Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination

EMBO Journal

Volumn 17, Issue 21, 1998, Pages 6412-6425

  Furuse, Munenori ^a,b   Nagase, Yuko ^a,c   Tsubouchi, Hideo ^d   Murakami Murofushi, Kimiko ^c   Shibata, Takehiko ^a,b   Ohta, Kunihiro ^a  

^a INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^b SAITAMA UNIVERSITY   (Japan)

^c OCHANOMIZU UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

DNA binding; Double strand break repair; DSB formation; Mre11; Nuclease

Indexed keywords

DNA BINDING PROTEIN; DOUBLE STRANDED DNA; MANGANESE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMATIN STRUCTURE; DNA REPAIR; DNA STRAND BREAKAGE; GENETIC RECOMBINATION; MEIOSIS; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; YEAST;

BACTERIOPHAGE M13; CHROMATIN; DEOXYRIBONUCLEASES; DNA REPAIR; DNA, CIRCULAR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; FUNGAL PROTEINS; MEIOSIS; METHYL METHANESULFONATE; MITOSIS; MUTATION; PHENOTYPE; PROTEIN CONFORMATION; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE;

SACCHAROMYCES CEREVISIAE;

EID: 0032476658     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.21.6412     Document Type: Article

References (63)

1. Ajimura, M., Leem, S.H. and Ogawa, H. (1993) Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae, Genetics, 133, 51-66
2. Alani, E., Padmore, R. and Kleckner, N. (1990) Analysis of wild-type and rad50 mutations of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell, 61, 419-436.
3. Anderson, D.G. and Kowalczykowski, S.C. (1997) The recombination hot spot chi is a regulatory element that switches the polarity of DNA degradation by the RecBCD enzyme. Genes Dev., 11, 571-581.
4. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A. and Forterre, P. (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature, 386, 414-417.
5. Boulton, S.J. and Jackson, S.P. (1996) Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J., 15, 5093-5103.
6. Boulton, S.J. and Jackson, S.P. (1998) Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J., 17, 1819-1828.
7. Cao, L., Alani, E. and Kleckner, N. (1990) A pathway for generation and processing of double-strand breaks during meiotic recombination in S.cerevisiae. Cell 61, 1089-1101.
8. Carlson, M. and Botstein, D. (1982) Two differentially regulated mRNAs with different 5′ ends encode secreted with intracellular forms of yeast invertase. Cell, 28, 145-154.
9. Carney, J.P., Maser, R.S., Olivares, H., Davis, E.M., Le Beau, M., Yates, J.R. III, Hays, L., Morgan, W.F. and Petrini, J.H. (1998) The hMre11/ hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell, 93, 477-486.
10. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl Acad. Sci. USA, 81, 1991-1995.
11. Cohen, P.T., Collins, J.F., Coulson, A.F., Berndt, N. and da Cruz e Silva, O.B. (1988) Segments of bacteriophage lambda (orf 221) and phi 80 are homologous to genes coding for mammalian protein phosphatases. Gene, 69, 131-134.
12. Connelly, J.C. and Leach, D.R. (1996) The sbcC and sbcD genes of Eacherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes Cells, 1, 285-291.
13. Cool, M. and Malone, R.E. (1992) Molecular and genetic analysis of the yeast early meiotic recombination genes REC102 and REC107/MER2. Mol. Cell. Biol, 12, 1248-1256.
14. Dolganov, G.M., Maser, R.S., Novikov, A., Tosto, L., Chong, S., Bressan, D.A. and Petrini, J.H. (1996) Human Rad50 is physically associated with human Mre11: identification of a conserved multiprotein complex implicated in recombinational DNA repair. Mol. Cell. Biol., 16, 4832-4841.
15. Engebrecht, J.A., Voelkel-Meiman, K. and Roeder, G.S. (1991) Meiosis-specific RNA splicing in yeast. Cell, 66, 1257-1268.
16. Fan, Q.Q. and Petes, T.D. (1996) Relationship between nuclease-hypersensitive sites and meiotic recombination hot spot activity at the HIS4 locus of Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 2037-2043.
17. Farnet, C., Padmore, R., Cao, L., Raymond, W., Alani, E. and Kleckner, N. (1988) The RAD50 gene of S.cerevisiae. In Frieberg, E. and Handbalt, P. (eds), Mechanisms and Consequences of DNA Damage Processing. (UCLA Symposia on Molecular and Cellular Biology) vol. 83, Alan R.Liss, Inc., New York pp. 1-15.
18. Game, J.C. and Motimer, R.K. (1974) A genetic study of X-ray sensitive mutants in yeast. Mutat. Res., 24, 281-292.
19. Griffith, J.P. et al. (1995) X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell, 82, 507-22.
20. Guerini, D. and Klee, C.B. (1989) Cloning of human calcineurin A: evidence for two isozymes and identification of a polyproline structural domain. Proc. Natl Acad. Sci. USA, 86, 9183-9187.
21. Haber, J.E. (1995) In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases. Bioessays, 17, 609-620.
22. Hashimoto-Gotoh, T., Mizuno, T., Ogasahara, Y. and Nakagawa, M. (1995) An oligodeoxyribonucleotide-directed dual amber method for site-directed mutagenesis. Gene, 152, 271-275.
23. Ivanov, E.L., Korolev, V.G. and Fabre, F. (1992) XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics, 132, 651-664.
24. Johzuka, K. and Ogawa, H. (1995) Interaction of Mrell and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics, 139, 1521-1532.
25. Keeney, S. and Kleckner, N. (1996) Communication between homologous chromosomes: genetic alterations at a nuclease-hypersensitive site can alter mitotic chromatin structure at that site both in cis and in trans. Genes Cells, 1, 475-490.
26. Keeney, S., Giroux, C.N. and Kleckner, N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spoil, a member of a widely conserved protein family. Cell, 88, 375-384.
27. Kironmai, K.M. and Muniyappa, K. (1997) Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells, 2, 443-455.
28. Kissinger, C.R. et al. (1995) Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature, 378, 641-644.
29. - mutant of yeast. Genetics, 100, 387-412.
30. Kon, N., Krawchuk, M.D., Warren, B.G., Smith, G.R. and Wahls, W.P. (1997) Transcription factor Mts1/Mts2 (Atf1/Pcr1, Gad7/Pcr1) activates the M26 meiotic recombination hotspot in Schizosaccharomyces pombe. Proc. Natl Acad. Sci. USA, 94, 13765-13770.
31. Kramer, K.M., Brock, J.A., Bloom, J.C., Moore, J.K. and Haber, J.E. (1994) Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol., 14, 1293-1301.
32. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
33. Leach, D.R., Lloyd, R.G. and Coulson, A.F. (1992) The SbcCD protein of Escherichia coli is related to two putative nucleases in the UvrA superfamily of nucleotide-binding proteins. Genetica, 87, 95-100.
34. Lee, S.E., Moore, J.K., Holmes, A., Umezu, K., Kolodner, R.D. and Haber, J.E. (1998) Saccharomyces Ku70, Mre11/Rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell, 94, 399-409.
35. Loidl, J., Klein, F. and Scherthan, H. (1994) Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol., 125, 1191-1200.
36. Malone, R.E., Bullard, S., Hermiston, M., Rieger, R., Cool, M. and Galbraith, A. (1991) Isolation of mutants defective in early steps of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics, 128, 79-88.
37. Matsuura, S. et al. (1998) Positional cloning of the gene for Nijmegen breakage syndrome. Nature Genet., 19, 179-181.
38. Mezard, C. and Nicolas, A. (1994) Homologous, homeologous and illegitimate repair of double-strand breaks during transformation of a wild-type strain and a rad52 mutant strain of Saccharomyces cerevisiae. Mol. Cell. Biol., 14, 1278-1292.
39. Milne, G.T., Jin, S., Shannon, K.B. and Weaver, D.T. (1996) Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell Biol., 16, 4189-4198.
40. Moore, J.K. and Haber, J.E. (1996) Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol., 16, 2164-2173.
41. Nairz, K. and Klein, F. (1997) mre11S-a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev., 11, 2272-2290.
42. Nakagawa, T. and Ogawa, H. (1997) Involvement of the MRE2 gene of yeast in formation of meiosis-specific double-strand breaks and crossover recombination through RNA splicing. Genes Cells, 2, 65-79.
43. Nugent, C.I., Bosco, G., Ross, L.O., Evans, S.K., Salinger, A.R, Moore, J.K., Haber, J.E. and Lundblad, V. (1998) Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol, 8, 657-660.
44. Ogawa, H., Johzuka, K., Nakagawa, T., Leem, S.H. and Hagihara, A.H. (1995) Functions of the yeast meiotic recombination genes, MRE11 and MRE2. Adv. Biophys., 31, 67-76.
45. Ohta, K., Shibata, T. and Nicolas, A. (1994) Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J., 13, 5754-5763.
46. Ohta, K., Nicolas, A., Furuse, M., Nabetani, A., Ogawa, H. and Shibata, T. (1998) Mutations in the MRE11, RAD50, XRS2 and MRE2 genes alter chromatin configuration at meiotic DNA double-stranded break sites in premeiotic and meiotic cells. Proc. Natl Acad. Sci. USA, 95, 646-651.
47. Paull, T.T. and Gellert, M. (1998) The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell, 1, 969-979.
48. Petrini, J.H., Walsh, M.E., DiMare, C., Chen, X.N., Korenberg, J.R. and Weaver, D.T. (1995) Isolation and characterization of the human MRE11 homologue. Genomics, 29, 80-86.
49. Rockmill, B., Engebrecht, J.A., Scherthan, H., Loidl, J. and Roeder, G.S. (1995) The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics, 141, 49-59.
50. Sharples, G.J. and Leach, D.R. (1995) Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol., 17, 1215-1217.
51. Sherman, F., Fink, G.R. and Laurence, C. (1979) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
52. Shinohara, A. and Ogawa, T. (1995) Homologous recombination and the roles of double-strand breaks. Trends Biochem. Sci., 20, 387-391.
53. Tavassoli, M., Shayeghi, M., Nasim, A. and Watts, F.Z. (1995) Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double strand breaks and recombination. Nucleic Acids Res., 23, 383-388.
54. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
55. Trujillo, K.M., Yuan, S.S.F., Lee, E.Y.H.P. and Sung, P. (1998) Nuclease activities in a complex of human recombination and DNA repair factors rad50, mre11 and p95. J. Biol Chem., 273, 21447-21450.
56. Tsubouchi, H. and Ogawa, H. (1998) A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol., 18, 260-268.
57. Tsukamoto, Y. and Ikeda, H. (1998) Double-strand break repair mediated by DNA end-joining. Genes Cells, 3, 135-144.
58. Tsukamoto, Y., Kato, J. and Ikeda, H. (1996) Hdf1, a yeast Ku-protein. homologue, is involved in illegitimate recombination, but not in homologous recombination. Nucleic Acids Res., 24, 2067-2072.
59. Tsukamoto, Y., Kato, J. and Ikeda, H. (1997) Budding yeast Rad50, Mre11, Xrs2 and Hdf1, but not Rad52, are involved in the formation of deletions on a dicentric plasmid. Mol. Gen. Genet., 255, 543-547.
60. Varon, R. et al. (1998) Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell, 93, 467-476.
61. Weiner, B.M. and Kleckner, N. (1994) Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell, 77, 977-991.
62. Wu, T.-C. and Lichten, M. (1994) Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science, 263, 515-518.
63. Zhuo, S., Clemens, J.C., Stone, R.L. and Dixon, J.E. (1994) Mutational analysis of a Ser/Thr phosphatase: identification of residues important in phosphoesterase substrate binding and catalysis. J. Biol. Chem., 269, 26234-26238.