Mph1p promotes gross chromosomal rearrangement through partial inhibition of homologous recombination

Journal of Cell Biology

Volumn 181, Issue 7, 2008, Pages 1083-1093

  Banerjee, Soma ^a,c   Smith, Stephanie ^a   Oum, Ji Hyun ^b   Liaw, Hung Jiun ^a   Hwang, Ji Young ^a,d   Sikdar, Nilabja ^a   Motegi, Akira ^a,e   Sang, Eun Lee ^b   Myung, Kyungjae ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b University of Texas Health Science Center at San Antonio   (United States)

^c INSTITUTE OF POST GRADUATE MEDICAL EDUCATION AND RESEARCH   (India)

^d Seoul Media Institute of Technology   (South Korea)

^e KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DEAD BOX PROTEIN; HELICASE; MESYLIC ACID METHYL ESTER; RAD51 PROTEIN; REPLICATION FACTOR A;

ARTICLE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; ENZYME ACTIVITY; GENE; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; GENE REPRESSION; HOMOLOGOUS RECOMBINATION; MPH1 GENE; MUTATOR GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SRS2 GENE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID MOTIFS; CHROMOSOMES, FUNGAL; DEAD-BOX RNA HELICASES; METHYL METHANESULFONATE; MUTATION; PROTEIN BINDING; RECOMBINATION, GENETIC; REPLICATION PROTEIN A; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 46249091062     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200711146     Document Type: Article

References (44)

1. Aguilera, A., and H.L. Klein. 1989. Yeast intrachromosomal recombination: long gene conversion tracts are preferentially associated with reciprocal exchange and require the RAD1 and RAD3 gene products. Genetics. 123:683-694.
2. Banerjee, S., S. Smith, and K. Myung. 2006. Suppression of gross chromosomal rearrangements by yKu70-yKu80 heterodimer through DNA damage checkpoints. Proc. Natl. Acad. Sci. USA. 103:1816-1821.
3. Budd, M.E., C.C. Reis, S. Smith, K. Myung, and J.L. Campbell. 2006. Evidence suggesting that Pif1 helicase functions in DNA replication with the Dna2 helicase/nuclease and DNA polymerase delta. Mol. Cell. Biol. 26:2490-2500.
4. Cheok, C.F., C.Z. Bachrati, K.L. Chan, C. Ralf, L. Wu, and I.D. Hickson. 2005. Roles of the Bloom's syndrome helicase in the maintenance of genome stability. Biochem. Soc. Trans. 33:1456-1459.
5. Clarke, L., and J. Carbon. 1 976. A colony bank containing synthetic Col E1 hybrid plasmids representative of the entire E. coli genome. Cell. 9:91-99.
6. Firmenich, A.A., M. Elias-Arnanz, and P. Berg. 1995. A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52. Mol. Cell. Biol. 15:1620-1631.
7. 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.
8. Gavin, A.C., P. Aloy, P. Grandi, R. Krause, M. Boesche, M. Marzioch, C. Rau, L.J. Jensen, S. Bastuck, B. Dumpelfeld, et al. 2006. Proteome survey reveals modularity of the yeast cell machinery. Nature. 440:631-636.
9. Hwang, J.Y., S. Smith, and K. Myung. 2005. The Rad1-Rad10 complex promotes the production of gross chromosomal rearrangements from spontaneous DNA damage in Saccharomyces cerevisiae. Genetics. 169:1927-1937.
10. 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.
11. Kennedy, R.D., and A.D. D'Andrea. 2005. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev. 19:2925-2940.
12. Kolodner, R.D., C.D. Putnam, and K. Myung. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science. 297:552-557.
13. Komori, K., M. Hidaka, T. Horiuchi, R. Fujikane, H. Shinagawa, and Y. Ishino. 2004. Cooperation of the N-terminal Helicase and C-terminal endonuclease activities of Archaeal Hef protein in processing stalled replication forks. J. Biol. Chem. 279:53175-53185.
14. 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.
15. Lea, D.E., and C.A. Coulson. 1948. The distribution of the numbers of mutants in bacterial populations. J. Genet. 49:264-285.
16. Lengauer, C. 2005. Aneuploidy and genetic instability in cancer. Semin. Cancer Biol. 15:1.
17. 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.
18. Levran, O., C. Attwooll, R.T. Henry, K.L. Milton, K. Neveling, P. Rio, S.D. Batish, R. Kalb, E. Velleuer, S. Barral, et al. 2005. The BRCA1-interacting helicase BRIP1 is deficient in Fanconi anemia. Nat. Genet. 37:931-933.
19. Lisby, M., J.H. Barlow, R.C. Burgess, and R. Rothstein. 2004. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell. 118:699-713.
20. Marcand, S., V. Brevet, C. Mann, and E. Gilson. 2000. Cell cycle restriction of telomere elongation. Curr. Biol. 10:487-490.
21. Meetei, A.R., A.L. Medhurst, C. Ling, Y. Xue, T.R. Singh, P. Bier, J. Steltenpool, S. Stone, I. Dokal, C.G. Mathew, et al. 2005. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat. Genet. 37:958-963.
22. Mosedale, G., W. Niedzwiedz, A. Alpi, F. Perrina, J.B. Pereira-Leal, M. Johnson, F. Langevin, P. Pace, and K.J. Patel. 2005. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat. Struct. Mol. Biol. 12:763-771.
23. Motegi, A., and K. Myung. 2007. Measuring the rate of gross chromosomal rearrangements in Saccharomyces cerevisiae: A practical approach to study genomic rearrangements observed in cancer. Methods. 41:168-176.
24. Motegi, A., K. Kuntz, A. Majeed, S. Smith, and K. Myung. 2006. Regulation of gross chromosomal rearrangements by ubiquitin and SUMO ligases in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:1424-1433.
25. Myung, K., C. Chen, and R.D. Kolodner. 2001a. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature. 411:1073-1076.
26. Myung, K., A. Datta, C. Chen, and R.D. Kolodner. 2001b. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27:113-116.
27. Myung, K., A. Datta, and R.D. Kolodner. 2001c. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell. 104:397-408.
28. Onge, R.P., R. Mani, J. Oh, M. Proctor, E. Fung, R.W. Davis, C. Nislow, F.P. Roth, and G. Giaever. 2007. Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet. 39:199-206.
29. Opresko, P.L., W.H. Cheng, and V.A. Bohr. 2004. Junction of RecQ helicase biochemistry and human disease. J. Biol. Chem. 279:18099-18102.
30. 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.
31. 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.
32. 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.
33. Schulz, V.P., and V.A. Zakian. 1994. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell. 76:145-155.
34. 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.
35. Shim, E.Y., J.L. Ma, J.H. Oum, Y. Yanez, and S.E. Lee. 2005. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25:3934-3944.
36. Smith, S., J.-Y. Hwang, S. Banerjee, A. Majeed, A. Gupta, and K. Myung. 2004. Mutaor genes for suppression of gross chromosomal rearrangements identified by a genome-wide screening in Saccharoymces cerevisiae. Proc. Natl. Acad. Sci. USA. 101:9039-9044.
37. 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.
38. 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.
39. 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.
40. Tong, A.H., G. Lesage, G.D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G.F. Berriz, R.L. Brost, M. Chang, et al. 2004. Global mapping of the yeast genetic interaction network. Science. 303:808-813.
41. 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.
42. Wu, X., C. Wu, and J.E. Haber. 1997. Rules of donor preference in Saccharomyces mating-type gene switching revealed by a competition assay involving two types of recombination. Genetics. 147:399-407.
43. Xu, H., C. Boone, and H.L. Klein. 2004. Mrc1 is required for sister chromatid cohesion to aid in recombination repair of spontaneous damage. Mol. Cell. Biol. 24:7082-7090.
44. Zhou, J., E.K. Monson, S.C. Teng, V.P. Schulz, and V.A. Zakian. 2000. P if1p helicase, a catalytic inhibitor of telomerase in yeast. Science. 289:771-774.