Suppression of gross chromosomal rearrangements by the multiple functions of the Mre11-Rad50-Xrs2 complex in Saccharomyces cerevisiae

DNA Repair

Volumn 4, Issue 5, 2005, Pages 606-617

  Smith, Stephanie ^a   Gupta, Amitabha ^a,c   Kolodner, Richard D ^b   Myung, Kyungjae ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Center for Language and Brain   (United States)

Author keywords

Cancer; Gross chromosomal rearrangements; Mre11 Rad50 Xrs2 complex

Indexed keywords

FUNGAL PROTEIN; NUCLEASE; PROTEIN COMPLEX MRX; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENETICS; CHROMOSOME REARRANGEMENT; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL GENETICS; GENE TRANSLOCATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; TELOMERE;

EID: 16244368497     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.01.004     Document Type: Article

References (77)

1. R.D. Kolodner, C.D. Putnam, and K. Myung Maintenance of genome stability in Saccharomyces cerevisiae Science 297 2002 552 557
2. C. Lengauer, K.W. Kinzler, and B. Vogelstein Genetic instabilities in human cancers Nature 396 1998 643 649
3. C.J. Vessey, C.J. Norbury, and I.D. Hickson Genetic disorders associated with cancer predisposition and genomic instability Prog. Nucl. Acid Res. Mol. Biol. 63 1999 189 221
4. K. Rennstam, B. Baldetorp, S. Kytola, M. Tanner, and J. Isola Chromosomal rearrangements and oncogene amplification precede aneuploidization in the genetic evolution of breast cancer Cancer Res. 61 2001 1214 1219
5. M.A. Matzke, M.F. Mette, T. Kanno, and A.J. Matzke Does the intrinsic instability of aneuploid genomes have a causal role in cancer? Trends Genet. 19 2003 253 256
6. K. Myung, A. Datta, C. Chen, and R.D. Kolodner SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination Nat. Genet. 27 2001 113 116
7. K. Myung, C. Chen, and R.D. Kolodner Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae Nature 411 2001 1073 1076
8. K. Myung, and R.D. Kolodner Suppression of genome instability by redundant S-phase checkpoint pathways in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U.S.A. 99 2002 4500 4507
9. K. Myung, V. Pennaneach, E.S. Kats, and R.D. Kolodner Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability Proc. Natl. Acad. Sci. U.S.A. 100 2003 6640 6645
10. K. Myung, A. Datta, and R.D. Kolodner Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae Cell 104 2001 397 408
11. S. Tanaka, and J.F. Diffley Deregulated G1-cyclin expression induces genomic instability by preventing efficient pre-RC formation Genes Dev. 16 2002 2639 2649
12. A. Lengronne, and E. Schwob The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1) Mol. Cell 9 2002 1067 1078
13. D. Huang, and D. Koshland Chromosome integrity in Saccharomyces cerevisiae: the interplay of DNA replication initiation factors, elongation factors, and origins Genes Dev. 17 2003 1741 1754
14. M.E. Huang, A.G. Rio, A. Nicolas, and R.D. Kolodner A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations Proc. Natl. Acad. Sci. U.S.A. 100 2003 11529 11534
15. S. Smith, J.-Y. Hwang, S. Banerjee, A. Majeed, A. Gupta, and K. Myung Mutator genes for suppression of gross chromosomal rearrangements identified by a genome-wide screening in Saccharoymces cerevisiae Proc. Natl. Acad. Sci. U.S.A. 101 2004 9039 9044
16. K. Savitsky, A. Bar-Shira, S. Gilad, G. Rotman, Y. Ziv, L. Vanagaite, D.A. Tagle, S. Smith, T. Uziel, and S. Sfez A single ataxia telangiectasia gene with a product similar to PI-3 kinase Science 268 1995 1749 1753
17. D.W. Bell, J.M. Varley, T.E. Szydlo, D.H. Kang, D.C. Wahrer, K.E. Shannon, M. Lubratovich, S.J. Verselis, K.J. Isselbacher, J.F. Fraumeni, J.M. Birch, F.P. Li, J.E. Garber, and D.A. Haber Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome Science 286 1999 2528 2531
18. N.A. Ellis, J. Groden, T.Z. Ye, J. Straughen, D.J. Lennon, S. Ciocci, M. Proytcheva, and J. German The Bloom's syndrome gene product is homologous to RecQ helicases Cell 83 1995 655 666
19. J.P. Carney, R.S. Maser, H. Olivares, E.M. Davis, M. Le Beau, J.R. Yates III, L. Hays, W.F. Morgan, and J.H. Petrini The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response Cell 93 1998 477 486
20. S. Kitao, A. Shimamoto, M. Goto, R.W. Miller, W.A. Smithson, N.M. Lindor, and Y. Furuichi Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome Nat. Genet. 22 1999 82 84
21. G.S. Stewart, R.S. Maser, T. Stankovic, D.A. Bressan, M.I. Kaplan, N.G. Jaspers, A. Raams, P.J. Byrd, J.H. Petrini, and A.M. Taylor The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder Cell 99 1999 577 587
22. C.E. Yu, J. Oshima, Y.H. Fu, E.M. Wijsman, F. Hisama, R. Alisch, S. Matthews, J. Nakura, T. Miki, S. Ouais, G.M. Martin, J. Mulligan, and G.D. Schellenberg Positional cloning of the Werner's syndrome gene Science 272 1996 258 262
23. R. Varon, C. Vissinga, M. Platzer, K.M. Cerosaletti, K.H. Chrzanowska, K. Saar, G. Beckmann, E. Seemanova, P.R. Cooper, N.J. Nowak, M. Stumm, C.M. Weemaes, R.A. Gatti, R.K. Wilson, M. Digweed, A. Rosenthal, K. Sperling, P. Concannon, and A. Reis Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome Cell 93 1998 467 476
24. H. Zou, and R. Rothstein Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism Cell 90 1997 87 96
25. K. Shirahige, Y. Hori, K. Shiraishi, M. Yamashita, K. Takahashi, C. Obuse, T. Tsurimoto, and H. Yoshikawa Regulation of DNA-replication origins during cell-cycle progression Nature 395 1998 618 621
26. C. Santocanale, and J.F. Diffley A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication Nature 395 1998 615 618
27. M. Lopes, C. Cotta-Ramusino, A. Pellicioli, G. Liberi, P. Plevani, M. Muzi-Falconi, C.S. Newlon, and M. Foiani The DNA replication checkpoint response stabilizes stalled replication forks Nature 412 2001 557 561
28. K. Watanabe, J. Morishita, K. Umezu, K. Shirahige, and H. Maki Involvement of RAD9-dependent damage checkpoint control in arrest of cell cycle, induction of cell death, and chromosome instability caused by defects in origin recognition complex in Saccharomyces cerevisiae Eukaryot. Cell 1 2002 200 212
29. E.H. Blackburn, S. Chan, J. Chang, T.B. Fulton, A. Krauskopf, M. McEachern, J. Prescott, J. Roy, C. Smith, and H. Wang Molecular manifestations and molecular determinants of telomere capping Cold Spring Harb. Symp. Quant. Biol. 65 2000 253 263
30. S. Banerjee, K. Myung, Increased genome instability and telomere length in the elg1-deficient S. cerevisiae mutant are regulated by S-phase checkpoints, Eukaryot. Cell 3 (2004) 1557-1566.
31. S.W. Chan, and E.H. Blackburn Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining Mol. Cell 11 2003 1379 1387
32. V. Pennaneach, and R.D. Kolodner Recombination and the Tel1 and Mec1 checkpoints differentially effect genome rearrangements driven by telomere dysfunction in yeast Nat. Genet. 36 2004 612 617
33. C. Chen, and R.D. Kolodner Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants Nat. Genet. 23 1999 81 85
34. P. Sung, K.M. Trujillo, and S. Van Komen Recombination factors of Saccharomyces cerevisiae Mutat. Res. 451 2000 257 275
35. L.S. Symington Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair Microbiol. Mol. Biol. Rev. 66 2002 630 670
36. E. Alani, R. Padmore, and N. Kleckner Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination Cell 61 1990 419 436
37. E.L. Ivanov, V.G. Korolev, and F. Fabre XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination Genetics 132 1992 651 664
38. J.K. Moore, and J.E. Haber Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae Mol. Cell. Biol. 16 1996 2164 2173
39. S.J. Boulton, and S.P. Jackson Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing EMBO J. 17 1998 1819 1828
40. S.E. Lee, J.K. Moore, A. Holmes, K. Umezu, R.D. Kolodner, and J.E. Haber Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage Cell 94 1998 399 409
41. M. Gellert, J.E. Hesse, K. Hiom, M. Melek, M. Modesti, T.T. Paull, D.A. Ramsden, and D.C. van Gent V(D)J recombination: links to transposition and double-strand break repair Cold Spring Harb. Symp. Quant. Biol. 64 1999 161 167
42. J.E. Haber The many interfaces of Mre11 Cell 95 1998 583 586
43. D.A. Bressan, H.A. Olivares, B.E. Nelms, and J.H. Petrini Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11 Genetics 150 1998 591 600
44. L. Chen, K. Trujillo, W. Ramos, P. Sung, and A.E. Tomkinson Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes Mol. Cell 8 2001 1105 1115
45. D. D'Amours, and S.P. Jackson The yeast Xrs2 complex functions in S phase checkpoint regulation Genes Dev. 15 2001 2238 2249
46. D. D'Amours, and S.P. Jackson The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling Nat. Rev. Mol. Cell. Biol. 3 2002 317 327
47. K.S. Lobachev, D.A. Gordenin, and M.A. Resnick The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements Cell 108 2002 183 193
48. S. Gonzalez-Barrera, F. Cortes-Ledesma, R.E. Wellinger, and A. Aguilera Equal sister chromatid exchange is a major mechanism of double-strand break repair in yeast Mol. Cell 11 2003 1661 1671
49. M. van den Bosch, R.T. Bree, and N.F. Lowndes The MRN complex: coordinating and mediating the response to broken chromosomes EMBO Rep. 4 2003 844 849
50. J.H. Lee, and T.T. Paull Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex Science 304 2004 93 96
51. R.S. Maser, K.J. Monsen, B.E. Nelms, and J.H. Petrini hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks Mol. Cell. Biol. 17 1997 6087 6096
52. T.T. Paull, and M. Gellert The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks Mol. Cell 1 1998 969 979
53. K.M. Trujillo, S.S. Yuan, E.Y. Lee, and P. Sung Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95 J. Biol. Chem. 273 1998 21447 21450
54. M. Furuse, Y. Nagase, H. Tsubouchi, K. Murakami-Murofushi, T. Shibata, and K. Ohta Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination EMBO J. 17 1998 6412 6425
55. B. Llorente, and L.S. Symington The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks Mol. Cell. Biol. 24 2004 9682 9694
56. S. Moreau, J.R. Ferguson, and L.S. Symington The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance Mol. Cell. Biol. 19 1999 556 566
57. H. Tsubouchi, and H. Ogawa Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae Mol. Biol. Cell 11 2000 2221 2233
58. S. Moreau, E.A. Morgan, and L.S. Symington Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism Genetics 159 2001 1423 1433
59. 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 160 2002 49 62
60. J.C. Connelly, and D.R. Leach Tethering on the brink: the evolutionarily conserved Mre11-Rad50 complex Trends Biochem. Sci. 27 2002 410 418
61. M. de Jager, and R. Kanaar Genome instability and Rad50(S): subtle yet severe Genes Dev. 16 2002 2173 2178
62. W.E. Raymond, and N. Kleckner RAD50 protein of S. cerevisiae exhibits ATP-dependent DNA binding Nucl. Acids Res. 21 1993 3851 3856
63. M. Chamankhah, T. Fontanie, and W. Xiao The Saccharomyces cerevisiae mre11(ts) allele confers a separation of DNA repair and telomere maintenance functions Genetics 155 2000 569 576
64. S.E. Lee, D.A. Bressan, J.H. Petrini, and J.E. Haber Complementation between N-terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance DNA Repair (Amst) 1 2002 27 40
65. G. Moncalian, B. Lengsfeld, V. Bhaskara, K.P. Hopfner, A. Karcher, E. Alden, J.A. Tainer, and T.T. Paull The Rad50 signature motif: Essential to ATP binding and biological function J. Mol. Biol. 335 2004 937 951
66. H. Tsubouchi, and H. Ogawa A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis Mol. Cell. Biol. 18 1998 260 268
67. R.S. Sikorski, and P. Hieter A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae Genetics 122 1989 19 27
68. D.E. Lea, and C.A. Coulson The distribution of the numbers of mutants in bacterial populations J. Genet. 49 1948 264 285
69. 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. 278 2003 45171 45181
70. T. Usui, T. Ohta, H. Oshiumi, J. Tomizawa, H. Ogawa, and T. Ogawa Complex formation and functional versatility of Mre11 of budding yeast in recombination Cell 95 1998 705 716
71. J. Zhou, E.K. Monson, S. Teng, V.P. Schulz, and V.A. Zakian Pif1p helicase, a catalytic inhibitor of telomerase in yeast Science 289 2000 771 774
72. P. Fiorentini, K.N. Huang, D.X. Tishkoff, R.D. Kolodner, and L.S. Symington Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro Mol. Cell. Biol. 17 1997 2764 2773
73. R.D. Kolodner, and G.T. Marsischky Eukaryotic DNA mismatch repair Curr. Opin. Genet Dev. 9 1999 89 96
74. L.S. Symington, L.E. Kang, and S. Moreau Alteration of gene conversion tract length and associated crossing over during plasmid gap repair in nuclease-deficient strains of Saccharomyces cerevisiae Nucl. Acids Res. 28 2000 4649 4656
75. T.T. Paull, and M. Gellert A mechanistic basis for Mre11-directed DNA joining at microhomologies Proc. Natl. Acad. Sci. U.S.A. 97 2000 6409 6414
76. J. Guirouilh-Barbat, S. Huck, P. Bertrand, L. Pirzio, C. Desmaze, L. Sabatier, and B.S. Lopez Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells Mol. Cell 14 2004 611 623
77. X. Yu, and A. Gabriel Reciprocal translocations in Saccharomyces cerevisiae formed by nonhomologous end joining Genetics 166 2004 741 751