., Elledge S.J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature. 421:2003;961-966.
65. Sullivan A., Yuille M., Repellin C., Reddy A., Reelfs O., Bell A., Dunne B., Gusterson B.A., Osin P., Farrell P.J., et al. Concomitant inactivation of p53 and Chk2 in breast cancer. Oncogene. 21:2002;1316-1324.
66. Takai H., Tominaga K., Motoyama N., Minamishima Y.A., Nagahama H., Tsukiyama T., Ikeda K., Nakayama K., Nakanishi M. Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev. 14:2000;1439-1447.
67. Takai H., Naka K., Okada Y., Watanabe M., Harada N., Saito S., Anderson C.W., Appella E., Nakanishi M., Suzuki H., et al. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21:2002;5195-5205.
68. Tavor S., Takeuchi S., Tsukasaki K., Miller C.W., Hofmann W.K., Ikezoe T., Said J.W., Koeffler H.P. Analysis of the CHK2 gene in lymphoid malignancies. Leuk. Lymphoma. 42:2001;517-520.
69. Tort F., Hernandez S., Bea S., Martinez A., Esteller M., Herman J.G., Puig X., Camacho E., Sanchez M., Nayach I., et al. CHK2-decreased protein expression and infrequent genetic alterations mainly occur in aggressive types of non-Hodgkin lymphomas. Blood. 100:2002;4602-4608.
70. Vahteristo P., Tamminen A., Karvinen P., Eerola H., Eklund C., Aaltonen L.A., Blomqvist C., Aittomaki K., Nevanlinna H. p53, CHK2, and CHK1 genes in Finnish families with Li-Fraumeni syndrome: further evidence of CHK2 in inherited cancer predisposition. Cancer Res. 61:2001;5718-5722.
71. Vahteristo P., Bartkova J., Eerola H., Syrjakoski K., Ojala S., Kilpivaara O., Tamminen A., Kononen J., Aittomaki K., Heikkila P., et al. A CHEK2 genetic variant contributing to a substantial fraction of familial breast cancer. Am. J. Hum. Genet. 71:2002;432-438.
72. Vassileva V., Millar A., Briollais L., Chapman W., Bapat B. Genes involved in DNA repair are mutational targets in endometrial cancers with microsatellite instability. Cancer Res. 62:2002;4095-4099.
73. Wang Y., Cortez D., Yazdi P., Neff N., Elledge S.J., Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:2000;927-939.
74. Wang B., Matsuoka S., Carpenter P.B., Elledge S.J. 53BP1, a mediator of the DNA damage checkpoint. Science. 298:2002;1435-1438.
75. Ward I.M., Minn K., Van Deursen J., Chen J. p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23:2003;2556-2563.
76. Weiss R.S., Matsuoka S., Elledge S.J., Leder P. Hus1 acts upstream of chk1 in a mammalian DNA damage response pathway. Curr. Biol. 12:2002;73-77.
77. Wu X., Webster S.R., Chen J. Characterization of tumor-associated Chk2 mutations. J. Biol. Chem. 274:2001;2971-2974.
78. Xiao Z., Chen Z., Gunasekera A.H., Sowin T.J., Rosenberg S.H., Fesik S., Zhang H. Chk1 mediates S and G2 arrests through Cdc25A degradation in response to DNA damaging agents. J. Biol. Chem. in press:2003;. Published online April 13, 2003. 10.1074/jbc.M300229200.
79. Xie S., Wu H., Wang Q., Kunicki J., Thomas R.O., Hollingsworth R.E., Cogswell J., Dai W. Genotoxic stress-induced activation of Plk3 is partly mediated by Chk2. Cell Cycle. 1:2002;424-429.
80. Xu X., Tsvetkov L., Stern D. Chk2 activation and phosphorylation- dependent oligomerization. Mol. Cell. Biol. 22:2002;4419-4432.
81. Yang S., Kuo C., Bisi J.E., Kim M.K. PML-dependent apoptosis after DNA damage is regulated by the checkpoint kinase hCds1/Chk2. Nat. Cell Biol. 4:2002;865-870.
82. Yarden R.I., Pardo-Reoyo S., Sgagias M., Cowan K.H., Brody L.C. BRCA1 regulates the G2/M checkpoint by activating Chk1 kinase upon DNA damage. Nat. Genet. 30:2002;285-289.
83. Zachos G., Rainey M.D., Gillespie D.A. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO J. 22:2003;713-723.
84. Zhao H., Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol. Cell. Biol. 21:2001;4129-4139.
85. 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. USA. 99:2002;14795-14800.
86. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature. 408:2000;433-439.
87. Zou L., Cortez D., Elledge S.J. Regulation of ATR substrate selection by Rad17-dependent loading of Rad 9 complex onto chromatin. Genes Dev. 16:2002;198-208.