Smc5p promotes faithful chromosome transmission and DNA repair in Saccharomyces cerevisiae

Genetics

Volumn 172, Issue 4, 2006, Pages 2185-2200

  Cost, Gregory J ^a   Cozzarelli, Nicholas R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; CHROMOSOME PROTEIN; FUNGAL PROTEIN; MMS21 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; FUNGAL STRAIN; FUNGUS MUTANT; GENE OVEREXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SURVIVAL; TEMPERATURE; TEMPERATURE SENSITIVITY; WILD TYPE; YEAST CELL;

CELL CYCLE PROTEINS; DIMERIZATION; DNA REPAIR; GENE EXPRESSION REGULATION, FUNGAL; MODELS, GENETIC; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUMO-1 PROTEIN;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 33646194957     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.105.053876     Document Type: Article

References (55)

1. ANDREWS, E. A., J. PALECEK, J. SERGEANT, E. TAYLOR, A. R. LEHMANN et al., 2005 Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell. Biol. 25: 185-196.
2. AUSUBEL, F. M., R. BRENT, R. E. KINGSTON, D. D. MOORE, J. G. SEIDMAN et al., 2005 Current Protocols in Molecular Biology. Wiley, New York.
3. BODDY, M. N., P. SHANAHAN, W. H. MCDONALD, A. LOPEZ-GIRONA, E. NOGUCHI et al., 2003 Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60. Mol. Cell. Biol. 23: 5939-5946.
4. BRACHMANN, C. B., A. DAVIES, G. J. COST, E. CAPUTO, J. LI et al., 1998 Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14: 115-132.
5. CHA, R. S., and N. KLECKNER, 2002 ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602-606.
6. CHEN, X. L., A. REINDLE and E. S. JOHNSON, 2005 Misregulation of 2 micron circle copy number in a SUMO pathway mutant. Mol. Cell. Biol. 25: 4311-4320.
7. COST, G. J., and J. D. BOEKE, 1996 A useful colony colour phenotype associated with the yeast selectable/counter-selectable marker MET15. Yeast 12: 939-941.
8. DE WULF, P., A. D. MCAINSH and P. K. SORGER, 2003 Hierarchical assembly of the budding yeast kinetochore from multiple subcomplexes. Genes Dev. 17: 2902-2921.
9. DOBSON, M. J., A. J. PICKETT, S. VELMURUGAN, J. B. PINDER, L. A. BARRETT et al., 2005 The 2 micron plasmid causes cell death in Saccharomyces cerevisiae with a mutation in Ulp1 protease. Mol. Cell. Biol. 25: 4299-4310.
10. FOUSTERI, M. I., and A. R. LEHMANN, 2000 A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J. 19: 1691-1702.
11. FUJIOKA, Y., Y. KIMATA, K. NOMAGUCHI, K. WATANABE and K. KOHNO, 2002 Identification of a novel non-structural maintenance of chromosomes (SMC) component of the SMC5-SMC6 complex involved in DNA repair. J. Biol. Chem. 277: 21585-21591.
12. GIAEVER, G., A. M. CHU, L. NI, C. CONNELLY, L. RILES et al., 2002 Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
13. GRUBER, S., C. H. HAERING and K. NASMYTH, 2003 Chromosomal cohesin forms a ring. Cell 112: 765-777.
14. HARVEY, S. H., D. M. SHEEDY, A. R. CUDDIHY and M. J. O'CONNELL, 2004 Coordination of DNA damage responses via the Smc5/Smc6 complex. Mol. Cell. Biol. 24: 662-674.
15. HAZBUN, T. R., L. MALMSTROM, S. ANDERSON, B. J. GRACZYK, B. FOX et al., 2003 Assigning function to yeast proteins by integration of technologies. Mol. Cell 12: 1353-1365.
16. HIRANO, T., 1998 SMC protein complexes and higher-order chromosome dynamics. Curr. Opin. Cell Biol. 10: 317-322.
17. HU, B., C. LIAO, S. H. MILLSON, M. MOLLAPOUR, C. PRODROMOU et al., 2005 Qri2/Nse4, a component of the essential Smc5/6 DNA repair complex. Mol. Microbiol. 55: 1735-1750.
18. IVESSA, A. S., J. Q. ZHOU and V. A. ZAKIAN, 2000 The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100: 479-489.
19. JESSBERGER, R., 2002 The many functions of SMC proteins in chromosome dynamics. Nat. Rev. Mol. Cell. Biol. 3: 767-778.
20. LEA, D. E., and C. A. COULSON, 1949 The distribution of numbers of mutants in bacterial populations. J. Genet. 49: 264-285.
21. LEE, W. L., J. R. OBERLE and J. A. COOPER, 2003 The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast. J. Cell Biol. 160: 355-364.
22. LEHMANN, A. R., M. WALICKA, D. J. GRIFFITHS, J. M. MURRAY, F. Z. WATTS et al., 1995 The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol. Cell. Biol. 15: 7067-7080.
23. LOPES, M., C. COTTA-RAMUSINO, A. PELLICIOLI, G. LIBERI, P. PLEVANI et al., 2001 The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
24. MCDONALD, W. H., Y. PAVLOVA, J. R. YATES, 3RD and M. N. BODDY, 2003 Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J. Biol. Chem. 278: 45460-45467.
25. MCMURRAY, M. A., and D. E. GOTTSCHLING, 2003 An age-induced switch to a hyper-recombinational state. Science 301: 1908-1911.
26. MELO, J., and D. TOCZYSKI, 2002 A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14: 237-245.
27. MORIKAWA, H., T. MORISHITA, S. KAWANE, H. IWASAKI, A. M. CARR et al., 2004 Rad62 protein functionally and physically associates with the smc5/smc6 protein complex and is required for chromosome integrity and recombination repair in fission yeast. Mol. Cell. Biol. 24: 9401-9413.
28. MORISHITA, T., Y. TSUTSUI, H. IWASAKI and H. SHINAGAWA, 2002 The Schizosaccharomyces pombe rad60 gene is essential for repairing double-strand DNA breaks spontaneously occurring during replication and induced by DNA-damaging agents. Mol. Cell. Biol. 22: 3537-3548.
29. NASH, R., G. TOKIWA, S. ANAND, K. ERICKSON and A. B. FUTCHER, 1988 The WHI1+ gene of Saccharomyces cerevisiae tethers cell division to cell size and is a cyclin homolog. EMBO J. 7: 4335-4346.
30. NASIM, A., and B. P. SMITH, 1975 Genetic control of radiation sensitivity in Schizosaccharomyces pombe. Genetics 79: 573-582.
31. ONO, B., N. ISHII, S. FUJINO and I. AOYAMA, 1991 Role of hydrosul-fide ions in methylmercury resistance in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 57: 3183-3186.
32. ONO, T., A. LOSADA, M. HIRANO, M. P. MYERS, A. F. NEUWALD et al., 2003 Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115: 109-121.
33. ONODA, F., M. TAKEDA, M. SEKI, D. MAEDA, J. TAJIMA et al., 2004 SMC6 is required for MMS-induced interchromosomal and sister chromatid recombinations in Saccharomyces cerevisiae. DNA Repair 3: 429-439.
34. ORTIZ, J., O. STEMMANN, S. RANK and J. LECHNER, 1999 A putative protein complex consisting of Ctf19, Mcm21, and Okp1 represents a missing link in the budding yeast kinetochore. Genes Dev. 13: 1140-1155.
35. OZENBERGER, B. A., and G. S. ROEDER, 1991 A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol. 11: 1222-1231.
36. PAPOULI, E., S. CHEN, A. A. DAVIES, D. HUTTNER, L. KREJCI et al., 2005 Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19: 123-133.
37. PEBERNARD, S., W. H. MCDONALD, Y. PAVLOVA, J. R. YATES, 3RD and M. N. BODDY, 2004 Nse1, Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a crucial role in meiosis. Mol. Biol. Cell 15: 4866-4876.
38. PELLICIOLI, A., C. LUCCA, G. LIBERI, F. MARINI, M. LOPES et al., 1999 Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18: 6561-6572.
39. 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.
40. POTTS, P. R., and H. YU, 2005 Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 25: 7021-7032.
41. PRAKASH, L., and S. PRAKASH, 1977 Isolation and characterization of MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 86: 33-55.
42. SEELER, J. S., and A. DEJEAN, 2003 Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell. Biol. 4: 690-699.
43. SEIGNEUR, M., V. BIDNENKO, S. D. EHRLICH and B. MICHEL, 1998 RuvAB acts at arrested replication forks. Cell 95: 419-430.
44. SERGEANT, J., E. TAYLOR, J. PALECEK, M. FOUSTERI, E. A. ANDREWS et al., 2005 Composition and architecture of the Schizosaccharomyces pombe Rad18 (Smc5-6) complex. Mol. Cell. Biol. 25: 172-184.
45. SHEEDY, D. M., D. DIMITROVA, J. K. RANKIN, K. L. BASS, K. M. LEE et al., 2005 Brc1-mediated DNA repair and damage tolerance. Genetics 171: 457-468.
46. SOGO, J. M., M. LOPES and M. FOIANI, 2002 Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
47. SPENCER, F., S. L. GERRING, C. CONNELLY and P. HIETER, 1990 Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124: 237-249.
48. STRAY, J. E., and J. E. LINDSLEY, 2003 Biochemical analysis of the yeast condensin Smc2/4 complex: an ATPase that promotes knotting of circular DNA. J. Biol. Chem. 278: 26238-26248.
49. STRUNNIKOV, A. V., E. HOGAN and D. KOSHLAND, 1995 SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev. 9: 587-599.
50. 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.
51. TORRES-ROSELL, J., F. MACHIN and L. ARAGON, 2005a Smc5-Smc6 complex preserves nucleolar integrity in S. cerevisiae. Cell Cycle 4: 868-872.
52. TORRES-ROSELL, J., F. MACHIN, S. FARMER, A. JARMUZ, T. EYDMANN et al., 2005b SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions. Nat. Cell Biol. 7: 412-419.
53. VERKADE, H. M., S. J. BUGG, H. D. LINDSAY, A. M. CARR and M. J. O'CONNELL, 1999 Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol. Biol. Cell 10: 2905-2918.
54. 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.
55. ZHAO, X., C. Y. WU and G. BLOBEL, 2004 Mlp-dependent anchorage and stabilization of a desumoylating enzyme is required to prevent clonal lethality. J. Cell Biol. 167: 605-611.