A novel recombination pathway initiated by the Mre11/Rad50/Nbs1 complex eliminates palindromes during meiosis in Schizosaccharomyces pombe

Genetics

Volumn 169, Issue 3, 2005, Pages 1261-1274

  Farah, Joseph A ^a   Cromie, Gareth ^a   Steiner, Walter W ^a,b   Smith, Gerald R ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b NIAGARA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MRE11 PROTEIN; NIBRIN; NUCLEASE; NUCLEIC ACID BINDING PROTEIN; PALINDROMIC DNA; PROTEIN MUS18; PROTEIN RAD16; PROTEIN RAD32; PROTEIN REC12; RAD50 PROTEIN; SPO11 PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; ENZYME ACTIVITY; EUKARYOTE; GENE TRANSLOCATION; GENETIC CONSERVATION; HOMOLOGOUS RECOMBINATION; IN VIVO STUDY; MEIOSIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; SCHIZOSACCHAROMYCES POMBE;

BASE SEQUENCE; CHROMOSOMAL PROTEINS, NON-HISTONE; CONSERVED SEQUENCE; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; GENETIC MARKERS; MEIOSIS; MODELS, GENETIC; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 17444366106     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: 10.1534/genetics.104.037515     Document Type: Article

References (63)

1. ADAIR, G. M., R. L. ROLIG, D. MOORE-FAVER, M. ZABELSHANSKY, J. H. WILSON et al., 2000 Role of ERCC1 in removal of long non-homologous tails during targeted homologous recombination. EMBO J. 19: 5552-5561.
2. AKGUN, E., J. ZAHN, S. BAUMES, G. BROWN, F. LIANG et al., 1997 Palindrome resolution and recombination in the mammalian germ line. Mol. Cell. Biol. 17: 5559-5570.
3. S/S mice. Genes Dev. 16: 2237-2251.
4. BODDY, M. N., A. LOPEZ-GIRONA, P. SHANAHAN, H. INTERTHAL, W. D. HEYER et al., 2000 Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol. Cell. Biol. 20: 8758-8766.
5. BODDY, M. N., P.-H. L. GAILLARD, W. H. MCDONALD, P. SHANAHAN, J. R. YATES et al., 2001 Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107: 537-548.
6. CAO, L., E. ALANI and N. KLECKNER, 1990 A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089-1101.
7. CARR, A. M., H. SCHMIDT, S. KIRCHHOFF, W. J. MURIEL, K. S. SHELDRICK et al., 1994 The rad16 gene of Schizosaccharomyces pombe: a homolog of the RAD1 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 2029-2040.
8. CERVANTES, M. D., J. A. FARAH and G. R. SMITH, 2000 Meiotic DNA breaks associated with recombination in S. pombe. Mol. Cell 5: 883-888.
9. CHAHWAN, C., T. M. NAKAMURA, S. SIVAKUMAR, P. RUSSELL and N. RHIND, 2003 The fission yeast Rad32 (Mre11)-Rad50-Nbs1 complex is required for the S-phase DNA damage checkpoint. Mol. Cell. Biol. 23: 6564-6573.
10. COLLINS, I., and C. S. NEWLON, 1994 Meiosis-specific formation of joint DNA molecules containing sequences from homologous chromosomes. Cell 76: 65-75.
11. COSTANZO, V., K. ROBERTSON, M. BIBIKOVA, E. KIM, D. GRIECO et al., 2001 Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell 8: 137-147.
12. CROMIE, G. A., C. RUBIO, R. W. HYPPA and G. R. SMITH, 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.
13. CUMMINS, J. E., and J. M. MITCHISON, 1967 Adenine uptake and pool formation in the fission yeast Schizosaccharomyces pombe. Biochim. Biophys. Acta 136: 108-120.
14. CUNNINGHAM, L. A., A. G. COTE, C. CAM-OZDEMIR and S. M. LEWIS, 2003 Rapid, stabilizing palindrome rearrangements in somatic cells by the center-break mechanism. Mol. Cell. Biol. 23: 8740-8750.
15. D'AMOURS, D., and S. P. JACKSON, 2001 The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15: 2238-2249.
16. DAVIS, L., and G. R. SMITH, 2003 Nonrandom homolog segregation at meiosis I in Schizosaccharomyces pombe mutants lacking recombination. Genetics 163: 857-874.
17. DEVEAUX, L. C., N. A. HOAGLAND and G. R. SMITH, 1992 Seventeen complementation groups of mutations decreasing meiotic recombination in Schizosaccharomyces pombe. Genetics 130: 251-262.
18. EDELMANN, L., E. SPITERI, K. KOREN, V. PULIJAAL, M. G. BIALER et al., 2001 AT-rich palindromes mediate the constitutional t(11;22) translocation. Am. J. Hum. Genet. 68: 1-13.
19. FARAH, J. A., E. HARTSUIKER, K. MIZUNO, K. OHTA and G. R. SMITH, 2002 A 160-bp palindrome is a Rad50asterisk inside a circle signRad32-dependent mitotic recombination hotspot in Schizosaccharomyces pombe. Genetics 161: 461-468.
20. FISHMAN-LOBELL, J., and J. E. HABER, 1992 Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258: 480-484.
21. FOX, M. F., T. YAMADA, K. OHTA and G. R. SMITH, 2000 A family of CRE-related DNA sequences with meiotic recombination hotspot activity in Schizosaccharomyces pombe. Genetics 156: 59-68.
22. GRIMM, C., J. BÄHLER and J. KOHLI, 1994 M26 recombinational hotspot and physical conversion tract analysis in the ade6 gene of Schizosaccharomyces pombe. Genetics 135: 41-51.
23. GUTZ, H., H. HESLOT, U. LEUPOLD and N. LOPRIENO, 1974 Schizosaccharomyces pombe, pp. 395-446 in Handbook of Genetics, edited by R. C. KING. Plenum Press, New York.
24. HABER, J. E., 1998 The many interfaces of Mrell. Cell 95: 583-586.
25. HOCHSTENBACH, F., F. M. KLIS, H. VAN DEN ENDE, E. VAN DONSELAAR, P. J. PETERS et al., 1998 Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc. Natl. Acad. Sci. USA 95: 9161-9166.
26. KURAHASHI, H., and B. S. EMANUEL, 2001a Long AT-rich palindromes and the constitutional t(11;22) breakpoint. Hum. Mol. Genet. 10: 2605-2617.
27. KURAHASHI, H., and B. S. EMANUEL, 2001b Unexpectedly high rate of de novo constitutional t(11;22) translocations in sperm from normal males. Nat. Genet. 29: 139-140.
28. KURAHASHI, H., T. SHAIKH, M. TAKATA, T. TODA and B. S. EMANUEL, 2003 The constitutional t(17;22): another translocation mediated by palindromic AT-rich repeats. Am. J. Hum. Genet. 72: 733-738.
29. LEACH, D. R., 1994 Long DNA palindromes, cruciform structures, genetic instability and secondary structure repair. BioEssays 16: 893-900.
30. LEE, S. E., R. A. MITCHELL, A. CHENG and E. A. HENDRICKSON, 1997 Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell. Biol. 17: 1425-1433.
31. Li, Y. F., and G. R. SMITH, 1997 The Schizosaccharomyces pombe rec16 gene product regulates multiple meiotic events. Genetics 146: 57-67.
32. LIN, Y., and G. R. SMITH, 1994 Transient meiosis-induced expression of the rec6 and rec12 genes of Schizosaccharomyces pombe. Genetics 136: 769-779.
33. LOBACHEV, K. S., B. M. SHOR, H. T. TRAN, W. TAYLOR, J. D. KEEN et al., 1998 Factors affecting inverted repeat stimulation of recombination and deletion in Saccharomyces cerevisiae. Genetics 148: 1507-1524.
34. LOBACHEV, K. S., D. A. GORDENIN and M. A. RESNICK, 2002 The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108: 183-193.
35. LOBACHEV, K. S., J. E. STENGER, O. G. KOZYREVA, J. JURKA, D. A. GORDENIN et al., 2000 Inverted Alu repeats unstable in yeast are excluded from the human genome. EMBO J. 19: 3822-3830.
36. LOU, G., M. S. YAO, C. F. BENDER, M. MILLS, A. R. BLADL et al. 1999 Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 96: 7376-7381.
37. MASER, R. S., O. K. MIRZOEVA, J. WELLS, H. OLIVARES, B. R. WILLIAMS et al., 2001 Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol. 21: 6006-6016.
38. MATA, J., R. LYNE, G. BURNS and J. BAHLER, 2002 The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 32: 143-147.
39. MOREAU, S., J. R. FERGUSON and L. S. SYMINGTON, 1999 The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19: 556-566.
40. MORENO, S., A. J. S. KLAR and P. NURSE, 1991 Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194: 795-823.
41. NAG, D. K., and A. KURST, 1997 A 140-bp-long palindromic sequence induces double-strand breaks during meiosis in the yeast Saccharomyces cerevisiae. Genetics 146: 835-847.
42. NASAR, F., C. JANKOWSKI and D. K. NAG, 2000 Long palindromic sequences induce double-strand breaks during meiosis in yeast. Mol. Cell. Biol. 20: 3449-3458.
43. OSMAN, F., J. DIXON, C. L. DOE and M. C. WHITBY, 2003 Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell 12: 761-774.
44. PAULL, T. T., and M. GELLERT, 1999 Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13: 1276-1288.
45. PONTICELLI, A. S., and G. R. SMITH, 1989 Meiotic recombination-deficient mutants of Schizosaccharomyces pombe. Genetics 123: 45-54.
46. PONTICELLI, A. S., and G. R. SMITH, 1992 Context dependence of a eukaryotic recombination hotspot. Proc. Natl. Acad. Sci. USA 89: 227-231.
47. PRENTICE, H. L., 1992 High efficiency transformation of Schiwsaccharomyces pombe by electroporation. Nucleic Acids Res. 20: 621.
48. RAY, B. L., C. I. WHITE and J. E. HABER, 1991 Heteroduplex formation and mismatch repair of the "stuck" mutation during mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 5372-5380.
49. RICHARDSON, C., and M. JASIN, 2000 Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405: 697-700.
50. ROEDER, G. S., 1997 Meiotic chromosomes: it takes two to tango. Genes Dev. 11: 2600-2621.
51. SCHWACHA, A., and N. KLECKNER, 1994 Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.
52. SMITH, G. R., M. N. BODDY, P. SHANAHAN and P. RUSSELL, 2003 Fission yeast Mus81asterisk inside a circle signEme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165: 2289-2293.
53. STEINER, W. W., R. W. SCHRECKHISE and G. R. SMITH, 2002 Meiotic DNA breaks at the S. pombe recombination hotspot M26. Mol. Cell 9: 847-855.
54. 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.
55. SZANKASI, P., W. D. HEYER, P. SCHUCHERT and J. KOHLI, 1988 DNA sequence analysis of the ade6 gene of Schizosaccharomyces pombe: wild-type and mutant alleles including the recombination hotspot allele ade6-M26. J. Mol. Biol. 204: 917-925.
56. TRUJILLO, K. M., and P. SUNG, 2001 DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50astrisk inside a circle signMre11 complex. J. Biol. Chem. 276: 35458-35464.
57. TRUJILLO, K. M., D. H. ROH, L. CHEN, S. VAN KOMEN, A. TOMKINSON et al., 2003 Yeast Xrs2 binds DNA and helps target Rad50 and Mre11 to DNA ends. J. Biol. Chem. 278: 48957-48964.
58. VIRGIN, J. B., J. METZGER and G. R. SMITH, 1995 Active and inactive transplacement of the M26 recombination hotspot in Schizosaccharomyces pombe. Genetics 141: 33-48.
59. WALDMAN, A. S., H. TRAN, E. C. GOLDSMITH and M. A. RESNICK, 1999 Long inverted repeats are an at-risk motif for recombination in mammalian cells. Genetics 153: 1873-1883.
60. YOUNG, J. A., R. W. SCHRECKHISE, W. W. STEINER and G. R. SMITH, 2002 Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol. Cell 9: 253-263.
61. YOUNG, J. A., R. W. HYPPA and G. R. SMITH, 2004 Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167: 593-605.
62. ZHOU, Z. H., E. AKGUN and M. JASIN, 2001 Repeat expansion by homologous recombination in the mouse germ line at palindromic sequences. Proc. Natl. Acad. Sci. USA 98: 8326-8333.
63. ZHU, J., S. PETERSEN, L. TESSAROLLO and A. NUSSENZWEIG, 2001 Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11: 105-109.