Defects in DNA lesion bypass lead to spontaneous chromosomal rearrangements and increased cell death

Eukaryotic Cell

Volumn 9, Issue 2, 2010, Pages 315-324

  Schmidt, Kristina H ^a   Viebranz, Emilie B ^a   Harris, Lorena B ^a   Mirzaei Souderjani, Hamed ^a   Syed, Salahuddin ^a   Medicus, Robin ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; HELICASE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL DEATH; CHROMOSOME; CHROMOSOME ABERRATION; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; FUNGAL GENOME; GENE REARRANGEMENT; GENETIC RECOMBINATION; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

CELL DEATH; CHROMOSOME ABERRATIONS; CHROMOSOMES, FUNGAL; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; GENE REARRANGEMENT; GENOME, FUNGAL; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 75849122515     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00260-09     Document Type: Article

References (50)

1. Banerjee, S., S. Smith, J. H. Oum, H. J. Liaw, J. Y. Hwang, N. Sikdar, A. Motegi, S. E. Lee, and K. Myung. 2008. Mph1p promotes gross chromosomal rearrangement through partial inhibition of homologous recombination. J. Cell Biol. 181:1083-1093.
2. Chen, C., K. Umezu, and R. D. Kolodner. 1998. Chromosomal rearrangements occur in S. cerevisiae rfa1 mutator mutants due to mutagenic lesions processed by double-strand-break repair. Mol. Cell 2:9-22.
3. Entian, K. D., T. Schuster, J. H. Hegemann, D. Becher, H. Feldmann, U. Guldener, R. Gotz, M. Hansen, C. P. Hollenberg, G. Jansen, W. Kramer, S. Klein, P. Kotter, J. Kricke, H. Launhardt, G. Mannhaupt, A. Maierl, P. Meyer, W. Mewes, T. Munder, R. K. Niedenthal, M. Ramezani Rad, A. Rohmer, A. Romer, A. Hinnen, et al. 1999. Functional analysis of 150 deletion mutants in Saccharomyces cerevisiae by a systematic approach. Mol. Gen. Genet. 262:683-702.
4. 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. U. S. A. 99:16887-16892.
5. 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.
6. Gangloff, S., C. Soustelle, and F. Fabre. 2000. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25:192-194.
7. Gari, K., C. Decaillet, M. Delannoy, L. Wu, and A. Constantinou. 2008. Remodeling of DNA replication structures by the branch point translocase FANCM. Proc. Natl. Acad. Sci. U. S. A. 105:16107-16112.
8. Gari, K., C. Decaillet, A. Z. Stasiak, A. Stasiak, and A. Constantinou. 2008. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 29:141-148.
9. Gietz, R. D., and R. A. Woods. 2006. Yeast transformation by the LiAc/SS carrier DNA/PEG method. Methods Mol. Biol. 313:107-120.
10. Hirota, Y., and J. M. Lahti. 2000. Characterization of the enzymatic activity of hChlR1, a novel human DNA helicase. Nucleic Acids Res. 28:917-924.
11. Holloway, S. L. 2000. CHL1 is a nuclear protein with an essential ATP binding site that exhibits a size-dependent effect on chromosome segregation. Nucleic Acids Res. 28:3056-3064.
12. Ira, G., A. Malkova, G. Liberi, M. Foiani, and J. E. Haber. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401-411.
13. Ivessa, A. S., B. A. Lenzmeier, J. B. Bessler, L. K. Goudsouzian, S. L. Schnakenberg, and V. A. Zakian. 2003. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell 12:1525-1536.
14. Ivessa, A. S., J. Q. Zhou, V. P. Schulz, E. K. Monson, and V. A. Zakian. 2002. Saccharomyces Rrm3p, a 5 to 3 DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16:1383-1396.
15. Joenje, H., and K. J. Patel. 2001. The emerging genetic and molecular basis of Fanconi anaemia. Nat. Rev. Genet. 2:446-457.
16. Kennedy, R. D., and A. D. D'Andrea. 2005. The Fanconi anemia/BRCA pathway: new faces in the crowd. Genes Dev. 19:2925-2940.
17. Klein, H. L. 2001. Mutations in recombinational repair and in checkpoint control genes suppress the lethal combination of srs2Delta with other DNA repair genes in Saccharomyces cerevisiae. Genetics 157:557-565.
18. Kolodner, R. D., C. D. Putnam, and K. Myung. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552-557.
19. 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.
20. Lee, S. K., R. E. Johnson, S. L. Yu, L. Prakash, and S. Prakash. 1999. Requirement of yeast SGS1 and SRS2 genes for replication and transcription. Science 286:2339-2342.
21. 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.
22. Lo, Y. C., K. S. Paffett, O. Amit, J. A. Clikeman, R. Sterk, M. A. Brenneman, and J. A. Nickoloff. 2006. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell Biol. 26:4086-4094.
23. Mathew, C. G. 2006. Fanconi anaemia genes and susceptibility to cancer. Oncogene 25:5875-5884.
24. Mullen, J. R., V. Kaliraman, and S. J. Brill. 2000. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154:1101-1114.
25. 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.
26. Nair, K. R. 1940. Table of confidence intervals for the median in samples from any continuous population. Sankhya 4:551-558.
27. Niedzwiedz, W., G. Mosedale, M. Johnson, C. Y. Ong, P. Pace, and K. J. Patel. 2004. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell 15:607-620.
28. Ogiwara, H., A. Ui, M. S. Lai, T. Enomoto, and M. Seki. 2007. Chl1 and Ctf4 are required for damage-induced recombinations. Biochem. Biophys. Res. Commun. 354:222-226.
29. Ooi, S. L., D. D. Shoemaker, and J. D. Boeke. 2003. DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 35:277-286.
30. Petronczki, M., B. Chwalla, M. F. Siomos, S. Yokobayashi, W. Helmhart, A. M. Deutschbauer, R. W. Davis, Y. Watanabe, and K. Nasmyth. 2004. Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/ Ctf8, the helicase Chl1 and the polymerase-alpha-associated protein Ctf4 is essential for chromatid disjunction during meiosis II. J. Cell Sci. 117:3547-3559.
31. 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.
32. Prakash, R., L. Krejci, S. Van Komen, K. Anke Schurer, W. Kramer, and P. Sung. 2005. Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3 to 5 DNA helicase. J. Biol. Chem. 280:7854-7860.
33. Prakash, R., D. Satory, E. Dray, A. Papusha, J. Scheller, W. Kramer, L. Krejci, H. Klein, J. E. Haber, P. Sung, and G. Ira. 2009. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev. 23:67-79.
34. Putnam, C. D., T. K. Hayes, and R. D. Kolodner. 2009. Specific pathways prevent duplication-mediated genome rearrangements. Nature 460:984-989.
35. Robert, T., D. Dervins, F. Fabre, and S. Gangloff. 2006. Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover. EMBO J. 25:2837-2846.
36. Scheller, J., A. Schurer, C. Rudolph, S. Hettwer, and W. Kramer. 2000. MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155:1069-1081.
37. Schmidt, K. H., and R. D. Kolodner. 2004. Requirement of Rrm3 helicase for repair of spontaneous DNA lesions in cells lacking Srs2 or Sgs1 helicase. Mol. Cell. Biol. 24:3213-3226.
38. Schmidt, K. H., and R. D. Kolodner. 2006. Suppression of spontaneous genome rearrangements in yeast DNA helicase mutants. Proc. Natl. Acad. Sci. U. S. A. 103:18196-18201.
39. Schmidt, K. H., V. Pennaneach, C. D. Putnam, and R. D. Kolodner. 2006. Analysis of gross-chromosomal rearrangements in Saccharomyces cerevisiae. Methods Enzymol. 409:462-476.
40. Schmidt, K. H., J. Wu, and R. D. Kolodner. 2006. Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom's syndrome protein. Mol. Cell. Biol. 26:5406-5420.
41. 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.
42. Shiratori, A., T. Shibata, M. Arisawa, F. Hanaoka, Y. Murakami, and T. Eki. 1999. Systematic identification, classification, and characterization of the open reading frames which encode novel helicase-related proteins in Saccharomyces cerevisiae by gene disruption and Northern analysis. Yeast 15: 219-253.
43. Sinclair, D. A., K. Mills, and L. Guarente. 1997. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science 277:1313-1316.
44. Thompson, L. H., J. M. Hinz, N. A. Yamada, and N. J. Jones. 2005. How Fanconi anemia proteins promote the four Rs: replication, recombination, repair, and recovery. Environ. Mol. Mutagen. 45:128-142.
45. Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G. F. Berriz, R. L. Brost, M. Chang, Y. Chen, X. Cheng, G. Chua, H. Friesen, D. S. Goldberg, J. Haynes, C. Humphries, G. He, S. Hussein, L. Ke, N. Krogan, Z. Li, J. N. Levinson, H. Lu, P. Menard, C. Munyana, A. B. Parsons, O. Ryan, R. Tonikian, T. Roberts, A. M. Sdicu, J. Shapiro, B. Sheikh, B. Suter, S. L. Wong, L. V. Zhang, H. Zhu, C. G. Burd, S. Munro, C. Sander, J. Rine, J. Greenblatt, M. Peter, A. Bretscher, G. Bell, F. P. Roth, G. W. Brown, B. Andrews, H. Bussey, and C. Boone. 2004. Global mapping of the yeast genetic interaction network. Science 303:808-813.
46. Torres, J. Z., S. L. Schnakenberg, and V. A. Zakian. 2004. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 24:3198-3212.
47. Veaute, X., J. Jeusset, C. Soustelle, S. C. Kowalczykowski, E. Le Cam, and F. Fabre. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309-312.
48. Wang, W. 2007. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat. Rev. Genet. 8:735-748.
49. Watt, P. M., E. J. Louis, R. H. Borts, and I. D. Hickson. 1995. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253-260.
50. 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. U. S. A. 95:8733-8738.