The versatile functions of ATM kinase

Biomedical Journal

Volumn 37, Issue 1, 2014, Pages 3-9

  Boohaker, Rebecca ^a   Xu, Bo ^a,b  

^a SOUTHERN RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

ataxia telangiectasia mutated; genome stability; metastasis; mitosis; Snail; spindle checkpoint

Indexed keywords

ATM PROTEIN; CELL CYCLE PROTEIN;

CELL CYCLE REGULATION; DNA REPAIR; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE MUTATION; GENOMIC INSTABILITY; METASTASIS; MITOSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; TUMOR GROWTH; ANIMAL; ATAXIA TELANGIECTASIA; CELL CYCLE CHECKPOINT; GENETICS; HUMAN; SIGNAL TRANSDUCTION;

ANIMALS; ATAXIA TELANGIECTASIA; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; DNA REPAIR; HUMANS; SIGNAL TRANSDUCTION;

EID: 84894178029     PISSN: 23194170     EISSN: None     Source Type: Journal    
DOI: 10.4103/2319-4170.125655     Document Type: Review

References (83)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011;144:646-74.
2. Lavin MF. Ataxia?telangiectasia: From a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 2008;9:759-69.
3. Shiloh Y, Ziv Y. The ATM protein kinase: Regulating the cellular response to genotoxic stress, and more. Nat Rev Mol Cell Biol 2013;14:197-210.
4. Kastan MB, Lim DS. The many substrates and functions of ATM. Nat Rev Mol Cell Biol 2000;1:179-86.
5. Lempiainen H, Halazonetis TD. Emerging common themes in regulation of PIKKs and PI3Ks. EMBO J 2009;28:3067-73.
6. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003;421:499-506.
7. Kozlov SV, Graham ME, Peng C, Chen P, Robinson PJ, Lavin MF. Involvement of novel autophosphorylation sites in ATM activation. EMBO J 2006;25:3504-14.
8. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J 2003;22:5612-21.
9. Lee JH, Paull TT. ATM activation by DNA double?strand breaks through the Mre11?Rad50?Nbs1 complex. Science 2005;308:551-4.
10. Lee JH, Paull TT. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 2004;304:93-6.
11. Lee JH, Paull TT. Activation and regulation of ATM kinase activity in response to DNA double?strand breaks. Oncogene 2007;26:7741-8.
12. Kanu N, Behrens A. ATMIN defines an NBS1?independent pathway of ATM signalling. EMBO J 2007;26:2933-41.
13. Mochan TA, Venere M, DiTullio RA Jr, Halazonetis TD. 53BP1 and NFBD1/MDC1?Nbs1 function in parallel interacting pathways activating ataxia?telangiectasia mutated (ATM) in response to DNA damage. Cancer Res 2003;63:8586-91.
14. Goldberg M, Stucki M, Falck J, D'Amours D, Rahman D, Pappin D, et al. MDC1 is required for the intra?S?phase DNA damage checkpoint. Nature 2003;421:952-6.
15. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double?strand breaks. Cell 2005;123:1213-26.
16. Guo JY, Yamada A, Kajino T, Wu JQ, Tang W, Freel CD, et al. Aven?dependent activation of ATM following DNA damage. Curr Biol 2008;18:933-42.
17. Tsai WB, Chung YM, Takahashi Y, Xu Z, Hu MC. Functional interaction between FOXO3 and ATM regulates DNA damage response. Nat Cell Biol 2008;10:460-7.
18. Wu J, Chen Y, Lu LY, Wu Y, Paulsen MT, Ljungman M, et al. Chfr and RNF8 synergistically regulate ATM activation. Nat Struct Mol Biol 2011;18:761-8.
19. Kim YC, Gerlitz G, Furusawa T, Catez F, Nussenzweig A, Oh KS, et al. Activation of ATM depends on chromatin interactions occurring before induction of DNA damage. Nat Cell Biol 2009;11:92-6.
20. Gupta A, Sharma GG, Young CS, Agarwal M, Smith ER, Paull TT, et al. Involvement of human MOF in ATM function. Mol Cell Biol 2005;25:5292-305.
21. Kastan MB, Lim DS, Kim ST, Xu B, Canman C. Multiple signaling pathways involving ATM. Cold Spring Harb Symp Quant Biol 2000;65:521-6.
22. Shreeram S, Demidov ON, Hee WK, Yamaguchi H, Onishi N, Kek C, et al. Wip1 phosphatase modulates ATM?dependent signaling pathways. Mol Cell 2006;23:757-64.
23. Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA. ATM is down?regulated by N?Myc?regulated microRNA?421. Proc Natl Acad Sci USA 2010;107:1506-11.
24. Song L, Lin C, Wu Z, Gong H, Zeng Y, Wu J, et al. miR?18a impairs DNA damage response through downregulation of ataxia telangiectasia mutated (ATM) kinase. PLoS One 2011;6:e25454.
25. Guo X, Yang C, Qian X, Lei T, Li Y, Shen H, et al. Estrogen Receptor alpha Regulates ATM Expression through miRNAs in Breast Cancer. Clin Cancer Res 2013;19:4994-5002.
26. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, et al. Atm?deficient mice: A paradigm of ataxia telangiectasia. Cell 1996;86:159-71.
27. 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.
28. Daniel JA, Pellegrini M, Lee JH, Paull TT, Feigenbaum L, Nussenzweig A. Multiple autophosphorylation sites are dispensable for murine ATM activation in vivo. J Cell Biol 2008;183:777-83.
29. Daniel JA, Pellegrini M, Lee BS, Guo Z, Filsuf D, Belkina NV, et al. Loss of ATM kinase activity leads to embryonic lethality in mice. J Cell Biol 2012;198:295-304.
30. Yamamoto K, Wang Y, Jiang W, Liu X, Dubois RL, Lin CS, et al. Kinase?dead ATM protein causes genomic instability and early embryonic lethality in mice. J Cell Biol 2012;198:305-13.
31. Hammond EM, Giaccia AJ. The role of ATM and ATR in the cellular response to hypoxia and re?oxygenation. DNA Repair (Amst) 2004;3:1117-22.
32. Hunt CR, Pandita RK, Laszlo A, Higashikubo R, Agarwal M, Kitamura T, et al. Hyperthermia activates a subset of ataxia?telangiectasia mutated effectors independent of DNA strand breaks and heat shock protein 70 status. Cancer Res 2007;67:3010-7.
33. Watters D, Kedar P, Spring K, Bjorkman J, Chen P, Gatei M, et al. Localization of a portion of extranuclear ATM to peroxisomes. J Biol Chem 1999;274:34277-82.
34. Li J, Han YR, Plummer MR, Herrup K. Cytoplasmic ATM in neurons modulates synaptic function. Curr Biol 2009;19:2091-6.
35. Lim DS, Kirsch DG, Canman CE, Ahn JH, Ziv Y, Newman LS, et al. ATM binds to beta?adaptin in cytoplasmic vesicles. Proc Natl Acad Sci USA 1998;95:10146-51.
36. Yang DQ, Kastan MB. Participation of ATM in insulin signalling through phosphorylation of eIF?4E?binding protein 1. Nat Cell Biol 2000;2:893-8.
37. Valentin?Vega YA, Kastan MB. A new role for ATM: Regulating mitochondrial function and mitophagy. Autophagy 2012;8:840-1.
38. Jackson SP, Bartek J. The DNA?damage response in human biology and disease. Nature 2009;461:1071-8.
39. Kastan MB, Bartek J. Cell?cycle checkpoints and cancer. Nature 2004;432:316-23.
40. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER 3rd, Hurov KE, Luo J, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007;316:1160-6.
41. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat Rev Cancer 2003;3:155-68.
42. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998;281:1677-9.
43. Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998;281:1674-7.
44. Maya R, Balass M, Kim ST, Shkedy D, Leal JF, Shifman O, et al. ATM?dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Dev 2001;15:1067-77.
45. Gannon HS, Woda BA, Jones SN. ATM phosphorylation of Mdm2 Ser394 regulates the amplitude and duration of the DNA damage response in mice. Cancer Cell 2012;21:668-79.
46. Dornan D, Shimizu H, Mah A, Dudhela T, Eby M, O'Rourke K, et al. ATM engages autodegradation of the E3 ubiquitin ligase COP1 after DNA damage. Science 2006;313:1122-6.
47. Chen L, Gilkes DM, Pan Y, Lane WS, Chen J. ATM and Chk2?dependent phosphorylation of MDMX contribute to p53 activation after DNA damage. EMBO J 2005;24:3411-22.
48. Batchelor E, Mock CS, Bhan I, Loewer A, Lahav G. Recurrent initiation: A mechanism for triggering p53 pulses in response to DNA damage. Mol Cell 2008;30:277-89.
49. Kastan MB. DNA damage responses: Mechanisms and roles in human disease: 2007 G.H.A. Clowes Memorial Award Lecture. Mol Cancer Res 2008;6:517-24.
50. 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.
51. Woo RA, Poon RY. Cyclin?dependent kinases and S phase control in mammalian cells. Cell Cycle 2003;2:316-24.
52. Xu B, Kim ST, Lim DS, Kastan MB. Two molecularly distinct G (2)/M checkpoints are induced by ionizing irradiation. Mol Cell Biol 2002;22:1049-59.
53. Xu B, Kim S, Kastan MB. Involvement of Brca1 in S?phase and G (2)?phase checkpoints after ionizing irradiation. Mol Cell Biol 2001;21:3445-50.
54. Xu B, O'Donnell AH, Kim ST, Kastan MB. Phosphorylation of serine 1387 in Brca1 is specifically required for the Atm?mediated S?phase checkpoint after ionizing irradiation. Cancer Res 2002;62:4588-91.
55. Ahn JY, Schwarz JK, Piwnica?Worms H, Canman CE. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res 2000;60:5934-6.
56. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia?mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci USA 2000;97:10389-94.
57. Geng C, He B, Xu L, Barbieri CE, Eedunuri VK, Chew SA, et al. Prostate cancer?associated mutations in speckle?type POZ protein (SPOP) regulate steroid receptor coactivator 3 protein turnover. Proc Natl Acad Sci USA 2013;110:6997-7002.
58. Bao S, Tibbetts RS, Brumbaugh KM, Fang Y, Richardson DA, Ali A, et al. ATR/ATM?mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 2001;411:969-74.
59. Garg R, Callens S, Lim DS, Canman CE, Kastan MB, Xu B. Chromatin association of rad17 is required for an ataxia telangiectasia and rad?related kinase?mediated S?phase checkpoint in response to low?dose ultraviolet radiation. Mol Cancer Res 2004;2:362-9.
60. Tang X, Hui ZG, Cui XL, Garg R, Kastan MB, Xu B. A novel ATM?dependent pathway regulates protein phosphatase 1 in response to DNA damage. Mol Cell Biol 2008;28:2559-66.
61. Matsuoka S, Huang M, Elledge SJ. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998;282:1893-7.
62. Foley EA, Kapoor TM. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 2013;14:25-37.
63. Musacchio A, Hardwick KG. The spindle checkpoint: Structural insights into dynamic signalling. Nat Rev Mol Cell Biol 2002;3:731-41.
64. May KM, Hardwick KG. The spindle checkpoint. J Cell Sci 2006;119:4139-42.
65. Shigeta T, Takagi M, Delia D, Chessa L, Iwata S, Kanke Y, et al. Defective control of apoptosis and mitotic spindle checkpoint in heterozygous carriers of ATM mutations. Cancer Res 1999;59:2602-7.
66. Takagi M, Delia D, Chessa L, Iwata S, Shigeta T, Kanke Y, et al. Defective control of apoptosis, radiosensitivity, and spindle checkpoint in ataxia telangiectasia. Cancer Res 1998;58:4923-9.
67. Shen KC, Heng H, Wang Y, Lu S, Liu G, Deng CX, et al. ATM and p21 cooperate to suppress aneuploidy and subsequent tumor development. Cancer Res 2005;65:8747-53.
68. Iourov IY, Vorsanova SG, Liehr T, Kolotii AD, Yurov YB. Increased chromosome instability dramatically disrupts neural genome integrity and mediates cerebellar degeneration in the ataxia?telangiectasia brain. Hum Mol Genet 2009;18:2656-69.
69. Yang C, Tang X, Guo X, Niikura Y, Kitagawa K, Cui K, et al. Aurora?B mediated ATM serine 1403 phosphorylation is required for mitotic ATM activation and the spindle checkpoint. Mol Cell 2011;44:597-608.
70. Yang C, Wang H, Xu Y, Brinkman KL, Ishiyama H, Wong ST, et al. The kinetochore protein Bub1 participates in the DNA damage response. DNA Repair (Amst) 2012;11:185-91.
71. Morrow CJ, Tighe A, Johnson VL, Scott MI, Ditchfield C, Taylor SS. Bub1 and aurora B cooperate to maintain BubR1?mediated inhibition of APC/CCdc20. J Cell Sci 2005;118:3639-52.
72. Fu J, Bian M, Jiang Q, Zhang C. Roles of Aurora kinases in mitosis and tumorigenesis. Mol Cancer Res 2007;5:1-10.
73. Fang G, Yu H, Kirschner MW. Control of mitotic transitions by the anaphase?promoting complex. Philos Trans R Soc Lond B Biol Sci 1999;354:1583-90.
74. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, et al. Oncogene?induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006;444:633-7.
75. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, et al. DNA damage response as a candidate anti?cancer barrier in early human tumorigenesis. Nature 2005;434:864-70.
76. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005;434:907-13.
77. Yang MH, Chang SY, Chiou SH, Liu CJ, Chi CW, Chen PM, et al. Overexpression of NBS1 induces epithelial?mesenchymal transition and co?expression of NBS1 and Snail predicts metastasis of head and neck cancer. Oncogene 2007;26:1459-67.
78. Thiery JP. Epithelial?mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
79. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial?mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005;17:548-58.
80. Nieto MA. The snail superfamily of zinc?finger transcription factors. Nat Rev Mol Cell Biol 2002;3:155-66.
81. Sun M, Guo X, Qian X, Wang H, Yang C, Brinkman KL, et al. Activation of the ATM?Snail pathway promotes breast cancer metastasis. J Mol Cell Biol 2012;4:304-15.
82. Boohaker RJ, Cui X, Stackhouse M, Xu B. ATM?mediated Snail Serine 100 phosphorylation regulates cellular radiosensitivity. Radiother Oncol 2013;108:403-8.
83. He H, Tian D, Guo J, Liu M, Chen Z, Hamdy FC, et al. DNA damage response in peritumoral regions of oesophageal cancer microenvironment. Carcinogenesis 2013;34:139-45.