Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway

Molecular and Cellular Biology

Volumn 24, Issue 22, 2004, Pages 10016-10025

  Nakada, Daisuke ^a   Hirano, Yukinori ^a   Sugimoto, Katsunori ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; DOUBLE STRANDED DNA; EXONUCLEASE; EXONUCLEASE 1; MRE11 PROTEIN; PROTEIN; PROTEIN DDC1; PROTEIN MEC1; PROTEIN MEC3; PROTEIN RAD17; RAD50 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVATION; GENETIC STABILITY; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

CELL CYCLE PROTEINS; DNA DAMAGE; DNA REPLICATION; DNA, FUNGAL; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; FUNGAL PROTEINS; GENES, FUNGAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; MUTATION; PHLEOMYCINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

MAMMALIA; SACCHAROMYCETALES;

EID: 7644232348     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.22.10016-10025.2004     Document Type: Article

References (66)

1. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
2. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506.
3. Bermudez, V. P., L. A. Lindsey-Boltz, A. J. Cesare, Y. Maniwa, J. D. Griffith, J. Hurwitz, and A. Sancar. 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.
4. 2/M checkpoint. EMBO J. 22:6610-6620.
5. Chan, S. W., J. Chang, J. Prescott, and E. H. Blackburn. 2001. Altering telomere structure allows telomerase to act in yeast lacking ATM kinases. Curr. Biol. 11:1240-1250.
6. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
7. Costanzo, V., K. Robertson, M. Bibikora, E. Kim, D. Grieco, M. Gottesman, D. Carroll, and J. Gautier. 2001. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8:137-147.
8. D'Amours, D., and S. P. Jackson. 2002. The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3:317-327.
9. D'Amours, D., and S. P. Jackson. 2001. The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15:2238-2249.
10. de-Laat, W. L., N. G. Jaspers, and J. H. Hoeijmakers. 1999. Molecular mechanism of nucleotide excision repair. Genes Dev. 13:768-785.
11. Elledge, S. J. 1996. Cell cycle checkpoints: preventing an identity crisis. Science 274:1664-1672.
12. Ellison, V., and B. Stillman. 2003. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5′ recessed DNA. PLoS Biol. 1:E33.
13. Fiorentini, P., K. N. Huang, D. X. Tishkoff, R. D. Kolodner, and L. S. Symington. 1997. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol. Cell. Biol. 17:2764-2773.
14. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis. ASM Press, Washington, D.C.
15. Giannattasio, M., F. Lazzaro, M. P. Longhese, P. Plevani, and M. Muzi-Falconi. 2004. Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. EMBO J. 23:429-438.
16. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527-534.
17. Green, C. M., H. Erdjument-Bromage, P. Tempst, and N. F. Lowndes. 2000. A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr. Biol. 10:39-42.
18. Greenwell, P. W., S. L. Kronmal, S. E. Porter, J. Gassenhuber, B. Obermaier, and T. D. Petes. 1995. TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82:823-829.
19. Grenon, M., C. Gilbert, and N. F. Lowndes. 2001. Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat. Cell Biol. 3:844-347.
20. Haber, J. E. 1998. The many interfaces of Mre11. Cell 95:583-586.
21. Ivanov, E. L., N. Sugawara, C. I. White, F. Fabre, and J. E. Haber. 1994. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:3414-3425.
22. Kastan, M. B., and D. S. Lim. 2000. The many substrates and functions of ATM. Nat. Rev. Mol. Cell Biol. 1:179-186.
23. Katou, Y., Y. Kanoh, M. Bando, H. Noguchi, H. Tanaka, T. Ashikari, K. Sugimoto, and K. Shirahige. 2003. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424:1073-1083.
24. Kitagawa, R., C. J. Bakkenist, P. J. McKinnon, and M. B. Kastan. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18:1423-1438.
25. Kondo, T., T. Wakayama, T. Naiki, K. Matsumoto, and K. Sugimoto. 2001. Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 5543:867-870.
26. Lee, J. H., and T. T. Paull. 2004. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304:93-96.
27. Lee, S. E., D. A. Bressan, J. H. Petrini, and J. E. Haber. 2002. Complementation between N-terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance. DNA Repair (Amsterdam) 1:27-40.
28. 2/M arrest after DNA damage. Cell 94:399-409.
29. Longhese, M. P., M. Foiani, M. Muzi-Falconi, G. Lucchini, and P. Plevani. 1998. DNA damage checkpoint in budding yeast. EMBO J. 17:5525-5528.
30. Lucca, C., F. Vanoli, C. Cotta-Ramusino, A. Pellicioli, G. Liberi, J. Haber, and M. Foiani. 2004. Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23:1206-1213.
31. Majka, J., and P. M. Burgers. 2003. Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 100: 2249-2254.
32. Melo, J. A., J. Cohen, and D. P. Toczyski. 2001. Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 21:2809-2821.
33. Moreau, S., J. R. Ferguson, and L. S. Symington. 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19:556-566.
34. Moreau, S., E. A. Morgan, and L. S. Symington. 2001. Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159:1423-1433.
35. Morrow, D. M., D. A. Tagle, Y. Shiloh, F. S. Collins, and P. Hieter. 1995. TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene, MEC1. Cell 82:831-840.
36. Naiki, T., T. Shimomura, T. Kondo, K. Matsumoto, and K. Sugimoto. 2000. Rfc5, in cooperation with Rad24, controls DNA damage checkpoints throughout the cell cycle in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:5888-5896.
37. Naiki, T., T. Wakayama, D. Nakada, K. Matsumoto, and K. Sugimoto. 2004. Association of Rad9 with double-strand breaks through a Mec1-dependent mechanism. Mol. Cell. Biol. 24:3277-3285.
38. Nakada, D., K. Matsumoto, and K. Sugimoto. 2003. ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev. 17:1957-1962.
39. Nakada, D., T. Shimomura, K. Matsumoto, and K. Sugimoto. 2003. The ATM-related Tel1 protein of Saccharomyces cerevisiae controls a checkpoint response following phleomycin treatment. Nucleic Acids Res. 31:1715-1724.
40. Osborn, A. J., and S. J. Elledge. 2003. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17:1755-1767.
41. Paciotti, V., M. Clerici, G. Lucchini, and M. P. Longhese. 2000. 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.
42. 2/M arrest. Mol. Cell 7:293-300.
43. Petrini, J. H. 2000. The Mre11 complex and ATM: collaborating to navigate S phase. Curr. Opin. Cell Biol. 12:293-296.
44. Qiu, J., M. X. Guan, A. M. Bailis, and B. Shen. 1998. Saccharomyces cerevisiae exonuclease-1 plays a role in UV resistance that is distinct from nucleotide excision repair. Nucleic Acids Res. 26:3077-3783.
45. Ritchie, K. B., J. C. Mollory, and T. D. Petes. 1999. 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.
46. Ritchie, K. B., and T. D. Petes. 2000. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics 155:475-479.
47. Rouse, J., and S. P. Jackson. 2000. LCD1: an essential gene involved in checkpoint control and regulation of the MECI signalling pathway in Saccharomyces cerevisiae. EMBO J. 19:5793-5800.
48. Rouse, J., and S. P. Jackson. 2002. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol. Cell 9:857-869.
49. Sanchez, Y., J. Bachant, H. Wang, F. Hu, D. Liu, M. Tetzlaff, and S. J. Elledge. 1999. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286:1166-1171.
50. Sanchez, Y., B. A. Desany, W. J. Jones, Q. Liu, B. Wang, and S. J. Elledge. 1996. Regulation of RAD53 by the ATM-like kinase MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271:357-360.
51. Takata, H., Y. Kanon, N. Gunge, K. Shirahige, and A. Matsuura. 2004. Reciprocal association of the budding yeast ATM-related proteins Tel1 and Mec1 with telomeres in vivo. Mol. Cell 14:515-522.
52. Tishkoff, D. X., N. S. Amin, C. S. Viars, K. C. Arden, and R. D. Kolodner. 1998. Identification of a human gene encoding a homologue of Saccharomyces cerevisiae EXO1, an exonuclease. Cancer Res. 58:5027-5031.
53. Toczyski, D. P., D. J. Galgoczy, and L. H. Hartwell. 1997. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90:1097-1106.
54. Tsubouchi, H., and H. Ogawa. 2000. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell 11:2221-2233.
55. Umezu, K., N. Sugawara, C. Chen, J. E. Haber, and R. D. Kolodner. 1998. Genetic analysis of yeast RPA1 reveals its multiple functions in DNA metabolism. Genetics 148:989-1005.
56. Usui, T., H. Ogawa, and J. H. Petrini. 2001. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell 7:1255-1266.
57. Uziel, T., Y. Lerenthal, L. Moyal, Y. Andegeko, L. Mittelman, and Y. Shiloh. 2003. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22:5612-5621.
58. Vialard, J. E., C. S. Gilbert, C. M. Green, and N. F. Lowndes. 1998. The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J. 17:5679-5688.
59. Wakayama, T., T. Kondo, S. Ando, K. Matsumoto, and K. Sugimoto. 2001. Pie1, a protein interacting with Mec1, controls cell growth and checkpoint responses in Saccharomyces cerevisiae. Mol. Cell. Biol. 21:755-764.
60. White, C. I., and J. E. Haber. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9:663-673.
61. Wold, M. S. 1997. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66:61-92.
62. Zhang, H., J. Taylor, and W. Siede. 2003. Checkpoint arrest signaling in response to UV damage is independent of nucleotide excision repair in Saccharomyces cerevisiae. J. Biol. Chem. 278:9382-9387.
63. Zhao, X., E. G. D. Muller, and R. Rothstein. 1998. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pool. Mol. Cell 2:329-340.
64. Zhou, B.-B. S., and S. J. Elledge. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-439.
65. Zou, L., and S. J. Elledge. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548.
66. Zou, L., D. Liu, and S. J. Elledge. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. USA 100:13827-13832.