Inhibition of the ATR/Chk1 pathway induces a p38-dependent S-phase delay in mouse embryonic stem cells

Cell Cycle

Volumn 4, Issue 10, 2005, Pages 1428-1434

  Jirmanova, Ludmila ^a   Bulavin, Dmitry V ^b   Fornace Jr , Albert J ^c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

ATM; ATR; Caffeine; Cell cycle; Embryonic stem cells; p38

Indexed keywords

7 HYDROXYSTAUROSPORINE; ATM PROTEIN; ATR PROTEIN; CAFFEINE; CHECKPOINT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1; MITOGEN ACTIVATED PROTEIN KINASE P38; WORTMANNIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; MOUSE; NONHUMAN; PROTEIN DEFICIENCY; WILD TYPE;

ATAXIA TELANGIECTASIA;

EID: 26444603774     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.4.10.2055     Document Type: Article

References (67)

1. Savatier P, Lapillone H, Jirmanova L, Vitelli L, Samarut J. Analysis of the cell cycle in mouse embryonic stem cells. Methods Mol Biol 2002; 185:27-33.
2. Aladjem MI, Spike B, Rodewald LW, Hope TJ, Klemm M, Jaenisch R, Wahl GM. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 1998; 8:145-55.
3. Prost S, Bellamy C, Clarke AR, Wyllie AH, Harrison DJ. p53-independent DNA repair and cell cycle arrest in embryonic stem cells. FEBS Lett 1998; 425:499-504.
4. 1) control and immortalization. Genes Dev 2000; 14:3037-50.
5. Burdon T, Smith A, Savatier P. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 2000; 12:432-8.
6. Blasina A, Price B, Turenne GA, McGowan CH. Caffeine inhibits the checkpoint kinase ATM. Curr Biol 1999; 9:1135-8.
7. Sarkaria JN, Busby E, Tibbetts RS, Roos P, Taya Y, Karnitz LM, Abraham RT. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 1999; 59:4375-82.
8. 2)/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J Biol Chem 2000; 275:10342-8.
9. 2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 2001; 411:102-7.
10. Bulavin DV, Amundson S, Fornace Jr AJ. p38 and Chk1 kinases: Different conductors for the G(2)/M checkpoint symphony. Curr Opin Gen Dev 2002; 12:92-7.
11. Manke IA, Nguyen A, Lim D, Stewart MQ, Elia AE, Yaffe MB. MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation. Mol Cell 2005; 17:37-48.
12. Sancar A, Lindsey-Boltz LA, Unsai-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39-85.
13. Mailand N, Falck J, Lukas C, Syljuasen RG, Welcker M, Bartek J, Lukas J. Rapid destruction of human Cdc25A in response to DNA damage. Science 2000; 288:1425-9.
14. Falck J, Mailand N, Syljuasen RG, Bartek J, Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 2001; 410:842-7.
15. 1- and S-phase checkpoints in response to DNA damage. Curr Opin Cell Biol 2001; 13:738-47.
16. Cliby WA, Roberts C, Cimprich KA, Stringer CM, Lamb JR, Schreiber SL, Friend SH. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J 1998; 17:159-69.
17. Hirao A, Kong Y, Matsuoka S, Wakeham A, Ruland J, Yoshida H, Liu D, Elledge SJ, Mak TW. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 2000; 287:1824-7.
18. Elledge S. Cell cycle checkpoints: Preventing an identity crisis. Science 1996; 274:1664-72.
19. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, Shiloh Y, Crawley JN, Ried T, Tagle D, Wynshaw-Boris A. Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 1996; 86:159-71.
20. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 1996; 10:2411-22.
21. Hecht F, Hecht B. Cancer in ataxia-telangiectasia patients. Cancer Genet Cytogenet 1990; 46:9-19.
22. Reichenbach J, Schubert R, Schindler D, Muller K, Bohles H, Zielen S. Elevated oxidative stress in patients with ataxia telangiectasia. Antioxid Redox Signal 2002; 4:465-9.
23. de Klein A, Muijtjens M, van Os R, Verhoeven Y, Smit B, Carr AM, Lehmann AR, Hoeijmakers JH. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr Biol 2000; 10:479-82.
24. Brown EJ, Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 2000; 14:397-402.
25. Brown EJ, Baltimore D. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev 2003; 17:615-28.
26. 2)/M DNA damage checkpoint. Genes Dev 2000; 14:1448-59.
27. Chehab NH, Malikzay A, Appel M, Halazonetis TD. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev 2000; 14:278-88.
28. Nakajo N, Oe T, Uto K, Sagata N. Involvement of Chk1 kinase in prophase I arrest of Xenopus oocytes. Dev Biol 1999; 207:432-44.
29. Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 2001; 21:4129-39.
30. Nghiem P, Park PK, Kim Y, Vaziri C, Schreiber SL. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc Natl Acad Sci USA 2001; 98:9092-7.
31. Nishijima H, Nishitani H, Saitoa N, Nishimoto T. Caffeine mimics adenine and 2′-deoxyadenosine, both of which inhibit the guanine-nucleotide exchange activity of RCC1 and the kinase activity of ATR. Genes to Cells 2003; 8:423-35.
32. Canman C. Replication checkpoint: Preventing mitotic catastrophe. Curr Biol 2001; 11:R121-4.
33. Osborn AJ, Elledge S, Zou L. Checking on the fork: The DNA-replication stress-response pathway. Trends Cell Biol 2002; 12:509-16.
34. Tibbetts RS, Brumbaugh K, Williams JM, Sarkaria JN, Cliby WA, Shieh SY, Taya Y, Prives C, Abraham RT. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev 1999; 13:152-7.
35. Pandita TK, Liebermann HB, Lim DS, Dhar S, Zheng W, Taya Y, Kastan MB. Ionizing radiation activates the ATM kinase throughout the cell cycle. Oncogene 2000; 19:1386-91.
36. Dai Y, Yu C, Singh V, Tang L, Wang Z, McInistry R, Dent P, Grant S. Pharmacological inhibitors of the mitogen-activated protein kinase (MAPK) kinase/MAPK cascade interact synergistically with UCN-01 to induce mitochondrial dysfunction and apoptosis in human leukemia cells. Cancer Res 2001; 61:5106-15.
37. He Z, Ma W, Hashimoto T, Bode AM, Yang CS, Dong Z. Induction of apoptosis by caffeine is mediated by the p53, Bax, and caspase 3 pathways. Cancer Res 2003; 63:4396-401.
38. 2 by X-irradiation. Int J Radiat Biol 1995; 67:347-58.
39. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J Immunol Methods 1995; 184:39-51.
40. van Engeland M, Ramaekers FC, Schutte B, Reutelingsperger CP. A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 1996; 24:131-9.
41. Duval D, Reinhardt B, Kedinger C, Boeuf H. Role of suppressors of cytokine signaling (Socs) in leukemia inhibitory factor (LIF) -dependent embryonic stem cell survival. FASEB J 2000; 14:1577-84.
42. Duval D, Malaise M, Reinhard B, Kedinger C, Boeuf H. A p38 inhibitor allows to dissociate differentiation and apoptotic processes triggered upon LIF withdrawal in mouse embryonic stem cells. Cell Death Differ 2004; 11:331-41.
43. Cazillis M, Bringuier A, Delautier D, Buisine M, Bernuau D, Gespach C, Groyer A. Disruption of MKK4 signaling reveals its tumor-suppressor role in embryonic stem cells. Oncogene 2004; 23:4735-44.
44. 2 arrest by caffeine. Radiat Res 1992; 129:224-7.
45. Hall-Jackson CA, Cross D, Morrice N, Smythe C. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 1999; 18:6707-13.
46. Hazeki O, Hazeki K, Katada T, Ui M. Inhibitory effect of wortmannin on phosphatidylinositol 3-kinase-mediated cellular events. J Lipid Mediat Cell Signal 1996; 14:259-61.
47. Mirzayans R, Pollock S, Scott A, Enns L, Andrais B, Murray D. Relationship between the radiosensitizing effect of wortmannin, DNA double-strand break rejoining, and p21WAF1 induction in human normal and tumor-derived cells. Mol Carcinog 2004; 39:164-72.
48. Loegering D, Arlander SJ, Hackbarth J, Vroman BT, Roos-Mattjus P, Hopkins KM, Lieberman HB, Karnitz LM, Kaufmann SH. Rad9 protects cells from topoisomerase poison-induced cell death. J Biol Chem 2004; 279:18641-7.
49. 1/S boundary of the cell cycle after gamma-irradiation due to p21WAF1/CIP1 degradation. Oncogene 2000; 19:3858-65.
50. Wright JA, Keegan K, Herendeen DR, Bentley NJ, Carr AM, Hoekstra MF, Concannon P. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc Natl Acad Sci USA 1998; 95:7445-50.
51. Goodarzi AA, Block W, Lees-Miller SP. The role of ATM and ATR in DNA damage-induced cell cycle control. Prog Cell Cycle Res 2003; 5:393-411.
52. 2 accumulation in irradiated AT cells. J Biol Chem 2003; 278:30869-74.
53. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
54. Sorensen CS, Syljuasen RG, Lukas J, Bartek J. ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 2004; 3:941-5.
55. Takai H, Tominaga K, Motoyama N, Minamishima YA, Nagahama H, Tsukiyama T, Ikeda K, Nakayama K, Nakanishi M, Nakayama K. Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev 2000; 14:1439-47.
56. Abraham R. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001; 15:2177-96.
57. Kim GY, Mercer S, Ewton DZ, Yan Z, Jin K, Friedman E. The stress-activated protein kinases p38 alpha and JNK1 stabilize p21(Cip1) by phosphorylation. J Biol Chem 2002; 277:29792-802.
58. Vidal A, Koff A. Cell-cycle inhibitors: Three families united by a common cause. Gene 2000; 247:1-15.
59. Gong J, Ammanamanchi S, Ko TC, Brattain MG. Transforming growth factor beta 1 increases the stability of p21/WAF1/CIP1 protein and inhibits CDK2 kinase activity in human colon carcinoma FET cells. Cancer Res 2003; 63:3340-6.
60. Morgan DO. Cyclin-dependent kinases: Engines, clocks, and microprocessors. Annu Rev Cell Dev Biol 1997; 13:261-91.
61. Zhu Y, Alvarez C, Doll R, Kurata H, Schebye XM, Parry D, Lees E. Intra-S-phase checkpoint activation by direct CDK2 inhibition. Mol Cell Biol 2004; 24:6268-77.
62. Michieli P, Chedid M, Lin D, Pierce JH, Mercer WE, Givol D. Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res 1994; 54:3391-5.
63. Parker SB, Eichele G, Zhang P, Rawls A, Sands AT, Bradley A, Olson EN, Harper JW, Elledge SJ. p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 1995; 267:1024-7.
64. Paulovich AG, Arrmour CD, Hartwell LH. The Saccharomyces cerevisiae RAD9, RAD17, RAD24 and MEC3 genes are required for tolerating irreparable, ultraviolet-induced DNA damage. Genetics 1998; 150:75-93.
65. Zou L, Cortez D, Elledge SJ. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev 2002; 16:198-208.
66. Weiss RS, Enoch T, Leder P. Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev 2000; 14:1886-98.
67. Weiss RS, Leder P, Vaziri C. Critical role for mouse Hus1 in an S-phase DNA damage cell cycle checkpoint. Mol Cell Biol 2003; 23:791-803.