This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Signon, L.
Right arrow Articles by Haber, J. E.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Signon, L.
Right arrow Articles by Haber, J. E.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, March 2001, p. 2048-2056, Vol. 21, No. 6
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.6.2048-2056.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Genetic Requirements for RAD51- and RAD54-Independent Break-Induced Replication Repair of a Chromosomal Double-Strand Break

Laurence Signon,1,dagger Anna Malkova,1 Maria L. Naylor,1 Hannah Klein,2 and James E. Haber1,*

Department of Biology and Rosenstiel Center, Brandeis University, Waltham, Massachusetts 02254-9110,1 and Department of Biochemistry, New York University School of Medicine, New York, New York 100162

Received 18 July 2000/Returned for modification 12 September 2000/Accepted 3 January 2001

Broken chromosomes can be repaired by several homologous recombination mechanisms, including gene conversion and break-induced replication (BIR). In Saccharomyces cerevisiae, an HO endonuclease-induced double-strand break (DSB) is normally repaired by gene conversion. Previously, we have shown that in the absence of RAD52, repair is nearly absent and diploid cells lose the broken chromosome; however, in cells lacking RAD51, gene conversion is absent but cells can repair the DSB by BIR. We now report that gene conversion is also abolished when RAD54, RAD55, and RAD57 are deleted but BIR occurs, as with rad51Delta cells. DSB-induced gene conversion is not significantly affected when RAD50, RAD59, TID1 (RDH54), SRS2, or SGS1 is deleted. Various double mutations largely eliminate both gene conversion and BIR, including rad51Delta rad50Delta , rad51Delta rad59Delta , and rad54Delta tid1Delta . These results demonstrate that there is a RAD51- and RAD54-independent BIR pathway that requires RAD59, TID1, RAD50, and presumably MRE11 and XRS2. The similar genetic requirements for BIR and telomere maintenance in the absence of telomerase also suggest that these two processes proceed by similar mechanisms.

* Corresponding author. Mailing address: MS029 Rosenstiel Center, Brandeis University, Waltham, MA 02454-9110. Phone: (781) 736-2462. Fax: (781) 736-2405. E-mail: haber{at}brandeis.edu.

dagger Present address: CIML, Parc Scientifique de Luminy, 13 288 Marseille Cedex 9, France.

Molecular and Cellular Biology, March 2001, p. 2048-2056, Vol. 21, No. 6
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.6.2048-2056.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Nagaraju, G., Hartlerode, A., Kwok, A., Chandramouly, G., Scully, R. (2009). XRCC2 and XRCC3 Regulate the Balance between Short- and Long-Tract Gene Conversions between Sister Chromatids. Mol. Cell. Biol. 29: 4283-4294 [Abstract] [Full Text]  
  • Willis, N., Rhind, N. (2009). Mus81, Rhp51(Rad51), and Rqh1 Form an Epistatic Pathway Required for the S-Phase DNA Damage Checkpoint. Mol. Biol. Cell 20: 819-833 [Abstract] [Full Text]  
  • Andersen, M. P., Nelson, Z. W., Hetrick, E. D., Gottschling, D. E. (2008). A Genetic Screen for Increased Loss of Heterozygosity in Saccharomyces cerevisiae. Genetics 179: 1179-1195 [Abstract] [Full Text]  
  • Coic, E., Feldman, T., Landman, A. S., Haber, J. E. (2008). Mechanisms of Rad52-Independent Spontaneous and UV-Induced Mitotic Recombination in Saccharomyces cerevisiae. Genetics 179: 199-211 [Abstract] [Full Text]  
  • Pohl, T. J., Nickoloff, J. A. (2008). Rad51-Independent Interchromosomal Double-Strand Break Repair by Gene Conversion Requires Rad52 but Not Rad55, Rad57, or Dmc1. Mol. Cell. Biol. 28: 897-906 [Abstract] [Full Text]  
  • Mozlin, A. M., Fung, C. W., Symington, L. S. (2008). Role of the Saccharomyces cerevisiae Rad51 Paralogs in Sister Chromatid Recombination. Genetics 178: 113-126 [Abstract] [Full Text]  
  • Maxwell, P. H., Curcio, M. J. (2007). Retrosequence formation restructures the yeast genome. Genes Dev. 21: 3308-3318 [Abstract] [Full Text]  
  • Cullen, J. K., Hussey, S. P., Walker, C., Prudden, J., Wee, B.-Y., Dave, A., Findlay, J. S., Savory, A. P., Humphrey, T. C. (2007). Break-Induced Loss of Heterozygosity in Fission Yeast: Dual Roles for Homologous Recombination in Promoting Translocations and Preventing De Novo Telomere Addition. Mol. Cell. Biol. 27: 7745-7757 [Abstract] [Full Text]  
  • Cortes-Ledesma, F., Tous, C., Aguilera, A. (2007). Different genetic requirements for repair of replication-born double-strand breaks by sister-chromatid recombination and break-induced replication. Nucleic Acids Res 35: 6560-6570 [Abstract] [Full Text]  
  • VanHulle, K., Lemoine, F. J., Narayanan, V., Downing, B., Hull, K., McCullough, C., Bellinger, M., Lobachev, K., Petes, T. D., Malkova, A. (2007). Inverted DNA Repeats Channel Repair of Distant Double-Strand Breaks into Chromatid Fusions and Chromosomal Rearrangements. Mol. Cell. Biol. 27: 2601-2614 [Abstract] [Full Text]  
  • Wu, Y., Siino, J. S., Sugiyama, T., Kowalczykowski, S. C. (2006). The DNA Binding Preference of RAD52 and RAD59 Proteins: IMPLICATIONS FOR RAD52 AND RAD59 PROTEIN FUNCTION IN HOMOLOGOUS RECOMBINATION. J. Biol. Chem. 281: 40001-40009 [Abstract] [Full Text]  
  • Javaheri, A., Wysocki, R., Jobin-Robitaille, O., Altaf, M., Cote, J., Kron, S. J. (2006). Yeast G1 DNA damage checkpoint regulation by H2A phosphorylation is independent of chromatin remodeling. Proc. Natl. Acad. Sci. USA 103: 13771-13776 [Abstract] [Full Text]  
  • Valencia-Burton, M., Oki, M., Johnson, J., Seier, T. A., Kamakaka, R., Haber, J. E. (2006). Different Mating-Type-Regulated Genes Affect the DNA Repair Defects of Saccharomyces RAD51, RAD52 and RAD55 Mutants. Genetics 174: 41-55 [Abstract] [Full Text]  
  • Ogiwara, H., Ui, A., Onoda, F., Tada, S., Enomoto, T., Seki, M. (2006). Dpb11, the budding yeast homolog of TopBP1, functions with the checkpoint clamp in recombination repair. Nucleic Acids Res 34: 3389-3398 [Abstract] [Full Text]  
  • Wu, Y., Sugiyama, T., Kowalczykowski, S. C. (2006). DNA Annealing Mediated by Rad52 and Rad59 Proteins. J. Biol. Chem. 281: 15441-15449 [Abstract] [Full Text]  
  • Wesoly, J., Agarwal, S., Sigurdsson, S., Bussen, W., Van Komen, S., Qin, J., van Steeg, H., van Benthem, J., Wassenaar, E., Baarends, W. M., Ghazvini, M., Tafel, A. A., Heath, H., Galjart, N., Essers, J., Grootegoed, J. A., Arnheim, N., Bezzubova, O., Buerstedde, J.-M., Sung, P., Kanaar, R. (2006). Differential Contributions of Mammalian Rad54 Paralogs to Recombination, DNA Damage Repair, and Meiosis. Mol. Cell. Biol. 26: 976-989 [Abstract] [Full Text]  
  • Azam, M., Lee, J. Y., Abraham, V., Chanoux, R., Schoenly, K. A., Johnson, F. B. (2006). Evidence that the S.cerevisiae Sgs1 protein facilitates recombinational repair of telomeres during senescence. Nucleic Acids Res 34: 506-516 [Abstract] [Full Text]  
  • Yang, C.-P., Chen, Y.-B., Meng, F.-L., Zhou, J.-Q. (2006). Saccharomyces cerevisiae Est3p dimerizes in vitro and dimerization contributes to efficient telomere replication in vivo. Nucleic Acids Res 34: 407-416 [Abstract] [Full Text]  
  • Kateneva, A. V., Konovchenko, A. A., Guacci, V., Dresser, M. E. (2005). Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae. JCB 171: 241-253 [Abstract] [Full Text]  
  • Putnam, C. D., Pennaneach, V., Kolodner, R. D. (2005). Saccharomyces cerevisiae as a Model System To Define the Chromosomal Instability Phenotype. Mol. Cell. Biol. 25: 7226-7238 [Abstract] [Full Text]  
  • Chen, Y.-B., Yang, C.-P., Li, R.-X., Zeng, R., Zhou, J.-Q. (2005). Def1p Is Involved in Telomere Maintenance in Budding Yeast. J. Biol. Chem. 280: 24784-24791 [Abstract] [Full Text]  
  • Malkova, A., Naylor, M. L., Yamaguchi, M., Ira, G., Haber, J. E. (2005). RAD51-Dependent Break-Induced Replication Differs in Kinetics and Checkpoint Responses from RAD51-Mediated Gene Conversion. Mol. Cell. Biol. 25: 933-944 [Abstract] [Full Text]  
  • Liberi, G., Maffioletti, G., Lucca, C., Chiolo, I., Baryshnikova, A., Cotta-Ramusino, C., Lopes, M., Pellicioli, A., Haber, J. E., Foiani, M. (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 [Abstract] [Full Text]  
  • Ramirez, M., Vinagre, A., Ambrona, J., Molina, F., Maqueda, M., Rebollo, J. E. (2004). Genetic Instability of Heterozygous, Hybrid, Natural Wine Yeasts. Appl. Environ. Microbiol. 70: 4686-4691 [Abstract] [Full Text]  
  • Puizina, J., Siroky, J., Mokros, P., Schweizer, D., Riha, K. (2004). Mre11 Deficiency in Arabidopsis Is Associated with Chromosomal Instability in Somatic Cells and Spo11-Dependent Genome Fragmentation during Meiosis. Plant Cell 16: 1968-1978 [Abstract] [Full Text]  
  • Sugawara, N., Goldfarb, T., Studamire, B., Alani, E., Haber, J. E. (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 [Abstract] [Full Text]  
  • Soustelle, C., Vernis, L., Freon, K., Reynaud-Angelin, A., Chanet, R., Fabre, F., Heude, M. (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 [Abstract] [Full Text]  
  • Torres, J. Z., Schnakenberg, S. L., Zakian, V. A. (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 [Abstract] [Full Text]  
  • Maringele, L., Lydall, D. (2004). EXO1 Plays a Role in Generating Type I and Type II Survivors in Budding Yeast. Genetics 166: 1641-1649 [Abstract] [Full Text]  
  • Davis, A. P., Symington, L. S. (2004). RAD51-Dependent Break-Induced Replication in Yeast. Mol. Cell. Biol. 24: 2344-2351 [Abstract] [Full Text]  
  • Grandin, N., Charbonneau, M. (2003). Mitotic Cyclins Regulate Telomeric Recombination in Telomerase-Deficient Yeast Cells. Mol. Cell. Biol. 23: 9162-9177 [Abstract] [Full Text]  
  • Trujillo, K. M., Roh, D. H., Chen, L., Van Komen, S., Tomkinson, A., Sung, P. (2003). Yeast Xrs2 Binds DNA and Helps Target Rad50 and Mre11 to DNA Ends. J. Biol. Chem. 278: 48957-48964 [Abstract] [Full Text]  
  • Lee, S. E., Pellicioli, A., Vaze, M. B., Sugawara, N., Malkova, A., Foiani, M., Haber, J. E. (2003). Yeast Rad52 and Rad51 Recombination Proteins Define a Second Pathway of DNA Damage Assessment in Response to a Single Double-Strand Break. Mol. Cell. Biol. 23: 8913-8923 [Abstract] [Full Text]  
  • Tsukamoto, M., Yamashita, K., Miyazaki, T., Shinohara, M., Shinohara, A. (2003). The N-Terminal DNA-Binding Domain of Rad52 Promotes RAD51-Independent Recombination in Saccharomyces cerevisiae. Genetics 165: 1703-1715 [Abstract] [Full Text]  
  • Spell, R. M., Jinks-Robertson, S. (2003). Role of Mismatch Repair in the Fidelity of RAD51- and RAD59-Dependent Recombination in Saccharomyces cerevisiae. Genetics 165: 1733-1744 [Abstract] [Full Text]  
  • Grandin, N., Charbonneau, M. (2003). The Rad51 Pathway of Telomerase-Independent Maintenance of Telomeres Can Amplify TG1-3 Sequences in yku and cdc13 Mutants of Saccharomyces cerevisiae. Mol. Cell. Biol. 23: 3721-3734 [Abstract] [Full Text]  
  • Myung, K., Pennaneach, V., Kats, E. S., Kolodner, R. D. (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 [Abstract] [Full Text]  
  • Dong, Z., Fasullo, M. (2003). Multiple recombination pathways for sister chromatid exchange in Saccharomyces cerevisiae: role of RAD1 and the RAD52 epistasis group genes. Nucleic Acids Res 31: 2576-2585 [Abstract] [Full Text]  
  • Yoshida, J., Umezu, K., Maki, H. (2003). Positive and Negative Roles of Homologous Recombination in the Maintenance of Genome Stability in Saccharomyces cerevisiae. Genetics 164: 31-46 [Abstract] [Full Text]  
  • Schmuckli-Maurer, J., Rolfsmeier, M., Nguyen, H., Heyer, W.-D. (2003). Genome instability in rad54 mutants of Saccharomyces cerevisiae. Nucleic Acids Res 31: 1013-1023 [Abstract] [Full Text]  
  • Stark, J. M., Jasin, M. (2003). Extensive Loss of Heterozygosity Is Suppressed during Homologous Repair of Chromosomal Breaks. Mol. Cell. Biol. 23: 733-743 [Abstract] [Full Text]  
  • Fabre, F., Chan, A., Heyer, W.-D., Gangloff, S. (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 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Rattray, A. J., Shafer, B. K., McGill, C. B., Strathern, J. N. (2002). The Roles of REV3 and RAD57 in Double-Strand-Break-Repair-Induced Mutagenesis of Saccharomyces cerevisiae. Genetics 162: 1063-1077 [Abstract] [Full Text]  
  • Vance, J. R., Wilson, T. E. (2002). Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc. Natl. Acad. Sci. USA 99: 13669-13674 [Abstract] [Full Text]  
  • Gonzalez-Barrera, S., Garcia-Rubio, M., Aguilera, A. (2002). Transcription and Double-Strand Breaks Induce Similar Mitotic Recombination Events in Saccharomyces cerevisiae. Genetics 162: 603-614 [Abstract] [Full Text]  
  • Shor, E., Gangloff, S., Wagner, M., Weinstein, J., Price, G., Rothstein, R. (2002). Mutations in Homologous Recombination Genes Rescue top3 Slow Growth in Saccharomyces cerevisiae. Genetics 162: 647-662 [Abstract] [Full Text]  
  • Ira, G., Haber, J. E. (2002). Characterization of RAD51-Independent Break-Induced Replication That Acts Preferentially with Short Homologous Sequences. Mol. Cell. Biol. 22: 6384-6392 [Abstract] [Full Text]  
  • Freedman, J. A., Jinks-Robertson, S. (2002). Genetic Requirements for Spontaneous and Transcription-Stimulated Mitotic Recombination in Saccharomyces cerevisiae. Genetics 162: 15-27 [Abstract] [Full Text]  
  • de Jager, M., Kanaar, R. (2002). Genome instability and Rad50S: subtle yet severe. Genes Dev. 16: 2173-2178 [Full Text]  
  • Difilippantonio, M. J., Petersen, S., Chen, H. T., Johnson, R., Jasin, M., Kanaar, R., Ried, T., Nussenzweig, A. (2002). Evidence for Replicative Repair of DNA Double-Strand Breaks Leading to Oncogenic Translocation and Gene Amplification. JEM 196: 469-480 [Abstract] [Full Text]  
  • Kolodner, R. D., Putnam, C. D., Myung, K. (2002). Maintenance of Genome Stability in Saccharomyces cerevisiae. Science 297: 552-557 [Abstract] [Full Text]  
  • Butler, D. K., Gillespie, D., Steele, B. (2002). Formation of Large Palindromic DNA by Homologous Recombination of Short Inverted Repeat Sequences in Saccharomyces cerevisiae. Genetics 161: 1065-1075 [Abstract] [Full Text]  
  • Stark, J. M., Hu, P., Pierce, A. J., Moynahan, M. E., Ellis, N., Jasin, M. (2002). ATP Hydrolysis by Mammalian RAD51 Has a Key Role during Homology-directed DNA Repair. J. Biol. Chem. 277: 20185-20194 [Abstract] [Full Text]  
  • van den Bosch, M., Zonneveld, J. B. M., Vreeken, K., de Vries, F. A. T., Lohman, P. H. M., Pastink, A. (2002). Differential expression and requirements for Schizosaccharomyces pombeRAD52 homologs in DNA repair and recombination. Nucleic Acids Res 30: 1316-1324 [Abstract] [Full Text]  
  • Klein, H. L. (2001). Spontaneous Chromosome Loss in Saccharomyces cerevisiae Is Suppressed by DNA Damage Checkpoint Functions. Genetics 159: 1501-1509 [Abstract] [Full Text]  
  • Davis, A. P., Symington, L. S. (2001). The Yeast Recombinational Repair Protein Rad59 Interacts With Rad52 and Stimulates Single-Strand Annealing. Genetics 159: 515-525 [Abstract] [Full Text]  
  • Kraus, E., Leung, W.-Y., Haber, J. E. (2001). Break-induced replication: A review and an example in budding yeast. Proc. Natl. Acad. Sci. USA 98: 8255-8262 [Abstract] [Full Text]  
  • Malkova, A., Signon, L., Schaefer, C. B., Naylor, M. L., Theis, J. F., Newlon, C. S., Haber, J. E. (2001). RAD51-independent break-induced replication to repair a broken chromosome depends on a distant enhancer site. Genes Dev. 15: 1055-1060 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»