Protein Determinants of Meiotic DNA Break Hot Spots

Molecular Cell

Volumn 49, Issue 5, 2013, Pages 983-996

  Fowler, Kyle R ^a   Gutiérrez Velasco, Susana ^b   Martín Castellanos, Cristina ^b   Smith, Gerald R ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CAENORHABDITIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME 1; CHROMOSOME 3; CHROMOSOME SEGREGATION; DNA CONTENT; DNA STRAND BREAKAGE; DOUBLE STRANDED DNA BREAK; GENETIC DIFFERENCE; GENETIC VARIABILITY; GENOME; HISTONE MODIFICATION; LIMIT OF DETECTION; MEIOSIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SCHIZOSACCHAROMYCES; SISTER CHROMATID; SYNAPTONEMAL COMPLEX;

CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA, FUNGAL; MEIOSIS; NUCLEAR PROTEINS; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

SCHIZOSACCHAROMYCETACEAE;

EID: 84876838435     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.01.008     Document Type: Article

References (52)

1. Baudat F., Buard J., Grey C., Fledel-Alon A., Ober C., Przeworski M., Coop G., de Massy B. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 2010, 327:836-840.
2. Bellani M.A., Boateng K.A., McLeod D., Camerini-Otero R.D. The expression profile of the major mouse SPO11 isoforms indicates that SPO11β introduces double strand breaks and suggests that SPO11α has an additional role in prophase in both spermatocytes and oocytes. Mol. Cell. Biol. 2010, 30:4391-4403.
3. Blat Y., Protacio R.U., Hunter N., Kleckner N. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 2002, 111:791-802.
4. Bonfils S., Rozalén A.E., Smith G.R., Moreno S., Martín-Castellanos C. Functional interactions of Rec24, the fission yeast ortholog of mouse Mei4, with the meiotic recombination-initiation complex. J. Cell Sci. 2011, 124:1328-1338.
5. Borde V., Wu T.-C., Lichten M. Use of a recombination reporter insert to define meiotic recombination domains on chromosome III of Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:4832-4842.
6. Borde V., Robine N., Lin W., Bonfils S., Géli V., Nicolas A. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J. 2009, 28:99-111.
7. Bühler C., Borde V., Lichten M. Mapping meiotic single-strand DNA reveals a new landscape of DNA double-strand breaks in Saccharomyces cerevisiae. PLoS Biol. 2007, 5:e324.
8. Cervantes M.D., Farah J.A., Smith G.R. Meiotic DNA breaks associated with recombination in S. pombe. Mol. Cell 2000, 5:883-888.
9. Colaiácovo M.P., MacQueen A.J., Martinez-Perez E., McDonald K., Adamo A., La Volpe A., Villeneuve A.M. Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 2003, 5:463-474.
10. Cromie G.A., Rubio C.A., Hyppa R.W., Smith G.R. A natural meiotic DNA break site in Schizosaccharomyces pombe is a hotspot of gene conversion, highly associated with crossing over. Genetics 2005, 169:595-605.
11. Cromie G.A., Hyppa R.W., Cam H.P., Farah J.A., Grewal S.I., Smith G.R. A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast. PLoS Genet. 2007, 3:e141.
12. Davis L., Rozalén A.E., Moreno S., Smith G.R., Martin-Castellanos C. Rec25 and Rec27, novel linear-element components, link cohesin to meiotic DNA breakage and recombination. Curr. Biol. 2008, 18:849-854.
13. de Castro E., Soriano I., Marín L., Serrano R., Quintales L., Antequera F. Nucleosomal organization of replication origins and meiotic recombination hotspots in fission yeast. EMBO J. 2012, 31:124-137.
14. DeVeaux L.C., Smith G.R. Region-specific activators of meiotic recombination in Schizosaccharomyces pombe. Genes Dev. 1994, 8:203-210.
15. Ding D.Q., Sakurai N., Katou Y., Itoh T., Shirahige K., Haraguchi T., Hiraoka Y. Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast. J. Cell Biol. 2006, 174:499-508.
16. Ellermeier C., Smith G.R. Cohesins are required for meiotic DNA breakage and recombination in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 2005, 102:10952-10957.
17. Eshaghi M., Lee J.H., Zhu L., Poon S.Y., Li J., Cho K.H., Chu Z., Karuturi R.K., Liu J. Genomic binding profiling of the fission yeast stress-activated MAPK Sty1 and the bZIP transcriptional activator Atf1 in response to H2O2. PLoS ONE 2010, 5:e11620.
18. Estreicher A., Lorenz A., Loidl J. Mug20, a novel protein associated with linear elements in fission yeast meiosis. Curr. Genet. 2012, 58:119-127.
19. Glynn E.F., Megee P.C., Yu H.G., Mistrot C., Unal E., Koshland D.E., DeRisi J.L., Gerton J.L. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae. PLoS Biol. 2004, 2:E259.
20. Hirota K., Mizuno K., Shibata T., Ohta K. Distinct chromatin modulators regulate the formation of accessible and repressive chromatin at the fission yeast recombination hotspot ade6-M26. Mol. Biol. Cell 2008, 19:1162-1173.
21. Hyppa R.W., Smith G.R. Crossover invariance determined by partner choice for meiotic DNA break repair. Cell 2010, 142:243-255.
22. + recombination intermediate. PLoS Genet. 2008, 4:e1000267.
23. Keeney S. Spo11 and the formation of DNA double-strand breaks in meiosis. Recombination and Meiosis: Crossing-over and Disjunction 2007, 81-123. Springer-Verlag, Berlin. R. Egel, D.-H. Lankenau (Eds.).
24. Kon N., Krawchuk M.D., Warren B.G., Smith G.R., Wahls W.P. Transcription factor Mts1/Mts2 (Atf1/Pcr1, Gad7/Pcr1) activates the M26 meiotic recombination hotspot in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 1997, 94:13765-13770.
25. Kugou K., Fukuda T., Yamada S., Ito M., Sasanuma H., Mori S., Katou Y., Itoh T., Matsumoto K., Shibata T., et al. Rec8 guides canonical Spo11 distribution along yeast meiotic chromosomes. Mol. Biol. Cell 2009, 20:3064-3076.
26. Lantermann A.B., Straub T., Strålfors A., Yuan G.C., Ekwall K., Korber P. Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat. Struct. Mol. Biol. 2010, 17:251-257.
27. Loidl J. S. pombe linear elements: the modest cousins of synaptonemal complexes. Chromosoma 2006, 115:260-271.
28. Lorenz A., Wells J.L., Pryce D.W., Novatchkova M., Eisenhaber F., McFarlane R.J., Loidl J. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J. Cell Sci. 2004, 117:3343-3351.
29. Lorenz A., Estreicher A., Kohli J., Loidl J. Meiotic recombination proteins localize to linear elements in Schizosaccharomyces pombe. Chromosoma 2006, 115:330-340.
30. Ludin K., Mata J., Watt S., Lehmann E., Bähler J., Kohli J. Sites of strong Rec12/Spo11 binding in the fission yeast genome are associated with meiotic recombination and with centromeres. Chromosoma 2008, 117:431-444.
31. Martín-Castellanos C., Blanco M., Rozalén A.E., Pérez-Hidalgo L., García A.I., Conde F., Mata J., Ellermeier C., Davis L., San-Segundo P., et al. A large-scale screen in S. pombe identifies seven novel genes required for critical meiotic events. Curr. Biol. 2005, 15:2056-2062.
32. Mieczkowski P.A., Dominska M., Buck M.J., Gerton J.L., Lieb J.D., Petes T.D. Global analysis of the relationship between the binding of the Bas1p transcription factor and meiosis-specific double-strand DNA breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 2006, 26:1014-1027.
33. Milman N., Higuchi E., Smith G.R. Meiotic DNA double-strand break repair requires two nucleases, MRN and Ctp1, to produce a single size class of Rec12 (Spo11)-oligonucleotide complexes. Mol. Cell. Biol. 2009, 29:5998-6005.
34. Miyoshi T., Ito M., Kugou K., Yamada S., Furuichi M., Oda A., Yamada T., Hirota K., Masai H., Ohta K. A central coupler for recombination initiation linking chromosome architecture to S phase checkpoint. Mol. Cell 2012, 47:722-733.
35. Molnar M., Bähler J., Sipiczki M., Kohli J. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics 1995, 141:61-73.
36. Molnar M., Doll E., Yamamoto A., Hiraoka Y., Kohli J. Linear element formation and their role in meiotic sister chromatid cohesion and chromosome pairing. J. Cell Sci. 2003, 116:1719-1731.
37. Muñoz-Fuentes V., Di Rienzo A., Vilà C. Prdm9, a major determinant of meiotic recombination hotspots, is not functional in dogs and their wild relatives, wolves and coyotes. PLoS ONE 2011, 6:e25498.
38. Pan J., Sasaki M., Kniewel R., Murakami H., Blitzblau H.G., Tischfield S.E., Zhu X., Neale M.J., Jasin M., Socci N.D., et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 2011, 144:719-731.
39. Panizza S., Mendoza M.A., Berlinger M., Huang L., Nicolas A., Shirahige K., Klein F. Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 2011, 146:372-383.
40. Phadnis N., Hyppa R.W., Smith G.R. New and old ways to control meiotic recombination. Trends Genet. 2011, 27:411-421.
41. Ponticelli A.S., Smith G.R. Chromosomal context dependence of a eukaryotic recombinational hot spot. Proc. Natl. Acad. Sci. USA 1992, 89:227-231.
42. Sharif W.D., Glick G.G., Davidson M.K., Wahls W.P. Distinct functions of S. pombe Rec12 (Spo11) protein and Rec12-dependent crossover recombination (chiasmata) in meiosis I; and a requirement for Rec12 in meiosis II. Cell Chromosome 2002, 1:1-14.
43. Simonis N., Rual J.F., Carvunis A.R., Tasan M., Lemmens I., Hirozane-Kishikawa T., Hao T., Sahalie J.M., Venkatesan K., Gebreab F., et al. Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat. Methods 2009, 6:47-54.
44. Spirek M., Estreicher A., Csaszar E., Wells J.L., McFarlane R.J., Watts F.Z., Loidl J. SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe. Chromosoma 2010, 119:59-72.
45. Steiner W.W., Smith G.R. Natural meiotic recombination hot spots in the Schizosaccharomyces pombe genome successfully predicted from the simple sequence motif M26. Mol. Cell. Biol. 2005, 25:9054-9062.
46. Steiner W.W., Davidow P.A., Bagshaw A.T. Important characteristics of sequence-specific recombination hotspots in Schizosaccharomyces pombe. Genetics 2011, 187:385-396.
47. Tischfield S.E., Keeney S. Scale matters: the spatial correlation of yeast meiotic DNA breaks with histone H3 trimethylation is driven largely by independent colocalization at promoters. Cell Cycle 2012, 11:1496-1503.
48. Wahls W.P., Davidson M.K. Discrete DNA sites regulate global distribution of meiotic recombination. Trends Genet. 2010, 26:202-208.
49. Wahls W.P., Siegel E.R., Davidson M.K. Meiotic recombination hotspots of fission yeast are directed to loci that express non-coding RNA. PLoS ONE 2008, 3:e2887.
50. Wang J., Fan H.C., Behr B., Quake S.R. Genome-wide single-cell analysis of recombination activity and de novo mutation rates in human sperm. Cell 2012, 150:402-412.
51. White M.A., Dominska M., Petes T.D. Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1993, 90:6621-6625.
52. Young J.A., Schreckhise R.W., Steiner W.W., Smith G.R. Meiotic recombination remote from prominent DNA break sites in S. pombe. Mol. Cell 2002, 9:253-263.