Regulation of gross chromosomal rearrangements by ubiquitin and SUMO ligases in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 26, Issue 4, 2006, Pages 1424-1433

  Motegi, Akira ^a   Kuntz, Karen ^a,b   Majeed, Anju ^a   Smith, Stephanie ^a   Myung, Kyungjae ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; HELICASE; LIGASE; PROTEIN BRE1; PROTEIN RAD18; PROTEIN RAD5; PROTEIN SRS2; SUMO LIGASE SIZ1; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME REARRANGEMENT; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; ENZYME INACTIVATION; FUNGAL STRAIN; GENE; GENE MUTATION; GROSS CHROMOSOMAL REARRANGEMENT; HOMOLOGOUS RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAD18 GENE; RAD5 GENE; SACCHAROMYCES CEREVISIAE; TELOMERE;

ADENOSINE TRIPHOSPHATASES; CHROMOSOMES, FUNGAL; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE REARRANGEMENT; GENES, FUNGAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; UBIQUITIN-PROTEIN LIGASES;

SACCHAROMYCES CEREVISIAE;

EID: 32044451333     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.4.1424-1433.2006     Document Type: Article

References (73)

1. Amin, N. S., and C. Holm. 1996. In vivo analysis reveals that the interdomain region of the yeast proliferating cell nuclear antigen is important for DNA replication and DNA repair. Genetics 144:479-493.
2. Bailly, V., J. Lamb, P. Sung, S. Prakash, and L. Prakash. 1994. Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev. 8:811-820.
3. Banerjee, S., and K. Myung. 2004. Increased genome instability and telomere length in the elg1-deficient Saccharomyces cerevisiae mutant are regulated by S-phase checkpoints. Eukaryot. Cell 3:1557-1566.
4. Broomfield, S., T. Hryciw, and W. Xiao. 2001. DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 486:167-184.
5. Broomfield, S., and W. Xiao. 2002. Suppression of genetic defects within the RAD6 pathway by srs2 is specific for error-free post-replication repair but not for damage-induced mutagenesis. Nucleic Acids Res. 30:732-739.
6. Chan, S. W., and E. H. Blackburn. 2003. Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining. Mol. Cell 11:1379-1387.
7. Chen, C., and R. D. Kolodner. 1999. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23:81-85.
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. Dohmen, R. J., K. Madura, B. Bartel, and A. Varshavsky. 1991. The N-end rule is mediated by the UBC2(RAD6) ubiquitin-conjugating enzyme. Proc. Natl. Acad. Sci. USA 88:7351-7355.
10. Fischhaber, P. L., and E. C. Friedberg. 2005. How are specialized (low-fidelity) eukaryotic polymerases selected and switched with high-fidelity polymerases during translesion DNA synthesis? DNA Repair (Amsterdam) 4:279-283.
11. Foiani, M., A. Pellicioli, M. Lopes, C. Lucca, M. Ferrari, G. Liberi, M. Muzi Falconi, and P. Plevani. 2000. DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae. Mutat. Res. 451:187-196.
12. Frank, S. A. 2004. Genetic predisposition to cancer-insights from population genetics. Nat. Rev. Genet. 5:764-772.
13. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis American Society for Microbiology, Washington, D.C.
14. Friedl, A. A., B. Liefshitz, R. Steinlauf, and M. Kupiec. 2001. Deletion of the SRS2 gene suppresses elevated recombination and DNA damage sensitivity in rad5 and rad18 mutants of Saccharomyces cerevisiae. Mutat. Res. 486:137-146.
15. Gill, G. 2004. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18:2046-2059.
16. Gollin, S. M. 2004. Chromosomal instability. Curr. Opin. Oncol. 16:25-31.
17. Haracska, L., C. A. Torres-Ramos, R. E. Johnson, S. Prakash, and L. Prakash. 2004. Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:4267-4274.
18. 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.
19. Hofmann, R. M., and C. M. Pickart. 1999. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96:645-653.
20. Huang, D., and D. Koshland. 2003. Chromosome integrity in Saccharomyces cerevisiae: the interplay of DNA replication initiation factors, elongation factors, and origins. Genes Dev. 17:1741-1754.
21. Huang, M. E., and R. D. Kolodner. 2005. A biological network in Saccharomyces cerevisiae prevents the deleterious effects of endogenous oxidative DNA damage. Mol. Cell. 17:709-720.
22. Hwang, J. Y., S. Smith, and K. Myung, 2005. The Rad1-Rad10 complex promtes the production of gross chromosomal rearrangements from spontaneous DNA damage in Saccharomyces cerevisiae. Genetics 169:1927-1937.
23. Johnson, R. E., C. M. Kondratick, S. Prakash, and L. Prakash. 1999. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263-265.
24. Kanellis, P., R. Agyei, and D. Durocher. 2003. Elg1 forms an alternative PCNA-interacting RFC complex required to maintain genome stability. Curr. Biol. 13:1583-1595.
25. Khanna, K. K., and S. P. Jackson. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:247-254.
26. Kolodner, R. D., C. D. Putnam, and K. Myung. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552-557.
27. Krejci, L., S. Van Komen, Y. Li, J. Villemain, M. S. Reddy, H. Klein, T. Ellenberger, and P. Sung. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305-309.
28. Lambert, S., A. Watson, D. M. Sheedy, B. Martin, and A. M. Carr. 2005. Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 121:689-702.
29. Lawrence, C. 1994. The RAD6 DNA repair pathway in Saccharomyces cerevisiae: what does it do, and how does it do it? Bioessays 16:253-258.
30. Lea, D. E., and C. A. Coulson. 1948. The distribution of the numbers of mutants in bacterial populations. J. Genet. 49:264-285.
31. Lengauer, C. 2005. Aneuploidy and genetic instability in cancer. Semin. Cancer Biol. 15:1.
32. Lengronne, A., and E. Schwob. 2002. The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol. Cell 9:1067-1078.
33. Liberi, G., I. Chiolo, A. Pellicioli, M. Lopes, P. Plevani, M. Muzi-Falconi, and M. Foiani. 2000. Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J. 19:5027-5038.
34. Loeb, L. A., K. R. Loeb, and J. P. Anderson. 2003. Multiple mutations and cancer. Proc. Natl. Acad. Sci. USA 100:776-781.
35. Martini, E. M., S. Keeney, and M. A. Osley. 2002. A role for histone H2B during repair of UV-induced DNA damage in Saccharomyces cerevisiae. Genetics 160:1375-1387.
36. Masutani, C., R. Kusumoto, A. Yamada, N. Dohmae, M. Yokoi, M. Yuasa, M. Araki, S. Iwai, K. Takio, and F. Hanaoka. 1999. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 399:700-704.
37. Michor, F., Y. Iwasa, B. Vogelstein, C. Lengauer, and M. A. Nowak. 2005. Can chromosomal instability initiate tumorigenesis? Semin. Cancer Biol. 15:43-49.
38. Myung, K., C. Chen, and R. D. Kolodner. 2001. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411:1073-1076.
39. 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.
40. Myung, K., A. Datta, and R. D. Kolodner. 2001. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 104:397-408.
41. Myung, K., and R. D. Kolodner. 2002. Suppression of genome instability by redundant S-phase checkpoint pathways in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99:4500-4507.
42. Myung, K., V. Pennaneach, E. S. Kats, and R. D. Kolodner. 2003. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl. Acad. Sci. USA 100:6640-6645.
43. Myung, K., S. Smith, and R. D. Kolodner. 2004. Mitotic checkpoint function in the formation of gross chromosomal rearrangements in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101:15980-15985.
44. Nagy, R., K. Sweet, and C. Eng. 2004. Highly penetrant hereditary cancer syndromes. Oncogene 23:6445-6470.
45. Osley, M. A. 2004. H2B ubiquitylation: the end is in sight. Biochim. Biophys. Acta 1677:74-78.
46. Papouli, E., S. Chen, A. A. Davies, D. Huttner, L. Krejci, 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.
47. Pennaneach, V., and R. D. Kolodner. 2004. Recombination and the Tel1 and Mec1 checkpoints differentially effect genome rearrangements driven by telomere dysfunction in yeast. Nat. Genet. 36:612-617.
48. Petrini, J. H. 2000. The Mre11 complex and ATM: collaborating to navigate S phase. Curr. Opin. Cell Biol. 12:293-296.
49. Pfander, B., G. L. Moldovan, M. Sacher, C. Hoege, and S. Jentsch. 2005. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436:428-433.
50. Plosky, B. S., and R. Woodgate. 2004. Switching from high-fidelity replicases to low-fidelity lesion-bypass polymerases. Curr. Opin. Genet. Dev. 14:113-119.
51. Prakash, S., and L. Prakash. 2000. Nucleotide excision repair in yeast. Mutat. Res. 451:13-24.
52. Putnam, C. D., V. Pennaneach, and R. D. Kolodner. 2004. Chromosome healing through terminal deletions generated by de novo telomere additions in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101:13262-13267.
53. Ronen, A., and B. W. Glickman. 2001. Human DNA repair genes. Environ. Mol. Mutagen. 37:241-283.
54. Sancar, A., L. A. Lindsey-Boltz, K. Unsal-Kacmaz, and S. Linn. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39-85.
55. Schar, P. 2001. Spontaneous DNA damage, genome instability, and cancer-when DNA replication escapes control. Cell 104:329-332.
56. Schiestl, R. H., S. Prakash, and L. Prakash. 1990. The SRS2 suppressor of rado mutations of Saccharomyces cerevisiae acts by channeling DNA lesions into the RAD52 DNA repair pathway. Genetics 124:817-831.
57. Schwartz, D. C., and M. Hochstrasser. 2003. A superfamily of protein tags: ubiquitin, SUMO and related modifiers. Trends Biochem. Sci. 28:321-328.
58. Smirnova, M., and H. L. Klein. 2003. Role of the error-free damage bypass postreplication repair pathway in the maintenance of genomic stability. Mutat. Res. 532:117-135.
59. Smith, S., A. Gupta, R. D. Kolodner, and K. Myung. 2005. Suppression of gross chromosomal rearrangements by the multiple functions of the Mre11-Rad50-Xrs2 complex in Saccharomyces cerevisiae. DNA Repair (Amsterdam) 4:606-617.
60. Smith, S., J. Y. Hwang, S. Banerjee, A. Majeed, A. Gupta, and K. Myung. 2004. Mutator genes for suppression of gross chromosomal rearrangements identified by a genome-wide screening in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 101:9039-9044.
61. Soustelle, C., L. Vernis, K. Freon, A. Reynaud-Angelin, R. Chanet, F. Fahre, and M. Heude. 2004. A new Saccharomyces cerevisiae strain with a mutant Smt3-deconjugating Ulp1 protein is affected in DNA replication and requires Srs2 and homologous recombination for its viability. Mol. Cell. Biol. 24:5130-5143.
62. Stelter, P., and H. D. Ulrich. 2003. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425:188-191.
63. Sung, P., S. Prakash, and L. Prakash. 1990. Mutation of cysteine-88 in the Saccharomyces cerevisiae RAD6 protein abolishes its ubiquitin-conjugating activity and its various biological functions. Proc. Natl. Acad. Sci. USA 87:2695-2699.
64. Symington, L. S. 2002. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66:630-670.
65. Tanaka, S., and J. F. Diffley. 2002. Deregulated G1-cyclin expression induces genomic instability by preventing efficient pre-RC formation. Genes Dev. 16:2639-2649.
66. Tateishi, S., H. Niwa, J. Miyazaki, S. Fujimoto, H. Inoue, and M. Yamaizumi. 2003. Enhanced genomic instability and defective postreplication repair in RAD18 knockout mouse embryonic stem cells. Mol. Cell. Biol. 23:474-481.
67. Teixeira, M. R., and S. Heim. 2005. Multiple numerical chromosome aberrations in cancer: what are their causes and what are their consequences? Semin. Cancer Biol. 15:3-12.
68. Ulrich, H. D. 2001. The srs2 suppressor of UV sensitivity acts specifically on the RAD5- and MM52-dependent branch of the RAD6 pathway. Nucleic Acids Res. 29:3487-3494.
69. Vaze, M. B., A. Pellicioli, S. E. Lee, G. Ira, G. Liberi, A. Arbel-Eden, M. Foiani, and J. E. Haber. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell 10:373-385.
70. Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting RadSl nucleoprotein filaments. Nature 423:309-312.
71. Wohlschlegel, J. A., E. S. Johnson, S. I. Reed, and J. R. Yates, III. 2004. Global analysis of protein sumoylation in Saccharomyces cerevisiae. J. Biol. Chem. 279:45662-45668.
72. Wood, A., N. J. Krogan, J. Dover, J. Schneider, J. Heidt, M. A. Boateng, K. Dean, A. Golshani, Y. Zhang, J. F. Greenblatt, M. Johnston, and A. Shilatifard. 2003. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol. Cell 11:267-274.
73. Zhao, X., and G. Blobel. 2005. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. USA 102:4777-4782.