Sensing, signaling, and responding to DNA damage: Organization of the checkpoint pathways in mammalian cells

Journal of Cellular Biochemistry

Volumn 94, Issue 2, 2005, Pages 298-306

  Li, Lei ^a   Zou, Lee ^b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cell cycle arrest; Cell cycle checkpoints; DNA damage; DNA damage recognition; Genomic instability; Replication interference

Indexed keywords

CELL CYCLE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENOMIC INSTABILITY; GENOTOXICITY; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; GENE; GENETICS; HUMAN; METABOLISM; MITOSIS; PHYSIOLOGY; ULTRAVIOLET RADIATION;

MAMMALIA;

CELL CYCLE PROTEIN; CYCLINE; DNA;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CYCLINS; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENES, CDC; HUMANS; MITOSIS; SIGNAL TRANSDUCTION; ULTRAVIOLET RAYS;

EID: 18444418299     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcb.20355     Document Type: Review

References (69)

1. Abraham RT. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Develop 15:2177-2196.
2. Ahn J, Urist M, Prives C. 2003. Questioning the role of checkpoint kinase 2 in the p53 DNA damage response. J Biol Chem 278:20480-20489.
3. Andegeko Y, Moyal L, Mittelman L, Tsarfaty I, Shiloh Y, Rotman G. 2001. Nuclear retention of ATM at sites of DNA double strand breaks. J Biol Chem 276:38224-38230.
4. Bao S, Lu T, Wang X, Zheng H, Wang LE, Wei Q, Hittelman WN, Li L. 2004. Disruption of the Rad9/Rad1/Hus1 (9-1-1) complex leads to checkpoint signaling and replication defects. Oncogene 23:5586-5593.
5. Bermudez VP, Lindsey-Boltz LA, Cesare AJ, Maniwa Y, Griffith JD, Hurwitz J, Sancar A. 2003. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc Natl Acad Sci USA 100:1633-1638.
6. Brown EJ, Baltimore D. 2000. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 14:397-402.
7. Brown EJ, Baltimore D. 2003. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev 17:615-628.
8. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677-1679.
9. Carney JP, Maser RS, Olivares H, Davis EM, Le Beau M, Yates JR 3rd, Hays L, Morgan WF, Petrini JH. 1998. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: Linkage of double-strand break repair to the cellular DNA damage response. Cell 93:477-486.
10. Carson CT, Schwartz RA, Stracker TH, Lilley CE, Lee DV, Weitzman MD. 2003. The Mre11 complex is required for ATM activation and the G2/M checkpoint. Embo J 22: 6610-6620.
11. Chen MS, Hurov J, White LS, Woodford-Thomas T, Piwnica-Worms H. 2001. Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol Cell Biol 21:3853-3861.
12. Chini CC, Chen J. 2003. Human claspin is required for replication checkpoint control. J Biol Chem 278:30057-30062.
13. Cortez D, Guntuku S, Qin J, Elledge SJ. 2001. ATR and ATRIP: Partners in checkpoint signaling. Science 294: 1713-1716.
14. Costanzo V, Robertson K, Ying CY, Kim E, Awedimento E, Gottesman M, Grieco D, Gautier J. 2000. Reconstitution of an ATM-dependent checkpoint that inhibits chromosomal DNA replication following DNA damage. Mol Cell 6:649-659.
15. Costanzo V, Shechter D, Lupardus PJ, Cimprich KA, Gottesman M, Gautier J. 2003. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol Cell 11:203-213.
16. Desany BA, Alcasabas AA, Bachant JB, Elledge SJ. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev 12:2956-2970.
17. Elledge SJ. 1996. Cell cycle checkpoints: Preventing an identity crisis. Science 274:1664-1672.
18. Ellison V, Stillman B. 2003. Biochemical characterization of DNA damage checkpoint complexes: Clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol 1:E33.
19. Falck J, Mailand N, Syljuasen RG, Bartek J, Lukas J. 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410:842-847.
20. Friedberg EC, Walker GC, Siede W. 1995. In DNA Repair and Mutagenesis. Washington, DC: ASM Press.
21. Gatei M, Young D, Cerosaletti KM, Desai-Mehta A, Spring K, Kozlov S, Lavin MF, Gatti RA, Concannon P, Khanna K. 2000. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat Genet 25:115-119.
22. Giannattasio M, Lazzaro F, Longhese MP, Plevani P, Muzi-Falconi M. 2004. Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. Embo J 23:429-438.
23. Goldberg M, Stucki M, Falck J, D'Amours D, Rahman D, Pappin D, Bartek J, Jackson SP. 2003. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421:952-956.
24. Griffiths DJ, Barbet NC, McCready S, Lehmann AR, Carr AM. 1995. Fission yeast rad17: A homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins. EMBO Journal 14:5812-5823.
25. Hartwell LH, Kastan MB. 1994. Cell cycle control and cancer. Science 266:1821-1828.
26. Higa LA, Mihaylov IS, Banks DP, Zheng J, Zhang H. 2003. Radiation-mediated proteolysis of CDT1 by CUL4-ROC1 and CSN complexes constitutes a new checkpoint. Nat Cell Biol 5:1008-1015.
27. Jallepalli PV, Lengauer C, Vogelstein B, Bunz F. 2003. The Chk2 tumor suppressor is not required for p53 responses in human cancer cells. J Biol Chem 278:20475-20479.
28. Jin J, Shirogane T, Xu L, Nalepa G, Qin J, Elledge SJ, Harper JW. 2003. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25 A protein phosphatase. Genes Dev 17:3062-3074.
29. Kim ST, Xu B, Kastan MB. 2002. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Develop 16:560-570.
30. Kinzler KW, Vogelstein B. 1997. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 386:761.
31. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 18:1423-1438.
32. Kumagai A, Dunphy WG. 2000. Claspin, a novel protein required for the activation of Chkl during a DNA replication checkpoint response in Xenopus egg extracts. Mol Cell 6:839-849.
33. Lim DS, Kim ST, Xu B, Maser RS, Lin J, Petrini JH, Kastan MB. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613-617.
34. Lin SY, Li K, Stewart GS, Elledge SJ. 2004. Human Claspin works with BRCA1 to both positively and negatively regulate cell proliferation. Proc Natl Acad Sci USA 101: 6484-6489.
35. 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 Develop 14:1448-1459.
36. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, Muzi-Falconi M, Newlon CS, Foiani M. 2001. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412:557-561.
37. Lopez-Girona A, Mondesert O, Leatherwood J, Russell P. 1998. Negative regulation of Cdc18 DNA replication protein by Cdc2. Mol Biol Cell 9:63-73.
38. Lou Z, Minter-Dykhouse K, Wu X, Chen J. 2003. MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421:957-961.
39. Majka J, Chung BY, Burgers PM. 2004. Requirement for ATP by the DNA damage checkpoint clamp loader. J Biol Chem 279:20921-20926.
40. Manke IA, Lowery DM, Nguyen A, Yaffe MB. 2003. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636-639.
41. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. 2000. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci USA 97:10389-10394.
42. 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. 2001. ATM-dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Develop 15:1067-1077.
43. McPherson JP, Lemmers B, Hirao A, Hakem A, Abraham J, Migon E, Matysiak-Zablocki E, Tamblyn L, Sanchez-Sweatman O, Khokha R, Squire J, Hande MP, Mak TW, Hakem R. 2004. Collaboration of Brca1 and Chk2 in tumorigenesis. Genes Dev 18:1144-1153.
44. Mochan TA, Venere M, DiTullio RA Jr., Halazonetis TD. 2003. 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res 63:8586-8591.
45. Nakada D, Matsumoto K, Sugimoto K. 2003. ATM-related Tell associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev 17:1957-1962.
46. 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.
47. 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.
48. Shechter D, Costanzo V, Gautier J. 2004. ATR and ATM regulate the timing of DNA replication origin firing. Nat Cell Biol 6:648-655.
49. Sogo JM, Lopes M, Foiani M. 2002. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297:599-602.
50. Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961-966.
51. Takai H, Naka K, Okada Y, Watanabe M, Harada N, Saito S, Anderson CW, Appella E, Nakanishi M, Suzuki H, Nagashima K, Sawa H, Ikeda K, Motoyama N. 2002. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. Embo J 21:5195-5205.
52. Tercero JA, Diffley JF. 2001. Regulation of DNA replication fork progression through damaged DNA by the Mec1/ Rad53 checkpoint. Nature 412:553-557.
53. 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.
54. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. 2003. Requirement of the MRN complex for ATM activation by DNA damage. Embo J 22:5612-5621.
55. Venclovas C, Thelen MP. 2000. Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res 28:2481-2493.
56. Vigo E, Muller H, Prosperini E, Hateboer G, Cartwright P, Moroni MC, Helin K. 1999. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol Cell Biol 19:6379-6395.
57. Wang Y, Qin J. 2003. MSH2 and ATR form a signaling module and regulate two branches of the damage response to DNA methylation. Proc Natl Acad Sci USA 100: 15387-15392.
58. Wang B, Matsuoka S, Carpenter PB, Elledge SJ. 2002. 53BP1, a mediator of the DNA damage checkpoint. Science 298:1435-1438.
59. Wang X, Zou L, Zheng H, Wei Q, Elledge SJ, Li L. 2003. Genomic Instability and Endoreduplication Triggered by RAD17 Deletion. Genes Develop 17:965-970.
60. Weiss RS, Matsuoka S, Elledge SJ, Leder P. 2002. Hus1 acts upstream of Chk1 in a mammalian DNA damage response pathway. Current Biology 12:73-77.
61. Yazdi PT, Wang Y, Zhao S, Patel N, Lee EY, Qin J. 2002. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Develop 16: 571-582.
62. You Z, Kong L, Newport J. 2002. The role of single-stranded DNA and polymerase alpha in establishing the ATR, Hus1 DNA replication checkpoint. J Biol Chem 277: 27088-27093.
63. Yu X, Chini CC, He M, Mer G, Chen J. 2003. The BRCT domain is a phospho-protein binding domain. Science 302:639-642.
64. Zachos G, Rainey MD, Gillespie DA. 2003a. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. Embo J 22:713-723.
65. Zachos G, Rainey MD, Gillespie DA. 2003b. Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO Journal 22:713-723.
66. Zhao S, Weng YC, Yuan SS, Lin YT, Hsu HC, Lin SC, Gerbino E, Song MH, Zdzienicka MZ, Gatti RA, Shay JW, Ziv Y, Shiloh Y, Lee EY. 2000. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405:473-477.
67. Zhou BB, Elledge SJ. 2000. The DNA damage response: Putting checkpoints in perspective. Nature 408:433-439.
68. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.
69. Zou L, Liu D, Elledge SJ. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc Natl Acad Sci USA 100:13827-13832.