Phosphorylation of Slx4 by Mec1 and Tel1 regulates the single-strand annealing mode of DNA repair in budding yeast

Molecular and Cellular Biology

Volumn 27, Issue 18, 2007, Pages 6433-6445

  Flott, Sonja ^a,d   Alabert, Constance ^b   Toh, Geraldine W ^a   Toth, Rachel ^a   Sugawara, Neal ^c   Campbell, David G ^a   Haber, James E ^c   Pasero, Philippe ^b   Rouse, John ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b INSTITUTE OF HUMAN GENETICS   (France)

^c BRANDEIS UNIVERSITY   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESYLIC ACID METHYL ESTER; PROTEIN MEC1; PROTEIN RAD1; PROTEIN SLX4; PROTEIN TEL1; RECQ HELICASE; REPLISOME; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE G1 PHASE; CELL VIABILITY; CHROMOSOME REPLICATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; EXCISION REPAIR; GENE AMPLIFICATION; GENETIC EPISTASIS; GENOME; GENOTYPE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

DNA REPAIR; DNA, FUNGAL; ENDODEOXYRIBONUCLEASES; FUNGAL PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; METHYL METHANESULFONATE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 34548747505     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00135-07     Document Type: Article

References (57)

1. Bardwell, L., A. J. Cooper, and E. C. Friedberg. 1992. Stable and specific association between the yeast recombination and DNA repair proteins RAD1 and RAD10 in vitro. Mol. Cell Biol. 12:3041-3049.
2. Bastin-Shanower, S. A., W. M. Fricke, J. R. Mullen, and S. J. Brill. 2003. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23:3487-3496.
3. Beranek, D. T. 1990. Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat. Res. 231:11-30.
4. Brusky, J., Y. Zhu, and W. Xiao. 2000. UBC13, a DNA-damage-inducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr. Genet. 37:168-174.
5. Chang, M., M. Bellaoui, C. Boone, and G. W. Brown. 2002. A genome-wide screen for methyl methancsulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. USA 99:16934-16939.
6. Chin, J. K., V. I. Bashkirov, W. D. Heyer, and F. E. Romesberg. 2006. Esc4/Rtt107 and the control of recombination during replication. DNA Repair (Amsterdam) 5:618-628.
7. Coulon, S., P. H. Gaillard, C. Chahwan, W. H. McDonald, J. R. Yates III, and P. Russell. 2004. Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell 15:71-80.
8. Desany, B. A., A. A. Alcasabas, J. B. Bachant, and S. J. Elledge. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12:2956-2970.
9. Duncker, B. P., K. Shimada, M. Tsai-Pflugfelder, P. Pasero, and S. M. Gasser. 2002. An N-terminal domain of Dbf4p mediates interaction with both origin recognition complex (ORC) and Rad53p and can deregulate late origin firing. Proc. Natl. Acad. Sci. USA 99:16087-16092.
10. Fabre, F., A. Chan, W. D. Heyer, and S. Gangloff. 2002. Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. USA 99:16887-16892.
11. Fishman-Lobell, J., and J. E. Haber. 1992. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258:480-484.
12. Flott, S., and J. Rouse. 2005. Slx4 becomes phosphorylated after DNA damage in a Mec1/Tel1-dependent manner and is required for repair of DNA alkylation damage. Biochem. J. 391:325-333.
13. Freudenreich, C. H., S. M. Kantrow, and V. A. Zakian. 1998. Expansion and length-dependent fragility of CTG repeats in yeast. Science 279:853-856.
14. Fricke, W. M., and S. J. Brill. 2003. Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3. Genes Dev. 17:1768-1778.
15. Gangloff, S., J. P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391-8398.
16. Goldfarb, T., and E. Alani. 2005. Distinct roles for the Saccharomyces cerevisiae mismatch repair proteins in heteroduplex rejection, mismatch repair and nonhomologous tail removal. Genetics 169:563-574.
17. Hanway, D., J. K. Chin, G. Xia, G. Oshiro, E. A. Winzeler, and F. E. Romesberg. 2002. Previously uncharacterized genes in the UV- and MMS-induced DNA damage response in yeast. Proc. Natl. Acad. Sci. USA 99:10605-10610.
18. Hennessy, K. M., A. Lee, E. Chen, and D. Botstein. 1991. A group of interacting yeast DNA replication genes. Genes Dev. 5:958-969.
19. Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169-178.
20. Higgins, N. P., K. Kato, and B. Strauss. 1976. A model for replication repair in mammalian cells. J. Mol. Biol. 101:417-425.
21. Hoege, C., B. Pfander, G. L. Moldovan, G. Pyrowolakis, and S. Jentsch. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
22. Ito, T., T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, and Y. Sakaki. 2001. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98:4569-4574.
23. Kaliraman, V., J. R. Mullen, W. M. Fricke, S. A. Bastin-Shanower, and S. J. Brill. 2001. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15:2730-2740.
24. Kaye, J. A., J. A. Melo, S. K. Cheung, M. B. Vaze, J. E. Haber, and D. P. Toczyski. 2004. DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr. Biol. 14:2096-2106.
25. Khakhar, R. R., J. A. Cobb, L. Bjergbaek, I. D. Hickson, and S. M. Gasser. 2003. RecQ helicases: multiple roles in genome maintenance. Trends Cell Biol. 13:493-501.
26. Lawrence, C. W., and V. M. Maher. 2001. Mutagenesis in eukaiyotes dependent on DNA polymerase zeta and Rev1p. Philos. Trans. R. Soc. London B 356:41-46.
27. Liberi, G., G. Maffioletti, C. Lucca, I. Chiolo, A. Baryshnikova, C. Cotta-Ramusino, M. Lopes, A. Pellicioli, J. E. Haber, and M. Foiani. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19:339-350.
28. Luke, B., G. Versini, M. Jaquenoud, I. W. Zaidi, T. Kurz, L. Pintard, P. Pasero, and M. Peter. 2006. The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr. Biol. 16:786-792.
29. Michalet, X., R. Ekong, F. Fougerousse, S. Rousseaux, C. Schurra, N. Hornigold, M. van Slegtenhorst, J. Wolfe, S. Povey, J. S. Beckmann, and A. Bensimon. 1997. Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science 277:1518-1523.
30. Mullen, J. R., V. Kaliraman, and S. J. Brill. 2000. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154:1101-1114.
31. Mullen, J. R., V. Kaliraman, S. S. Ibrahim, and S. J. Brill. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103-118.
32. Myung, K., A. Datta, C. Chen, and R. D. Kolodner. 2001. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27:113-116.
33. Papouli, E., S. Chen, A. A. Davies, D. Huttner, L. Krejei, P. Sung, and H. D. Ulrich. 2005. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19:123-133.
34. Pasero, P., A. Bensimon, and E. Schwob. 2002. Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev. 16:2479-2484.
35. Prakash, L. 1981. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184:471-478.
36. Prakash, S., R. E. Johnson, and L. Prakash. 2005. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74:317-353.
37. Roberts, T. M., M. S. Kobor, S. A. Bastin-Shanower, M. Ii, S. A. Horte, J. W. Gin, A. Emili, J. Rine, S. J. Brill, and G. W. Brown. 2006. Slx4 regulates DNA damage checkpoint-dependent phosphorylation of the BRCT domain protein Rtt107/Esc4. Mol. Biol. Cell 17:539-548.
38. Rouse, J. 2004. Esc4p, a new target of Mec1p (ATR), promotes resumption of DNA synthesis after DNA damage. EMBO J 23:1188-1197.
39. Rouse, J., and S. P. Jackson. 2000. LCD1: an essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae. EMBO J. 19:5801-5812.
40. Rupp, W. D., C. E. Wilde III, D. L. Reno, and P. Howard-Flanders. 1971. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. J. Mol. Biol. 61:25-44.
41. Scholes, D. T., M. Banerjee, B. Bowen, and M. J. Curcio. 2001. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159:1449-1465.
42. Schurer, K. A., C. Rudolph, H. D. Ulrich, and W. Kramer. 2004. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from Homologous recombination, but not from postreplicative repair. Genetics 166:1673-1686.
43. Spell, R. M., and S. Jinks-Robertson. 2004. Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics 168:1855-1865.
44. Stelter, P., and H. D. Ulrich. 2003. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425:188-191.
45. Sugawara, N., T. Goldfarb, B. Studamire, E. Alani, and J. E. Haber. 2004. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc. Natl. Acad. Sci. USA 101:9315-9320.
46. Thomas, B. J., and R. Rothstein. 1989. The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination at GAL10, a transcriptionally regulated gene. Genetics 123:725-738.
47. Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364-2368.
48. Tourriere, H., G. Versini, V. Cordon-Preciado, C. Alabert, and P. Pasero. 2005. Mre1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol. Cell. 19:699-706.
49. Traven, A., and J. Heierhorst. 2005. SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays 27:397-407.
50. Ui, A., M. Seki, H. Ogiwara, R. Onodera, S. Fukushige, F. Onoda, and T. Enomoto. 2005. The ability of Sgs1 to interact with DNA topoisomerase III is essential for damage-induced recombination. DNA Repair (Amsterdam) 4:191-201.
51. Ulrich, H. D. 2005. The RAD6 pathway: control of DNA damage bypass and mutagenesis by ubiquitin and SUMO. ChemBiochem 6:1735-1743.
52. Watt, P. M., I. D. Hickson, R. H. Borts, and E. J. Louis. 1996. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144:935-945.
53. Wu, L., and I. D. Hickson. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870-874.
54. Yamagata, K., J. Kato, A. Shimamoto, M. Goto, Y. Furuichi, and H. Ikeda. 1998. Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: implication for genomic instability in human diseases. Proc. Natl. Acad. Sci. USA 95:8733-8738.
55. Zappulla, D. C., A. S. Maharaj, J. J. Connelly, R. A. Jockusch, and R. Sternglanz. 2006. Rtt107/Esc4 binds silent chromatin and DNA repair proteins using different BRCT motifs. BMC Mol. Biol. 7:40.
56. Zhang, C., T. M. Roberts, J. Yang, R. Desai, and G. W. Brown. 2006. Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair (Amsterdam) 5:336-346.
57. Zhang, H., and C. W. Lawrence. 2005. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. USA 102:15954-15959.