The DNA damage response: putting checkpoints in perspective (original) (raw)

• George, J., Castellazzi, M. & Buttin, G. Prophage induction and cell division in E. coli. III. Mutations sfiA and sfiB restore division in tif and lon strains and permit the expression of mutator properties of tif. Mol. Gen. Genet. 140, 309– 332 ( 1975).
  CAS PubMed Google Scholar
• Painter, R. B. & Young, B. R. Radiosensitivity in ataxia-telangiectasia: A new explanation. Proc. Natl Acad. Sci. USA 77, 7315– 7317 (1980).
  ADS CAS PubMed PubMed Central Google Scholar
• Weinert, T. A. & Hartwell, L. H. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241, 317– 322 ( 1988).
  ADS CAS PubMed Google Scholar
• Cortez, D., Wang, Y., Qin, J. & Elledge, S. J. Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 286, 1162– 1166 (1999).
  CAS PubMed Google Scholar
• Lim, D. S. et al. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404, 613– 617 (2000).
  ADS CAS PubMed Google Scholar
• Gatei, M. et al. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nature Genet. 25, 115– 119 (2000).
  CAS PubMed Google Scholar
• Zhao, S. et al. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405, 473– 477 (2000).
  ADS CAS PubMed Google Scholar
• Wu, X. et al. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405, 477 – 482 (2000).
  ADS CAS PubMed Google Scholar
• Martin, S. G., Laroche, T., Suka, N., Grunstein, M. & Gasser, S. M. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell 97, 621– 633 (1999).
  CAS PubMed Google Scholar
• Mills, K. D., Sinclair, D. A. & Guarente, L. MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell 97, 609– 620 (1999).
  CAS PubMed Google Scholar
• Elledge, S. J. Cell cycle checkpoints: preventing an identity crisis. Science 274, 1664– 1672 ( 1996).
  ADS CAS PubMed Google Scholar
• Naito, T., Matsuura, A. & Ishikawa, F. Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nature Genet. 20, 203– 206 (1998).
  CAS PubMed Google Scholar
• Ritchie, K. B., Mallory, J. C. & Petes, T. D. Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 6065– 6075 (1999).
  CAS PubMed PubMed Central Google Scholar
• Lowe, S. W., Schmitt, E. M., Smith, S. W., Osborne, B. A. & Jacks, T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362, 847– 849 (1993).
  ADS CAS PubMed Google Scholar
• Clarke, A. R. et al. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362, 849– 852 (1993).
  ADS CAS PubMed Google Scholar
• Xu, Y. & Baltimore, D. Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 10, 2401– 2410 (1996).
  CAS PubMed Google Scholar
• Hirao, A. et al. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287, 1824– 1827 (2000).
  ADS CAS PubMed Google Scholar
• Brown, E. J. & Baltimore, D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397– 402 (2000).
  CAS PubMed PubMed Central Google Scholar
• de Klein, A. et al. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10, 479– 482 (2000).
  CAS PubMed Google Scholar
• Liu, Q. 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 , 1448– 1459 (2000).
  CAS PubMed PubMed Central Google Scholar
• Takai, H. et al. Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev. 14, 1439– 1447 (2000).
  CAS PubMed PubMed Central Google Scholar
• Rotman, G. & Shiloh, Y. Ataxia-telangiectasia: is ATM a sensor of oxidative damage and stress? BioEssays 19, 911– 917 (1997).
  CAS PubMed Google Scholar
• Sun, Z., Hsiao, J., Fay, D. S. & Stern, D. F. Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science 281, 272– 274 ( 1998).
  ADS CAS PubMed Google Scholar
• Emili, A. MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol. Cell 2, 183– 189. ( 1998).
  CAS PubMed Google Scholar
• Vialard, J. E., Gilbert, C. S., Green, C. M. & Lowndes, N. F. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J. 17, 5678– 5688 ( 1998).
  Google Scholar
• Sanchez, Y. et al. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286, 1166– 1171 (1999).
  CAS PubMed Google Scholar
• Durocher, D., Henckel, J., Fersht, A. R. & Jackson, S. P. The FHA domain is a modular phosphopeptide recognition motif. Mol. Cell 4, 387– 394 ( 1999).
  CAS PubMed Google Scholar
• Liao, H., Byeon, I. J. & Tsai, M. D. Structure and function of a new phosphopeptide-binding domain containing the FHA2 of Rad53. J. Mol. Biol. 294, 1041– 1049 (1999).
  CAS PubMed Google Scholar
• Wang, Z. Q. et al. Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9, 509– 520 (1995).
  CAS PubMed Google Scholar
• Jimenez, G. S. et al. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 400, 81– 83 (1999).
  ADS CAS PubMed Google Scholar
• O'Connell, M. J., Walworth, N. C. & Carr, A. M. The G2-phase DNA damage checkpoint. Trends Cell Biol. 10, 296– 303 ( 2000).
  CAS PubMed Google Scholar
• Volkmer, E. & Karnitz, L. M. Human homologs of Schizosaccharomyces pombe rad1, hus1, and rad9 form a DNA damage-responsive protein complex. J. Biol. Chem. 274, 567– 570 (1999).
  CAS PubMed Google Scholar
• Weiss, R. S., Enoch, T. & Leder, P. Inactivation of mouse hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev. 14, 1886– 1898 (2000).
  CAS PubMed PubMed Central Google Scholar
• Sugimoto, K., Ando, S., Shimomura, T. & Matsumoto, K. Rfc5, a replication factor C component, is required for regulation of Rad53 protein kinase in the yeast checkpoint pathway. Mol. Cell. Biol. 17, 5905– 5914 (1996).
  Google Scholar
• Noskov, V. N., Araki, H. & Sugino, A. The RFC2 gene, encoding the third-largest subunit of the replication factor C complex, is required for an S-phase checkpoint in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 4914– 4923 (1998).
  CAS PubMed PubMed Central Google Scholar
• Shimomura, T., Ando, S., Matsumoto, K. & Sugimoto, K. Functional and physical interaction between Rad24 and Rfc5 in the yeast checkpoint pathways. Mol. Cell. Biol. 18, 5485– 5491 (1998).
  CAS PubMed PubMed Central Google Scholar
• Shimada, M. et al. Replication factor C3 of Schizosaccharomyces pombe, a small subunit of replication factor C complex, plays a role in both replication and damage checkpoints. Mol. Biol. Cell 10, 3991– 4003 (1999).
  CAS PubMed PubMed Central Google Scholar
• Green, C. M., Erdjument-Bromage, H., Tempst, P. & Lowndes, N. F. A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr. Biol. 10, 39– 42 (2000).
  CAS PubMed Google Scholar
• Edwards, R. J., Bentley, N. J. & Carr, A. M. A Rad3-Rad26 complex responds to DNA damage independently of other checkpoint proteins. Nature Cell Biol. 1, 393– 398 (1999).
  CAS PubMed Google Scholar
• Paciotti, V., Clerici, M., Lucchini, G. & Longhese, M. P. The checkpoint protein Ddc2, functionally related to S. pombe Rad26, interacts with Mec1 and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14, 2046– 2059 (2000).
  CAS PubMed PubMed Central Google Scholar
• Rouse, J. & Jackson, S. P. LCD1: An essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae. EMBO J. 19, 5801– 5812 (2000).
  CAS PubMed PubMed Central Google Scholar
• Xu, X. et al. Centrosome amplification and a defective G2-M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell 3, 389– 395 ( 1999).
  CAS PubMed Google Scholar
• Wang, Y. et al. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14, 927– 939 ( 2000).
  CAS PubMed PubMed Central Google Scholar
• Gong, J. G. et al. The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature 399, 806– 809 (1999).
  ADS CAS PubMed Google Scholar
• Kastan, M. B. et al. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71, 587– 597 (1992).
  CAS PubMed Google Scholar
• Paules, R. S. et al. Defective G2 checkpoint function in cells from individuals with familial cancer syndromes. Cancer Res. 55, 1763– 1773 (1995).
  CAS PubMed Google Scholar
• Cliby, W. A. et al. Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17, 159– 169 ( 1998).
  CAS PubMed PubMed Central Google Scholar
• Wright, J. A. et al. Protein kinase mutants of human ATR increase sensitivity to UV and ionizing radiation and abrogate cell cycle checkpoint control. Proc. Natl Acad. Sci. USA 95, 7445– 7450 (1998).
  ADS CAS PubMed PubMed Central Google Scholar
• Kim, S. T., Lim, D. S., Canman, C. E. & Kastan, M. B. Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274, 37538 – 37543 (1999).
  CAS PubMed Google Scholar
• Canman, C. E. et al. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281, 1677– 1679 (1998).
  ADS CAS PubMed Google Scholar
• Banin, S. et al. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281, 1674– 1677 (1998).
  ADS CAS PubMed Google Scholar
• Tibbetts, R. S. et al. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13, 152– 157 (1999).
  CAS PubMed PubMed Central Google Scholar
• Tibbetts, R. S. et al. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. (in the press).
• Barlow, C. et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159– 171 ( 1996).
  CAS PubMed Google Scholar
• Elson, A. et al. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl Acad. Sci. USA 93, 13084 – 13089 (1996).
  ADS CAS PubMed PubMed Central Google Scholar
• Desany, B. A., Alcasabas, A. A., Bachant, J. B. & Elledge, S. J. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12, 2956– 2970 (1998).
  CAS PubMed PubMed Central Google Scholar
• Khanna, K. K. et al. ATM associates with and phosphorylates p53: mapping the region of interaction. Nature Genet. 20, 398– 400 (1998).
  CAS PubMed Google Scholar
• Chan, D. W. et al. Purification and characterization of ATM from human placenta. A manganese-dependent, wortmannin-sensitive serine/threonine protein kinase. J. Biol. Chem. 275, 7803– 7810 (2000).
  CAS PubMed Google Scholar
• Smith, G. C. et al. Purification and DNA binding properties of the ataxia-telangiectasia gene product ATM. Proc. Natl Acad. Sci. USA 96, 11134– 11139 (1999).
  ADS CAS PubMed PubMed Central Google Scholar
• Lakin, N. D., Hann, B. C. & Jackson, S. P. The ataxia-telangiectasia related protein ATR mediates DNA-dependent phosphorylation of p53. Oncogene 18, 3989– 3995 (1999).
  CAS PubMed Google Scholar
• Hall-Jackson, C. A., Cross, D. A., Morrice, N. & Smythe, C. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18, 6707– 6713 (1999).
  CAS PubMed Google Scholar
• Matsuoka, S., Huang, M. & Elledge, S. J. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282, 1893– 1897 (1998).
  ADS CAS PubMed Google Scholar
• Blasina, A. et al. A human homologue of the checkpoint kinase Cds1 directly inhibits Cdc25 phosphatase. Curr. Biol. 9, 1– 10 (1999).
  CAS PubMed Google Scholar
• Brown, A. L. et al. A human Cds1-related kinase that functions downstream of ATM protein in the cellular response to DNA damage. Proc. Natl Acad. Sci. USA 96, 3745– 3750 ( 1999).
  ADS CAS PubMed PubMed Central Google Scholar
• Chaturvedi, P. et al. Mammalian Chk2 is a downstream effector of the ATM-dependent DNA damage checkpoint pathway. Oncogene 18, 4047– 4054 (1999).
  CAS PubMed Google Scholar
• Zhou, B.-B. S. et al. Caffeine abolishes the mammalian G2/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem. 275, 10342– 10348 (2000).
  CAS PubMed Google Scholar
• Matsuoka, S. et al. ATM phosphorylates Chk2 in vivo and in vitro. Proc. Natl Acad. Sci. USA 97, 10389– 10394 (2000).
  ADS CAS PubMed PubMed Central Google Scholar
• Melchionna, R., Chen, X., Blasina, A. & McGowan, C. H. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nature Cell Biol. 2, 762– 765 (2000).
  CAS PubMed Google Scholar
• 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, 278– 288 ( 2000).
  CAS PubMed PubMed Central Google Scholar
• 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, 289– 300 ( 2000).
  CAS PubMed PubMed Central Google Scholar
• 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, 13777– 13782 (1999).
  ADS CAS PubMed PubMed Central Google Scholar
• Ashcroft, M., Kubbutat, M. H. & Vousden, K. H. Regulation of p53 function and stability by phosphorylation. Mol. Cell. Biol. 19, 1751– 1758 (1999).
  CAS PubMed PubMed Central Google Scholar
• Khosravi, R. et al. Rapid ATM-dependent phosphorylation of MDM2 precedes p53 accumulation in response to DNA damage. Proc. Natl Acad. Sci. USA 96, 14973– 14977 (1999).
  ADS CAS PubMed PubMed Central Google Scholar
• Bell, D. W. et al. Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science 286, 2528– 2531 (1999).
  CAS PubMed Google Scholar
• 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, 201– 204 (2000).
  ADS CAS PubMed Google Scholar
• Sanchez, Y. et al. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science 277, 1497– 1501 (1997).
  CAS PubMed Google Scholar
• Walworth, N. C. & Bernards, R. rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint. Science 271, 353– 356 (1996).
  ADS CAS PubMed Google Scholar
• Nurse, P. Checkpoint pathways come of age. Cell 91, 865– 867 (1997).
  CAS PubMed Google Scholar
• Morgan, D. O. Principles of CDK regulation. Nature 374, 131– 134 (1995).
  ADS CAS PubMed Google Scholar
• Peng, C. Y. et al. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277, 1501– 1505 (1997).
  CAS PubMed Google Scholar
• Dalal, S. N., Schweitzer, C. M., Gan, J. & DeCaprio, J. A. Cytoplasmic localization of human cdc25C during interphase requires an intact 14-3-3 binding site. Mol. Cell. Biol. 19, 4465– 4479 (1999).
  CAS PubMed PubMed Central Google Scholar
• Yang, J., Winkler, K., Yoshida, M. & Kornbluth, S. Maintenance of G2 arrest in the Xenopus oocyte: a role for 14-3-3-mediated inhibition of Cdc25 nuclear import. EMBO J. 18, 2174 – 2183 (1999).
  CAS PubMed PubMed Central Google Scholar
• Bunz, F. et al. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282, 1497– 1501 (1998).
  CAS PubMed Google Scholar
• Chan, T. A., Hermeking, H., Lengauer, C., Kinzler, K. W. & Vogelstein, B. 14-3-3 Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401, 616– 620 (1999).
  ADS CAS PubMed Google Scholar
• Jelinsky, S. A. & Samson, L. D. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Natl Acad. Sci. USA 96, 1486– 1491 (1999).
  ADS CAS PubMed PubMed Central Google Scholar
• Hwang, B. J., Ford, J. M., Hanawalt, P. C. & Chu, G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl Acad. Sci. USA 96, 424– 428 (1999).
  ADS CAS PubMed PubMed Central Google Scholar
• Tanaka, H. et al. A ribonucleotide reductase gene involved in a p53-dependent cell-cycle checkpoint for DNA damage. Nature 404, 42– 49 (2000).
  ADS CAS PubMed Google Scholar
• Carney, J. P. et al. 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 (1998).
  CAS PubMed Google Scholar
• Stewart, G. S. et al. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99, 577– 587 ( 1999).
  CAS PubMed Google Scholar
• Jeggo, P. A., Carr, A. M. & Lehmann, A. R. Splitting the ATM: distinct repair and checkpoint defects in ataxia-telangiectasia. Trends Genet. 14, 312– 316 (1998).
  CAS PubMed Google Scholar
• Moynahan, M. E., Chiu, J. W., Koller, B. H. & Jasin, M. Brca1 controls homology-directed DNA repair. Mol. Cell 4, 511– 518 (1999).
  CAS PubMed Google Scholar
• Bashkirov, V. I., King, J. S., Bashkirova, E. V., Schmuckli-Maurer, J. & Heyer, W. D. DNA repair protein Rad55 is a terminal substrate of the DNA damage checkpoints. Mol. Cell. Biol. 20, 4393– 4404 (2000).
  CAS PubMed PubMed Central Google Scholar
• Brush, G. S., Morrow, D. M., Hieter, P. & Kelly, T. J. The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proc. Natl Acad. Sci. USA 93, 15075– 15080 (1996).
  ADS CAS PubMed PubMed Central Google Scholar
• Lydall, D. & Weinert, T. Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270, 1488– 1491 (1995).
  ADS CAS PubMed Google Scholar
• Bochar, D. A. et al. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 102, 257– 265 (2000).
  CAS PubMed Google Scholar
• Gasser, S. M. A sense of the end. Science 288, 1377– 1379 (2000).
  ADS CAS PubMed Google Scholar