Ctp1 and Exonuclease 1, alternative nucleases regulated by the MRN complex, are required for efficient meiotic recombination

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 23, 2009, Pages 9356-9361

  Farah, Joseph A ^a   Cromie, Gareth A ^a   Smith, Gerald R ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

DNA resection; DSB repair; S. pombe; Sae2

Indexed keywords

CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; CTP1 PROTEIN; EXONUCLEASE; EXONUCLEASE 1; NIBRIN; NUCLEASE; NUCLEASE SAE2; NUCLEIC ACID BINDING PROTEIN; RAD32 PROTEIN; RAD50 PROTEIN; SPO11 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; COMPLEX FORMATION; COVALENT BOND; CROSSING OVER; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; EXCISION REPAIR; GENE CONVERSION; GENETIC RECOMBINATION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; WILD TYPE; YEAST;

CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; MEIOSIS; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 67249153681     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902793106     Document Type: Article

References (39)

1. Haber JE (2008) in Recombination and Meiosis: Models, Means, and Evolution, eds. Egel R, Lankenau D-H (Springer, Berlin), pp 1-64.
2. Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52:1-53. (Pubitemid 33804625)
3. Neale MJ, Pan J, Keeney S (2005) Endonucleolytic processing of covalent protein-linked DNA double-strand breaks. Nature 436:1053-1057. (Pubitemid 41191692)
4. Wilson S, Tavassoli M, Watts FZ (1998) Schizosaccharomyces pombe rad32 protein: a phosphoprotein with an essential phosphoesterase motif required for repair of DNA double strand breaks. Nucleic Acids Res 26:5261-5269. (Pubitemid 28542723)
5. Chahwan C, Nakamura TM, Sivakumar S, Russell P, Rhind N (2003) The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol Cell Biol 23:6564-6573. (Pubitemid 37075767)
6. Limbo O, et al. (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol Cell 28:134-146. (Pubitemid 47531975)
7. Lengsfeld BM, Rattray AJ, Bhaskara V, Ghirlando R, Paull TT (2007) Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol Cell 28:638-651. (Pubitemid 350137798)
8. Szankasi P, Smith GR (1992) A DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J Biol Chem 267:3014-3023.
9. Carr AM, et al. (1994) The rad16 gene of Schizosaccharomyces pombe: a homolog of the RAD1 gene of Saccharomyces cerevisiae. Mol Cell Biol 14:2029-2040. (Pubitemid 24074600)
10. Cromie GA, et al. (2006) Single Holliday junctions are intermediates of meiotic recombination. Cell 127:1167-1178. (Pubitemid 44894523)
11. Smith GR, Boddy MN, Shanahan P, Russell P (2003) Fission yeast Mus81•Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165:2289-2293. (Pubitemid 38040308)
12. Osman F, Dixon J, Doe CL, Whitby MC (2003) Generating crossovers by resolution of nicked Holliday junctions: A role for Mus81-Eme1 in meiosis. Mol Cell 12:761-774. (Pubitemid 37222495)
13. Boddy MN, et al. (2001) Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537-548. (Pubitemid 33152788)
14. Colleaux L, d'Auriol L, Galibert F, Dujon B (1988) Recognition and cleavage site of the intron-encoded omega transposase. Proc Natl Acad Sci USA 85:6022-6026. (Pubitemid 18209064)
15. Davis L, Smith GR (2003) Non-random homolog segregation at meiosis I in Schizosaccharomyces pombe mutants lacking recombination. Genetics 163:857-874. (Pubitemid 36417932)
16. Ponticelli AS, Smith GR (1989) Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics 123:45-54. (Pubitemid 19233889)
17. Cromie GA, Rubio CA, Hyppa RW, Smith GR (2005) A natural meiotic DNA break site in Schizosaccharomyces pombe is a hotspot of gene conversion, highly associated with crossing over. Genetics 169:595-605. (Pubitemid 40404297)
18. Mata J, Lyne R, Burns G, Bahler J (2002) The transcription program of meiosis and sporulation in fission yeast. Nat Genet 32:143-147. (Pubitemid 34977209)
19. Lin Y, Smith GR (1994) Transient meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe. Genetics 136:769-779. (Pubitemid 24085629)
20. Young JA, Schreckhise RW, Steiner WW, Smith GR (2002) Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol Cell 9:253-263. (Pubitemid 34195552)
21. Cromie GA, Smith GR (2008) in Recombination and Meiosis: Models, Means, and Evolution, eds. Egel R, Lankenau D-H (Springer, Berlin), pp 195-230.
22. Cromie GA, et al. (2007) A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genet 3:e141. (Pubitemid 47358086)
23. + and rad50S strains of fission yeast. PLoS Genet 4:e1000267.
24. Young JA, Hyppa RW, Smith GR (2004) Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167:593-605. (Pubitemid 38931850)
25. Trujillo KM, Sung P (2001) DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50*Mre11 complex. J Biol Chem 276:35458-35464. (Pubitemid 37384342)
26. Szankasi P, Smith GR (1995) A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267:1166-1169.
27. Farah JA, Cromie G, Steiner WW, Smith GR (2005) A novel recombination pathway initiated by the Mre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe. Genetics 169:1261-1274. (Pubitemid 40547441)
28. Grossenbacher-Grunder AM, Thuriaux P (1981) Spontaneous and UV-induced recombination in radiation-sensitive mutants of Schizosaccharomyces pombe. Mut Res 81:37-48. (Pubitemid 11167560)
29. Gutz H (1971) Site specific induction of gene conversion in Schizosaccharomyces pombe. Genetics 69:317-337.
30. Grimm C, Bahler J, Kohli J (1994) M26 recombinational hotspot and physical conversion tract analysis in the ade6 gene of Schizosaccharomyces pombe. Genetics 135:41-51. (Pubitemid 24016672)
31. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981-994.
32. Sartori AA, et al. (2007) Human CtIP promotes DNA end resection. Nature 450:509-514. (Pubitemid 350190253)
33. 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.
34. Rudolph C, Fleck O, Kohli J (1998) Schizosaccharomyces pombe exo1 is involved in the same mismatch repair pathway as msh2 and pms1. Curr Genet 34:343-350. (Pubitemid 29004638)
35. Kirkpatrick DT, Ferguson JR, Petes TD, Symington LS (2000) Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics 156:1549-1557. (Pubitemid 32001224)
36. Tsubouchi H, Ogawa H (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell 11:2221-2233. (Pubitemid 30489910)
37. Mimitou EP, Symington LS (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770-774.
38. Tomita K, et al. (2003) Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol Cell Biol 23:5186-5197. (Pubitemid 36950874)
39. Whitehouse HLK (1982) Genetic Recombination (John Wiley & Sons, New York).