ATM and ATR: Sensing DNA damage

World Journal of Gastroenterology

Volumn 10, Issue 2, 2004, Pages 155-160

  Yang, Jun ^a   Xu, Zheng Ping ^a   Huang, Yun ^a   Hamrick, Hope E ^b   Duerksen Hughes, Penelope J ^c   Yu, Ying Nian ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b WELLESLEY COLLEGE   (United States)

^c LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ATM PROTEIN; ATR PROTEIN; CELL CYCLE PROTEIN; CISPLATIN; DNA; DOXORUBICIN; ETOPOSIDE; FRP1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOMYCIN C; PROTEIN KINASE; PROTEIN P53; PROTEIN TYROSINE KINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL; ATAXIA TELANGIECTASIA; BIOCHEMISTRY; CANCER; CELL CYCLE; CELL DEATH; CELL FUNCTION; DNA DAMAGE; DNA REPAIR; DRUG EFFECT; ENZYME ACTIVATION; GENE EXPRESSION; GENE MUTATION; GENETIC DISORDER; GENOTOXICITY; HUMAN; NONHUMAN; PHYSIOLOGY; PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STRESS;

EID: 1042292696     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v10.i2.155     Document Type: Review

References (92)

1. Yang J, Yu Y, Duerksen-Hughes PJ. Protein kinases and their involvement in the cellular responses to genotoxic stress. Mutat Res 2003; 543: 31-58
2. Liu Y, Guyton KZ, Gorospe M, Xu Q, Lee JC, Holbrook NJ. Differential activation of ERK, JNK/SAPK, and p38/CSBP/RK map kinase family members during the cellular response to arsenite. Free Radic Biol Med 1996; 21: 771-781
3. Liu ZG, Baskaran R, Lea-Chou ET, Wood LD, Chen Y, Karin M, Wang JY. Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 1996; 384: 273-276
4. Sanchez-Prieto R, Rojas JM, Taya Y, Gutkind JS. A role for the p38 mitogen-activated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chemotherapeutic agents. Cancer Res 2000; 60: 2464-2472
5. Kharbanda S, Saxena S, Yoshida K, Pandey P, Kaneki M, Wang Q, Cheng K, Chen YN, Campbell A, Sudha T, Yuan ZM, Narula J, Weichselbaum R, Nalin C, Kufe D. Translocation of SAPK/JNK to mitochondria and interaction with Bcl-x(L) in response to DNA damage. J Biol Chem 2000; 275: 322-327
6. Zhang Y, Zhong S, Dong Z, Chen N, Bode AM, Ma W, Dong Z. UVA induces Ser381 phosphorylation of p90RSK/MAPKAP-K1 via ERK and JNK pathways. J Biol Chem 2001; 276: 14572-14580
7. She QB, Chen N, Dong Z. ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J Biol Chem 2000; 275: 20444-20449
8. Akechi M, Ito M, Uemura K, Takamatsu N, Yamashita S, Uchiyama K, Yoshioka K, Shiba T. Expression of JNK cascade scaffold protein JSAP1 in the mouse nervous system. Neurosci Res 2001; 39: 391-400
9. Tawadros T, Formenton A, Dudler J, Thompson N, Nicod P, Leisinger HJ, Waeber G, Haefliger JA. The scaffold protein IB1/JIP-1 controls the activation of JNK in rat stressed urothelium. J Cell Sci 2002; 115(pt2): 385-393
10. Ito M, Akechi M, Hirose R, Ichimura M, Takamatsu N, Xu P, Nakabeppu Y, Tadayoshi S, Yamamoto K, Yoshioka K. Isoforms of JSAP1 scaffold protein generated through alternative splicing. Gene 2000; 255: 229-234
11. Yang J, Duerksen-Hughes P. A new approach to identifying genotoxic carcinogens: p53 induction as an indicator of genotoxic damage. Carcinogenesis 1998; 19: 1117-1125
12. Wahl GM, Linke SP, Paulson TG, Huang LC. Maintaining genetic stability through TP53 mediated checkpoint control. Cancer Serv 1997; 29: 183-219
13. Lowndes NF, Murguia JR. Sensing and responding to DNA damage. Curr Opin Genet Dev 2000; 10: 17-25
14. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001; 15: 2177-2196
15. Rouse J, Jackson SP. Interfaces between the detection, signaling, and repair of DNA damage. Science 2002; 297: 547-551
16. O'Connell MJ, Walworth NC, Carr AM. The G2-phase DNA-damage checkpoint. Trends Cell Biol 2000; 10: 296-303
17. Green CM, Erdjument-Bromage H, Tempst P, Lowndes NF. A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr Biol 2000; 10: 39-42
18. Roos-Mattjus P, Vroman BT, Burtelow MA, Rauen M, Eapen AK, Karnitz LM. Genotoxin-induced Rad9-Hus1-Rad1 (9-1-1) chromatin association is an early checkpoint signaling event. J Biol Chem 2002; 277: 43809-43812
19. Durocher D, Jackson SP. DNA-PK, ATM and ATR as sensors of DNA damage: Variations on a theme? Curr Opin Cell Biol 2001; 13: 225-231
20. Rotman G, Shiloh Y. ATM: A mediator of multiple responses to genotoxic stress. Oncogene 1999; 18: 6135-6144
21. Chan ED, Winston BW, Jarpe MB, Wynes MW, Riches DW. Preferential activation of the p46 isoform of JNK/SAPK in mouse macrophages by TNF alpha. Proc Natl Acad Sci U S A 1997; 94: 13169-13174
22. Bao S, Tibbetts RS, Brumbaugh KM, Fang Y, Richardson DA, Ali A, Chen SM, Abraham RT, Wang XF. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 2001; 411: 969-974
23. Plumb MA, Smith GC, Cunniffe SM, Jackson SP, O'Neill P. DNA-PK activation by ionizing radiation-induced DNA single-strand breaks. Int J Radiat Biol 1999; 75: 553-561
24. Jackson SP. DNA-dependent protein kinase. Int J Biochem Cell Biol 1997; 29: 935-938
25. Gately DP, Hittle JC, Chan GK, Yen TJ. Characterization of ATM expression, localization, and associated DNA-dependent protein kinase activity. Mol Biol Cell 1998; 9: 2361-2374
26. Pandita TK, Lieberman HB, Lim DS, Dhar S, Zheng W, Taya Y, Kastan MB. Ionizing radiation activates the ATM kinase throughout the cell cycle. Oncogene 2000; 19: 1386-1391
27. Andegeko Y, Moyal L, Mittelman L, Tsarfaty I, Shiloh Y, Rotman G. Nuclear retention of ATM at sites of DNA double strand breaks. J Biol Chem 2001; 276: 38224-38230
28. Wright JA, Keegan KS, Herendeen DR, Bentley NJ, Carr AM, Hoekstra MF, Concannon P. Protein kinase mutants of human ATR increases sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc Natl Acad Sci U S A 1998; 95: 7445-7450
29. Hekmat-Nejad M, You Z, Yee MC, Newport JW, Cimprich KA. Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr Biol 2000; 10: 1565-1573
30. Wahl GM, Carr AM. The evolution of diverse biological responses to DNA damage: Insights from yeast and p53. Nature Cell Biol 2001; 3: E227-E286
31. Suzuki K, Kodama S, Watanabe M. Recruitment of ATM protein to double strand DNA irradiated with ionizing radiation. J Biol Chem 1999; 274: 25571-25575
32. Smith GC, Cary RB, Lakin ND, Hann BC, Teo SH, Chen DJ, Jackson SP. Purification and DNA binding properties of the ataxia-telangiectasia gene product ATM. Proc Natl Acad Sci U S A 1999; 96: 11134-11139
33. Guo Z, Kumagai A, Wang SX, Dunphy WG. 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 2000; 14: 2745-2756
34. Unsal-Kacmaz K, Makhov AM, Griffith JD, Sancar A. Preferential binding of ATR protein to UV-damaged DNA. Proc Natl Acad Sci U S A 2002; 99: 6673-6678
35. Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 2000; 14: 927-939
36. Kim GD, Choi YH, Dimtchev A, Jeong SJ, Dritschilo A, Jung M. Sensing of ionizing radiation-induced DNA damage by ATM through interaction with histone deacetylase. J Biol Chem 1999; 274: 31127-31130
37. 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
38. Tibbetts RS, Cortez D, Brumbaugh KM, Scully R, Livingston D, Elledge SJ, Abraham RT. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev 2000; 14: 2989-3002
39. Schmidt DR, Schreiber SL. Molecular association between ATR and two components of the nucleosome remodeling and deacetylating complex, HDAC2 and CHD4. Biochemistry 1999; 38: 14711-14717
40. Wang JY. Cellular responses to DNA damage. Curr Opin Cell Biol 1998; 10: 240-247
41. Wen ST, Van Etten RA. The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev 1997; 11: 2456-2467
42. Kharbanda S, Ren R, Pandey P, Shafman TD, Feller SM, Weichselbaum RR, Kufe DW. Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature 1995; 376: 785-788
43. Shafman T, Khanna KK, Kedar P, Spring K, Kozlov S, Yen T, Hobson K, Gatei M, Zhang N, Watters D, Egerton M, Shiloh Y, Kharbanda S, Kufe D, Lavin MF. Interaction between ATM protein and c-Abl in response to DNA damage. Nature 1997; 387: 520-523
44. Baskaran R, Wood LD, Whitaker LL, Canman CE, Morgan SE, Xu Y, Barlow C, Baltimore D, Wynshaw-Boris A, Kastan MB, Wang JY. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 1997; 387: 516-519
45. Shangary S, Brown KD, Adamson AW, Edmonson S, Ng B, Pandita TK, Yalowich J, Taccioli GE, Baskaran R. Regulation of DNA-dependent protein kinase activity by ionizing radiation-activated Abl kinase is an ATM-dependent process. J Biol Chem 2000; 275: 30163-30168
46. Takao N, Mori R, Kato H, Shinohara A, Yamamoto K. c-Abl tyrosine kinase is not essential for ataxia telangiectasia mutated functions in chromosomal maintenance. J Biol Chem 2000; 275: 725-728
47. Yuan ZM, Huang Y, Whang Y, Sawyers C, Weichselbaum R, Kharbanda S, Kufe D. Role of c-Abl tyrosine kinase in growth arrest response to DNA damage. Nature 1996; 382: 272-274
48. Wen ST, Jackson PK, Van Etten RA. The cytostatic function of c-Abl is controlled by multiple nuclear localization signals and requires the p53 and Rb tumor suppressor gene products. EMBO J 1996; 15: 1583-1595
49. Sionov RV, Moallem E, Berger M, Kazaz A, Gerlitz O, Ben-Neriah Y, Oren M, Haupt Y. C-Abl neutralizes the inhibitory effect of Mdm2 on p53. J Biol Chem 1999; 274: 8371-8374
50. Sionov RV, Coen S, Goldberg Z, Berger M, Bercovich B, Ben-Neria Y, Ciechanover A, Haupt Y. C-Abl regulates p53 levels under normal and stress conditions by preventing its nuclear export and ubiquitination. Mol Cell Biol 2001; 21: 5869-5878
51. Huang Y, Yuan ZM, Ishiko T, Nakada S, Utsugisawa T, Kato T, Kharbanda S, Kufe DW. Pro-apoptotic effect of the c-Abl tyrosine kinase in the cellular response to 1-beta-D-arabinofuranosylcytosine. Oncogene 1997; 15: 1947-1952
52. Yuan ZM, Huang Y, Ishiko T, Kharbanda S, Weichselbaum R, Kufe, D. Regulation of DNA damage-induced apoptosis by the c-Abl tyrosine kinase. Proc Natl Acad Sci U S A 1997; 94: 1437-1440
53. Shaul Y. C-Abl: Activation and nuclear targets. Cell Death Differ 2000; 7: 10-16
54. Gong JG, Costanzo A, Yang HQ, Melino G, Kaelin WG Jr, Levrero M, Wang JY. The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature 1999; 399: 806-809
55. Agami R, Blandino G, Oren M, Shaul Y. Interaction of c-Abl and p73alpha and their collaboration to induce apoptosis. Nature 1999; 399: 809-813
56. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano, JD. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998; 281: 1677-1679
57. Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, Smorodinsky NI, Prives C, Reiss Y, Shiloh Y, Ziv Y. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998; 281: 1674-1677
58. Nakagawa K, Taya, Y, Tamai K, Yamaizumi M. Requirement of ATM in phosphorylation of the human p53 protein at serine 15 following DNA double-strand breaks. Mol Cell Biol 1999; 19: 2828-2834
59. Tibbetts RS, Brumbaugh KM, 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: 152-157
60. Waterman MJ, Stavridi ES, Waterman JL, Halazonetis TD. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat Genet 1998; 19: 175-178
61. Saito S, Goodarzi AA, Higashimoto Y, Noda Y, Lees-Miller SP, Appella E, Anderson CW. ATM mediates phosphorylation at multiple p53 sites, including Ser(46), in responses to ionizing radiation. J Biol Chem 2002; 277: 12491-12494
62. Alarcon-Vargas D, Ronai Z. p53-Mdm2 - The affair that never ends. Carcinogenesis 2002; 23: 541-547
63. Hirao A, Kong YY, Matsuoka S, Wakeham A, Ruland 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: 1824-1827
64. 1 by stabilizing p53. Genes Dev 2000; 14: 278-288
65. Chehab NH, Malikzay A, Stavridi ES, Halazonetis TD. Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc Natl Acad Sci U S A 1999; 96: 13777-13782
66. Khosravi R, Maya R, Gottlieb T, Oren M, Shiloh Y, Shkedy D. Rapid ATM-dependent phosphorylation of MDM2 precedes p53 accumulation in response to DNA damage. Proc Natl Acad Sci U S A 1999; 96: 14973-14977
67. De Toledo SM, Azzam EI, Dahlberg WK, Gooding TB, Little JB. ATM complexes with HDM2 and promotes its rapid phosphorylation in a p53- independent manner in normal and tumor human cells exposed to ionizing radiation. Oncogene 2000; 19: 6185-6193
68. Maya R, Balass M, Kim ST, Shkedy D, Leal JF, Shifman O, Moas M, Buschmann T, Ronai Z, Shiloh Y, Kastan MB, Katzir E, Oren M. ATM-dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Dev 2001; 15: 1067-1077
69. Tang D, Wu D, Hirao A, Lahti JM, Liu L, Mazza B, Kidd VJ, Mak TW, Ingram AJ. ERK activation mediates cell cycle arrest and apoptosis after DNA damage independently of p53. J Biol Chem 2002; 227: 12710-12717
70. Zhang Y, Ma WY, Kaji A, Bode AM, Dong Z. Requirement of ATM in UVA-induced signaling and apoptosis. J Biol Chem 2002; 277: 3124-3131
71. Wang X, McGowan CH, Zhao M, He L, Downey JS, Fearns C, Wang Y, Huang S, Han J. Involvement of the MKK6-p38γ cascade in γ-radiation-induced cell cycle arrest. Mol Cell Biol 2000; 20: 4543-4552
72. Sanchez-Prieto R, Sanchez-Arevalo VJ, Servitja JM, Gutkind JS. Regulation of p73 by c-Abl through the p38 MAP kinase pathway. Oncogene 2002; 21: 974-979
73. Pandey P, Raingeaud J, Kaneki M, Weichselbaum R, Davis RJ, Kufe D, Kharbanda S. Activation of p38 mitogen-activated protein kinase by c-Abl-dependent and -independent mechanisms. J Biol Chem 1996; 271: 23775-23779
74. Cong F, Goff SP. C-Abl-induced apoptosis, but not cell cycle arrest, requires mitogen-activated protein kinase kinase 6 activation. Proc Natl Acad Sci U S A 1999; 96: 13819-13824
75. Ito Y, Pandey P, Sathyanarayana P, Ling P, Rana A, Weochselbaum R, Tan TH, Kufe D, Kharbanda S. Interaction of hemotopoietic progenitor kinase S and c-Abl tyrosine kinase in response to genotoxic stress. J Biol Chem 2001; 276: 18130-18138
76. Liu RY, Fan C, Liu G, Olashaw NE, Zuckerman KS. Activation of p38 mitogen-activated protein kinase is required for tumor necrosis factor-α-supported proliferation of leukemia and lymphoma cell lines. J Biol Chem 2000; 275: 21086-21093
77. Bar-Shira A, Rashi-Elkeles S, Zlochover L, Moyal L, Smorodinsky NI, Seger R, Shiloh Y. ATM-dependent activation of the gene encoding MAP kinase phosphatase 5 by the radiomimetic DNA damage. Oncogene 2002; 21: 849-855
78. Ejima Y, Yang L, Sasaki MS. Aberrant splicing of the ATM gene associated with shortening of the intronic mononucleotide tract in human colon tumor cell lines: A novel mutation target of microsatellite instability. Int J Cancer 2000; 86: 262-268
79. Shen CY, Yu JC, Lo YL, Kuo CH, Yue CT, Jou YS, Huang CS, Lung JC, Wu CW. Genome-wide search for loss of heterozygosity using laser capture microdissected tissue of breast carcinoma: An implication for mutator phenotype and breast cancer pathogenesis. Cancer Res 2000; 60: 3884-3892
80. Worgul BV, Smilenov L, Brenner DJ, Junk A, Zhou W, Hall EJ. Atm heterozygous mice are more sensitive to radiation-induced cataracts than are their wild-type counterparts. Proc Natl Acad Sci U S A 2002; 99: 9836-9839
81. Spring K, Ahangari F, Scott SP, Waring P, Purdie DM, Chen PC, Hourigan K, Ramsay J, McKinnon PJ, Swift M, Lavin MF: Mice heterozygous for mutation in Atm, the gene involved in ataxia-telangiectasia, have heightened susceptibility to cancer. Nat Genet 2002; 32: 185-190
82. Concannon P. ATM heterozygosity and cancer risk. Nat Genet 2002; 32: 89-90
83. Brown EJ, Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 2000; 14: 397-402
84. 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: 479-482
85. Cliby WA, Roberts CJ, 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: 159-169
86. Smith GC, D'Adda Di Fagagna F, Lakin ND, Jackson SP. Cleavage and inactivation of ATM during apoptosis. Mol Cell Biol 1999; 19: 6076-6084
87. Hotti A, Jarvinen K, Siivola P, Holtta E. Caspases and mitochondria in c-Myc-induced apoptosis: Identification of ATM as a new target of caspases. Oncogene 2000; 19: 2354-2362
88. Tong X, Liu B, Dong Y, Sun Z. Cleavage of ATM during radiation-induced apoptosis: Caspase-3-like apoptotic protease as a candidate. Int J Radiat Biol 2000; 76: 1387-1395
89. Cortez D, Guntuku S, Qin J, Elledge SJ. ATR and ATRIP: Partners in checkpoint signaling. Science 2001; 294: 1713-1716
90. Williams GM, Weisburger JH. Chemical Carcinogenesis. New York, NY, Pergamon Press 1991
91. Smart RC. Carcinogenesis. Norwalk, CT, Appleton Lange 1994
92. Yang J, Yu Y, Hamrick HE, Duerksen-Hughes PJ. ATM, ATR, and DNA-PK: Initiators of the cellular genotoxic stress responses. Carcinogenesis 2003; 24: 1571-1580