Interaction of Mre11 and Rad50: Two Proteins Required for DNA Repair and Meiosis-Specific Double-Strand Break Formation in Saccharomyces cerevisiae

INVESTIGATIONS

Interaction of Mre11 and Rad50: Two Proteins Required for DNA Repair and Meiosis-Specific Double-Strand Break Formation in Saccharomyces cerevisiae

K. Johzuka and H. Ogawa
Department of Biology, Faculty of Science, Osaka University, Toyonaka, Osaka 560, Japan

A temperature-sensitive mre11-1 mutation of Saccharomyces cerevisiae causes defects in meiotic recombination and DNA repair during vegetative grwoth at a restrictive temperature. We cloned the MRE11 gene and found that it encodes a 643-amino acid protein with a highly acidic region containing a heptad repeat of Asp at its C-terminus and is located downstream of YMR44 near the RNA1 locus on the right arm of chromosome XIII. Transcripts of the MRE11 gene increased transiently and showed the same kinetics as that of the RAD50 gene during meiosis. In a mre11 disruption mutant (mre11::hisG), meiosis-specific double-strand break (DSB) formation is abolished. A comparison of the properties of mre11::hisG and a rad50 deletion mutant (rad50{delta}) indicated that both mutants exhibited similar phenotypes in both meiosis and mitosis. Characterization of two double mutants, mre11::hisG rad50{delta} and mre11::hisG rad50S, showed that MRE11 and RAD50 belong to the same epistasis group with respect to meiotic DSB formation and mitotic DNA repair. Using a two-hybrid system, we found that Mre11 interacts with Rad50 and itself in vivo. These results suggest that Mre11 and Rad50 proteins work in a complex in DSB formation and DNA repair during vegetative growth.

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				J. A. Young, R. W. Hyppa, and G. R. Smith Conserved and Nonconserved Proteins for Meiotic DNA Breakage and Repair in Yeasts Genetics, June 1, 2004; 167(2): 593 - 605. [Abstract] [Full Text] [PDF]

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				L. M. Arthur, K. Gustausson, K.-P. Hopfner, C. T. Carson, T. H. Stracker, A. Karcher, D. Felton, M. D. Weitzman, J. Tainer, and J. P. Carney Structural and functional analysis of Mre11-3 Nucleic Acids Res., March 26, 2004; 32(6): 1886 - 1893. [Abstract] [Full Text] [PDF]

				S.-J. Park, S. L. M. Ciccone, B. Freie, A. Kurimasa, D. J. Chen, G. C. Li, D. W. Clapp, and S.-H. Lee A Positive Role for the Ku Complex in DNA Replication Following Strand Break Damage in Mammals J. Biol. Chem., February 13, 2004; 279(7): 6046 - 6055. [Abstract] [Full Text] [PDF]

				J.-L. Ma, E. M. Kim, J. E. Haber, and S. E. Lee Yeast Mre11 and Rad1 Proteins Define a Ku-Independent Mechanism To Repair Double-Strand Breaks Lacking Overlapping End Sequences Mol. Cell. Biol., December 1, 2003; 23(23): 8820 - 8828. [Abstract] [Full Text] [PDF]

				M. Tsukamoto, K. Yamashita, T. Miyazaki, M. Shinohara, and A. Shinohara The N-Terminal DNA-Binding Domain of Rad52 Promotes RAD51-Independent Recombination in Saccharomyces cerevisiae Genetics, December 1, 2003; 165(4): 1703 - 1715. [Abstract] [Full Text] [PDF]

				J.-H. Lee, R. Ghirlando, V. Bhaskara, M. R. Hoffmeyer, J. Gu, and T. T. Paull Regulation of Mre11/Rad50 by Nbs1: EFFECTS ON NUCLEOTIDE-DEPENDENT DNA BINDING AND ASSOCIATION WITH ATAXIA-TELANGIECTASIA-LIKE DISORDER MUTANT COMPLEXES J. Biol. Chem., November 14, 2003; 278(46): 45171 - 45181. [Abstract] [Full Text] [PDF]

				L. Liu, M. Usher, Y. Hu, and E. B. Kmiec Nuclease Activity of Saccharomyces cerevisiae Mre11 Functions in Targeted Nucleotide Alteration Appl. Envir. Microbiol., October 1, 2003; 69(10): 6216 - 6224. [Abstract] [Full Text] [PDF]

				K. Jiao, L. Salem, and R. Malone Support for a Meiotic Recombination Initiation Complex: Interactions among Rec102p, Rec104p, and Spo11p Mol. Cell. Biol., August 15, 2003; 23(16): 5928 - 5938. [Abstract] [Full Text] [PDF]

				L. S. Symington Role of RAD52 Epistasis Group Genes in Homologous Recombination and Double-Strand Break Repair Microbiol. Mol. Biol. Rev., December 1, 2002; 66(4): 630 - 670. [Abstract] [Full Text] [PDF]

				L. F. Revers, J. M. Cardone, D. Bonatto, J. Saffi, M. Grey, H. Feldmann, M. Brendel, and J. A. P. Henriques Thermoconditional modulation of the pleiotropic sensitivity phenotype by the Saccharomyces cerevisiae PRP19 mutant allele pso4-1 Nucleic Acids Res., November 15, 2002; 30(22): 4993 - 5003. [Abstract] [Full Text] [PDF]

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				D. K. Butler, D. Gillespie, and B. Steele Formation of Large Palindromic DNA by Homologous Recombination of Short Inverted Repeat Sequences in Saccharomyces cerevisiae Genetics, July 1, 2002; 161(3): 1065 - 1075. [Abstract] [Full Text] [PDF]

				J. A. Farah, E. Hartsuiker, K.-i. Mizuno, K. Ohta, and G. R. Smith A 160-bp Palindrome Is a Rad50{middle dot}Rad32-Dependent Mitotic Recombination Hotspot in Schizosaccharomyces pombe Genetics, May 1, 2002; 161(1): 461 - 468. [Abstract] [Full Text] [PDF]

				C. Rinaldo, P. Bazzicalupo, S. Ederle, M. Hilliard, and A. La Volpe Roles for Caenorhabditis elegans rad-51 in Meiosis and in Resistance to Ionizing Radiation During Development Genetics, February 1, 2002; 160(2): 471 - 479. [Abstract] [Full Text] [PDF]

				L. K. Lewis, G. Karthikeyan, J. W. Westmoreland, and M. A. Resnick Differential Suppression of DNA Repair Deficiencies of Yeast rad50, mre11 and xrs2 Mutants by EXO1 and TLC1 (the RNA Component of Telomerase) Genetics, January 1, 2002; 160(1): 49 - 62. [Abstract] [Full Text] [PDF]

				S. Moreau, E. A. Morgan, and L. S. Symington Overlapping Functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 Nucleases in DNA Metabolism Genetics, December 1, 2001; 159(4): 1423 - 1433. [Abstract] [Full Text] [PDF]

				D. D'Amours and S. P. Jackson The yeast Xrs2 complex functions in S phase checkpoint regulation Genes & Dev., September 1, 2001; 15(17): 2238 - 2249. [Abstract] [Full Text] [PDF]

				L. Davis and G. R. Smith Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe PNAS, July 17, 2001; 98(15): 8395 - 8402. [Abstract] [Full Text] [PDF]

				A. Desai-Mehta, K. M. Cerosaletti, and P. Concannon Distinct Functional Domains of Nibrin Mediate Mre11 Binding, Focus Formation, and Nuclear Localization Mol. Cell. Biol., March 15, 2001; 21(6): 2184 - 2191. [Abstract] [Full Text]

				M. de Jager, M. L. G. Dronkert, M. Modesti, C. E. M. T. Beerens, R. Kanaar, and D. C. van Gent DNA-binding and strand-annealing activities of human Mre11: implications for its roles in DNA double-strand break repair pathways Nucleic Acids Res., March 15, 2001; 29(6): 1317 - 1325. [Abstract] [Full Text] [PDF]

				G. M. Chin and A. M. Villeneuve C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G2 DNA damage checkpoint Genes & Dev., March 1, 2001; 15(5): 522 - 534. [Abstract] [Full Text]