Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe

Molecular and Cellular Biology

Volumn 30, Issue 7, 2010, Pages 1570-1581

  Latypov, Vitaly ^a,c   Rothenberg, Maja ^a   Lorenz, Alexander ^b,d   Octobre, Guillaume ^a,e   Csutak, Ortansa ^a,f   Lehmann, Elisabeth ^a   Loidl, Josef ^b   Kohli, Jürg ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^f UNIVERSITY OF BUCHAREST   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PROTEIN HOP1; UNCLASSIFIED DRUG;

ARTICLE; CELL VIABILITY; CHROMOSOME PAIRING; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENETIC RECOMBINATION; HOLLIDAY JUNCTION; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SCHIZOSACCHAROMYCES POMBE; SISTER CHROMATID;

CELL CYCLE PROTEINS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; MAP KINASE KINASE 1; MEIOSIS; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SISTER CHROMATID EXCHANGE; SPORES, FUNGAL;

SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE;

EID: 77949363046     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00919-09     Document Type: Article

References (74)

1. Bahler, J., T. Wyler, J. Loidl, and J. Kohli. 1993. Unusual nuclear structures in meiotic prophase of fission yeast: a cytological analysis. J. Cell Biol. 121:241-256.
2. Bailis, J. M., and G. S. Roeder. 1998. Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein. Genes Dev. 12:3551-3563.
3. Bishop, D. K., Y. Nikolski, J. Oshiro, J. Chon, M. Shinohara, and X. Chen. 1999. High copy number suppression of the meiotic arrest caused by a dmc1 mutation: REC114 imposes an early recombination block and RAD54 promotes a DMC1-independent DSB repair pathway. Genes Cells 4:425-444.
4. Bishop, D. K., D. Park, L. Xu, and N. Kleckner. 1992. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69:439-456.
5. Boddy, M. N., P. H. Gaillard, W. H. McDonald, P. Shanahan, J. R. Yates III, and P. Russell. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537-548.
6. Carballo, J. A., A. L. Johnson, S. G. Sedgwick, and R. S. Cha. 2008. Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132:758-770.
7. Catlett, M. G., and S. L. Forsburg. 2003. Schizosaccharomyces pombe Rdh54 (TID1) acts with Rhp54 (RAD54) to repair meiotic double-strand breaks. Mol. Biol. Cell 14:4707-4720.
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. Couteau, F., K. Nabeshima, A. Villeneuve, and M. Zetka. 2004. A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr. Biol. 14: 585-592.
10. Cromie, G., and G. R. Smith. 2007. Meiotic recombination in Schizosaccharomyces pombe: a paradigm for genetic and molecular analysis, p. 196-230. In R. Egel and D.-H. Lankenau (ed.), Recombination and meiosis, vol. 3. Springer, Berlin, Germany.
11. Cromie, G. A., R. W. Hyppa, A. F. Taylor, K. Zakharyevich, N. Hunter, and G. R. Smith. 2006. Single Holliday junctions are intermediates of meiotic recombination. Cell 127:1167-1178.
12. Cromie, G. A., and G. R. Smith. 2007. Branching out: meiotic recombination and its regulation. Trends Cell Biol. 17:448-455.
13. Davis, L., and G. R. Smith. 2001. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. U. S. A. 98:8395-8402.
14. Doll, E. 2005. Ph.D. thesis. University of Berne, Berne, Switzerland.
15. Doll, E., M. Molnar, Y. Hiraoka, and J. Kohli. 2005. Characterization of rec15, an early meiotic recombination gene in Schizosaccharomyces pombe. Curr. Genet 48:323-333.
16. Ehmsen, K. T., and W. D. Heyer. 2008. Biochemistry of meiotic recombination: formation, processing, and resolution of recombination intermediates, p. 91-164. In R. Egel and D.-H. Lankenau (ed.), Recombination and meiosis, vol. 3. Springer, Berlin, Germany.
17. Ellermeier, C., and G. R. Smith. 2005. Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. U. S. A. 102:10952-10957.
18. Fukuda, T., K. Daniel, L. Wojtasz, A. Toth, and C. Hoog. 2009. A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp. Cell Res. 316:158-171.
19. Gregan, J., P. K. Rabitsch, B. Sakem, O. Csutak, V. Latypov, E. Lehmann, J. Kohli, and K. Nasmyth. 2005. Novel genes required for meiotic chromosome segregation are identified by a high-throughput knockout screen in fission yeast. Curr. Biol. 15:1663-1669.
20. Grishchuk, A. L., and J. Kohli. 2003. Five RecA-like proteins of Schizosaccharomyces pombe are involved in meiotic recombination. Genetics 165: 1031-1043.
21. Gutz, H., H. Heslot, U. Leupold, and N. Loprieno. 1974. Schizosaccharomyces pombe, p. 395-446. In R. C. King (ed.), Handbook of genetics, vol. 1. Plenum Press, New York, NY.
22. Haber, J. E. 2007. Evolution of models of homologous recombination, p. 1-64. In R. Egel and D.-H. Lankenau (ed.), Recombination and meiosis, vol. 3. Springer, Berlin, Germany.
23. Hartsuiker, E., K. Mizuno, M. Molnar, J. Kohli, K. Ohta, and A. M. Carr. 2009. Ctp1CtIP and Rad32Mre11 nuclease activity are required for Rec12Spo11 removal, but Rec12Spo11 removal is dispensable for other MRN-dependent meiotic functions. Mol. Cell. Biol. 29:1671-1681.
24. Hartsuiker, E., E. Vaessen, A. M. Carr, and J. Kohli. 2001. Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J. 20:6660-6671.
25. Hiraoka, Y., D. Q. Ding, A. Yamamoto, C. Tsutsumi, and Y. Chikashige. 2000. Characterization of fission yeast meiotic mutants based on live observation of meiotic prophase nuclear movement. Chromosoma 109:103-109.
26. Hollingsworth, N. M., and B. Byers. 1989. HOP1: a yeast meiotic pairing gene. Genetics 121:445-462.
27. Hunter, N., and N. Kleckner. 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106:59-70.
28. Kadyk, L. C., and L. H. Hartwell. 1993. Replication-dependent sister chromatid recombination in rad1 mutants of Saccharomyces cerevisiae. Genetics 133:469-487.
29. Keeney, S., and M. J. Neale. 2006. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34:523-525.
30. Ledesma, F. C., S. F. El Khamisy, M. C. Zuma, K. Osborn, and K. W. Caldecott. 2009. A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature 461:674-678.
31. Leem, S. H., and H. Ogawa. 1992. The MRE4 gene encodes a novel protein kinase homologue required for meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 20:449-457.
32. Limbo, O., C. Chahwan, Y. Yamada, R. A. de Bruin, C. Wittenberg, and P. Russell. 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.
33. Loidl, J., F. Klein, and J. Engebrecht. 1998. Genetic and morphological approaches for the analysis of meiotic chromosomes in yeast. Methods Cell Biol. 53:257-285.
34. Lorenz, A., A. Estreicher, J. Kohli, and J. Loidl. 2006. Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe. Chromosoma 115:330-340.
35. Lorenz, A., J. Fuchs, R. Burger, and J. Loidl. 2003. Chromosome pairing does not contribute to nuclear architecture in vegetative yeast cells. Eukaryot. Cell 2:856-866.
36. Lorenz, A., J. L. Wells, D. W. Pryce, M. Novatchkova, F. Eisenhaber, R. J. McFarlane, and J. Loidl. 2004. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J. Cell Sci. 117:3343-3351.
37. Ludin, K., J. Mata, S. Watt, E. Lehmann, J. Bahler, and J. Kohli. 2008. Sites of strong Rec12/Spo11 binding in the fission yeast genome are associated with meiotic recombination and with centromeres. Chromosoma 117:431-444.
38. Lydall, D., Y. Nikolsky, D. K. Bishop, and T. Weinert. 1996. A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383:840-843.
39. Maloney, D. H., and S. Fogel. 1987. Gene conversion, unequal crossing-over and mispairing at a non-tandem duplication during meiosis of Saccharomyces cerevisiae. Curr. Genet. 12:1-7.
40. Martin-Castellanos, C., M. Blanco, A. E. Rozalen, L. Perez-Hidalgo, A. I. Garcia, F. Conde, J. Mata, C. Ellermeier, L. Davis, P. San-Segundo, G. R. Smith, and S. Moreno. 2005. A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events. Curr. Biol. 15:2056-2062.
41. Martinez-Perez, E., M. Schvarzstein, C. Barroso, J. Lightfoot, A. F. Dernburg, and A. M. Villeneuve. 2008. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 22:2886-2901.
42. 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.
43. Milman, N., E. Higuchi, and G. R. Smith. 2009. Meiotic double-strand break repair requires two nucleases, MRN and Ctp1, to produce a single size-class of Rec12 (Spo11)-oligonucleotides. Mol. Cell. Biol. 29:5998-6005.
44. Molnar, M., E. Doll, A. Yamamoto, Y. Hiraoka, and J. Kohli. 2003. Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing. J. Cell Sci. 116:1719-1731.
45. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823.
46. Munz, P. 1994. An analysis of interference in the fission yeast Schizosaccharomyces pombe. Genetics 137:701-707.
47. Niu, H., X. Li, E. Job, C. Park, D. Moazed, S. P. Gygi, and N. M. Hollingsworth. 2007. Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol. Cell. Biol. 27:5456-5467.
48. Niwa, O., M. Shimanuki, and F. Miki. 2000. Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19:3831-3840.
49. Nurse, P. 1975. Genetic control of cell size at cell division in yeast. Nature 256:547-551.
50. Octobre, G., A. Lorenz, J. Loidl, and J. Kohli. 2008. The Rad52 homologs Rad22 and Rti1 of Schizosaccharomyces pombe are not essential for meiotic interhomolog recombination, but are required for meiotic intrachromosomal recombination and mating-type-related DNA repair. Genetics 178:2399-2412.
51. Osman, F., M. Adriance, and S. McCready. 2000. The genetic control of spontaneous and UV-induced mitotic intrachromosomal recombination in the fission yeast Schizosaccharomyces pombe. Curr. Genet. 38:113-125.
52. Osman, F., J. Dixon, C. L. Doe, and M. C. Whitby. 2003. Generating cross-overs by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell 12:761-774.
53. Page, S. L., and R. S. Hawley. 2003. Chromosome choreography: the meiotic ballet. Science 301:785-789.
54. Page, S. L., and R. S. Hawley. 2004. The genetics and molecular biology of the synaptonemal complex. Annu. Rev. Cell Dev. Biol. 20:525-558.
55. Paques, F., and J. E. Haber. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:349-404.
56. Pecina, A., K. N. Smith, C. Mezard, H. Murakami, K. Ohta, and A. Nicolas. 2002. Targeted stimulation of meiotic recombination. Cell 111:173-184.
57. Perez-Hidalgo, L., S. Moreno, and P. A. San-Segundo. 2003. Regulation of meiotic progression by the meiosis-specific checkpoint kinase Mek1 in fission yeast. J. Cell Sci. 116:259-271.
58. Prado, F., F. Cortes-Ledesma, P. Huertas, and A. Aguilera. 2003. Mitotic recombination in Saccharomyces cerevisiae. Curr. Genet 42:185-198.
59. Rockmill, B., and G. S. Roeder. 1991. A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes Dev. 5:2392-2404.
60. Rothenberg, M., J. Kohli, and K. Ludin. 2009. Ctp1 and the MRN-complex are required for endonucleolytic Rec12 removal with release of a single class of oligonucleotides in fission yeast. PLoS Genet. 5:e1000722.
61. Sanchez-Moran, E., K. Osman, J. D. Higgins, M. Pradillo, N. Cunado, G. H. Jones, and F. C. Franklin. 2008. ASY1 coordinates early events in the plant meiotic recombination pathway. Cytogenet. Genome Res. 120:302-312.
62. Sartori, A. A., C. Lukas, J. Coates, M. Mistrik, S. Fu, J. Bartek, R. Baer, J. Lukas, and S. P. Jackson. 2007. Human CtIP promotes DNA end resection. Nature 450:509-514.
63. Schuchert, P., and J. Kohli. 1988. The ade6-M26 mutation of Schizosaccharomyces pombe increases the frequency of crossing over. Genetics 119:507-515.
64. Schwacha, A., and N. Kleckner. 1997. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90:1123-1135.
65. Sheridan, S., and D. K. Bishop. 2006. Red-Hed regulation: recombinase Rad51, though capable of playing the leading role, may be relegated to supporting Dmc1 in budding yeast meiosis. Genes Dev. 20:1685-1691.
66. Sipiczki, M., and L. Ferenczy. 1977. Protoplast fusion of Schizosaccharomyces pombe auxotrophic mutants of identical mating-type. Mol. Gen. Genet. 151:77-81.
67. Smith, A. V., and G. S. Roeder. 1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136:957-967.
68. Smith, G. R., M. N. Boddy, P. Shanahan, and P. Russell. 2003. Fission yeast Mus81. Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165:2289-2293.
69. Thompson, D. A., and F. W. Stahl. 1999. Genetic control of recombination partner preference in yeast meiosis. Isolation and characterization of mutants elevated for meiotic unequal sister-chromatid recombination. Genetics 153:621-641.
70. Wells, J. L., D. W. Pryce, A. Estreicher, J. Loidl, and R. J. McFarlane. 2006. Linear element-independent meiotic recombination in Schizosaccharomyces pombe. Genetics 174:1105-1114.
71. Xu, L., B. M. Weiner, and N. Kleckner. 1997. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11:106-118.
72. 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.
73. 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.
74. Zierhut, C., M. Berlinger, C. Rupp, A. Shinohara, and F. Klein. 2004. Mnd1 is required for meiotic interhomolog repair. Curr. Biol. 14:752-762.