Variation in Genome-Wide Levels of Meiotic Recombination Is Established at the Onset of Prophase in Mammalian Males

PLoS Genetics

Volumn 10, Issue 1, 2014, Pages

  Baier, Brian ^a   Hunt, Patricia ^a   Broman, Karl W ^b   Hassold, Terry ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; DMC1 PROTEIN; MSH4 PROTEIN; PROTEIN; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; DOUBLE STRANDED BREAK; GENE LOCUS; GENETIC VARIABILITY; IMMUNOFLUORESCENCE; INBRED MOUSE STRAIN; MALE; MITOTIC RECOMBINATION; MOUSE; NONHUMAN; PROPHASE; PROTEIN ANALYSIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA, CRUCIFORM; ENDODEOXYRIBONUCLEASES; GENOME; MALE; MEIOSIS; MICE; NUCLEAR PROTEINS; PROPHASE; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SYNAPTONEMAL COMPLEX;

EID: 84896740086     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004125     Document Type: Article

References (62)

1. Rockmill B, Roeder GS, (1994) The yeast med1 mutant undergoes both meiotic homolog nondisjunction and precocious separation of sister chromatids. Genetics 136: 65-74.
2. Molnar M, Parisi S, Kakihara Y, Nojima H, Yamamoto A, et al. (2001) Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe. Genetics 157: 519-532.
3. Zetka MC, Rose AM, (1995) Mutant rec-1 eliminates the meiotic pattern of crossing over in Caenorhabditis elegans. Genetics 141: 1339-1349.
4. Hawley RS, Theurkauf WE, (1993) Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet 9: 310-317.
5. Hassold T, Hunt P, (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2: 280-291.
6. Cheung VG, Burdick JT, Hirschmann D, Morley M, (2007) Polymorphic variation in human meiotic recombination. American journal of human genetics 80: 526-530.
7. Coop G, Wen X, Ober C, Pritchard JK, Przeworski M, (2008) High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319: 1395-1398.
8. Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467: 1099-1103.
9. Lynn A, Koehler KE, Judis L, Chan ER, Cherry JP, et al. (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296: 2222-2225.
10. Hassold T, Hansen T, Hunt P, VandeVoort C, (2009) Cytological studies of recombination in rhesus males. Cytogenetic and genome research 124: 132-138.
11. Koehler KE, Cherry JP, Lynn A, Hunt PA, Hassold TJ, (2002) Genetic control of mammalian meiotic recombination. I. Variation in exchange frequencies among males from inbred mouse strains. Genetics 162: 297-306.
12. Dumont BL, White MA, Steffy B, Wiltshire T, Payseur BA, (2011) Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps. Genome research 21: 114-125.
13. Chowdhury R, Bois PR, Feingold E, Sherman SL, Cheung VG, (2009) Genetic analysis of variation in human meiotic recombination. PLoS genetics 5: e1000648.
14. Fledel-Alon A, Leffler EM, Guan Y, Stephens M, Coop G, et al. (2011) Variation in human recombination rates and its genetic determinants. PloS one 6: e20321.
15. Matise TC, Chen F, Chen W, De La Vega FM, Hansen M, et al. (2007) A second-generation combined linkage physical map of the human genome. Genome Res 17: 1783-1786.
16. Martini E, Diaz RL, Hunter N, Keeney S, (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285-295.
17. Cole F, Kauppi L, Lange J, Roig I, Wang R, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nature cell biology 14: 424-430.
18. Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, et al. (2008) Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319: 1398-1401.
19. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, et al. (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nature Genetics 45: 269-278.
20. Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, et al. (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over [see comments]. Nat Genet 13: 336-342.
21. Masson JY, West SC, (2001) The Rad51 and Dmc1 recombinases: a non-identical twin relationship. Trends in biochemical sciences 26: 131-136.
22. Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, et al. (2000) MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 14: 1539-1547.
23. Jessop L, Rockmill B, Roeder GS, Lichten M, (2006) Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS genetics 2: e155.
24. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
25. Keeney S, Baudat F, Angeles M, Zhou ZH, Copeland NG, et al. (1999) A mouse homolog of the Saccharomyces cerevisiae meiotic recombination DNA transesterase Spo11p. Genomics 61: 170-182.
26. Anderson LK, Reeves A, Webb LM, Ashley T, (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151: 1569-1579.
27. Svetlanov A, Baudat F, Cohen PE, de Massy B, (2008) Distinct functions of MLH3 at recombination hot spots in the mouse. Genetics 178: 1937-1945.
28. Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG, et al. (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic acids research 36: 4057-4066.
29. Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, et al. (2002) The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. Journal of cell science 115: 1611-1622.
30. Tarsounas M, Morita T, Pearlman RE, Moens PB, (1999) RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J Cell Biol 147: 207-220.
31. Barchi M, Mahadevaiah S, Di Giacomo M, Baudat F, de Rooij DG, et al. (2005) Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Molecular and cellular biology 25: 7203-7215.
32. Callender TL, Hollingsworth NM, (2010) Mek1 suppression of meiotic double-strand break repair is specific to sister chromatids, chromosome autonomous and independent of Rec8 cohesin complexes. Genetics 185: 771-782.
33. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
34. Bellani MA, Romanienko PJ, Cairatti DA, Camerini-Otero RD, (2005) SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. Journal of cell science 118: 3233-3245.
35. Barchi M, Roig I, Di Giacomo M, de Rooij DG, Keeney S, et al. (2008) ATM promotes the obligate XY crossover and both crossover control and chromosome axis integrity on autosomes. PLoS genetics 4: e1000076.
36. Baker SM, Bronner CE, Zhang L, Plug AW, Robatzek M, et al. (1995) Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell 82: 309-319.
37. Yuan L, Liu JG, Hoja MR, Wilbertz J, Nordqvist K, et al. (2002) Female germ cell aneuploidy and embryo death in mice lacking the meiosis-specific protein SCP3. Science 296: 1115-1118.
38. Baudat F, Manova K, Yuen JP, Jasin M, Keeney S, (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking spo11. Mol Cell 6: 989-998.
39. Edelmann W, Cohen PE, Kneitz B, Winand N, Lia M, et al. (1999) Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nature Genetics 21: 123-127.
40. Badge RM, Yardley J, Jeffreys AJ, Armour JA, (2000) Crossover breakpoint mapping identifies a subtelomeric hotspot for male meiotic recombination. Human Molecular Genetics 9: 1239-1244.
41. Lien S, Szyda J, Schechinger B, Rappold G, Arnheim N, (2000) Evidence for heterogeneity in recombination in the human pseudoautosomal region: high resolution analysis by sperm typing and radiation-hybrid mapping. American journal of human genetics 66: 557-566.
42. Jeffreys AJ, Murray J, Neumann R, (1998) High-resolution mapping of crossovers in human sperm defines a minisatellite-associated recombination hotspot. Mol Cell 2: 267-273.
43. Jeffreys AJ, May CA, (2004) Intense and highly localized gene conversion activity in human meiotic crossover hot spots. Nature Genetics 36: 151-156.
44. McVean GA, Myers SR, Hunt S, Deloukas P, Bentley DR, et al. (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304: 581-584.
45. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P, (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310: 321-324.
46. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836-840.
47. Berg IL, Neumann R, Lam KW, Sarbajna S, Odenthal-Hesse L, et al. (2010) PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nature Genetics 42: 859-863.
48. Parvanov ED, Petkov PM, Paigen K, (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327: 835.
49. Stefansson H, Helgason A, Thorleifsson G, Steinthorsdottir V, Masson G, et al. (2005) A common inversion under selection in Europeans. Nature Genetics 37: 129-137.
50. Hinch AG, Tandon A, Patterson N, Song Y, Rohland N, et al. (2011) The landscape of recombination in African Americans. Nature 476: 170-175.
51. Murdoch B, Owen N, Shirley S, Crumb S, Broman KW, et al. (2010) Multiple loci contribute to genome-wide recombination levels in male mice. Mammalian genome: official journal of the International Mammalian Genome Society 21: 550-555.
52. Dumont BL, Payseur BA, (2011) Genetic analysis of genome-scale recombination rate evolution in house mice. PLoS Genet 7: e1002116.
53. Moens PB, Marcon E, Shore JS, Kochakpour N, Spyropoulos B, (2007) Initiation and resolution of interhomolog connections: crossover and non-crossover sites along mouse synaptonemal complexes. Journal of cell science 120: 1017-1027.
54. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286-1289.
55. Gruhn J, Rubio C, Broman K, Hunt P, Hassold T, (2013) Cytological studies of human meiosis: sex-specific differences in recombination originate at, or prior to, establishment of double-strand breaks. PloS one 8 (12):: e85075.
56. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, et al. (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472: 375-378.
57. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV, (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485: 642-645.
58. de La Casa-Esperon E, Loredo-Osti JC, Pardo-Manuel de Villena F, Briscoe TL, Malette JM, et al. (2002) X chromosome effect on maternal recombination and meiotic drive in the mouse. Genetics 161: 1651-1659.
59. Royo H, Polikiewicz G, Mahadevaiah SK, Prosser H, Mitchell M, et al. (2010) Evidence that meiotic sex chromosome inactivation is essential for male fertility. Current biology: CB 20: 2117-2123.
60. Adelman CA, Petrini JH, (2008) ZIP4H (TEX11) deficiency in the mouse impairs meiotic double strand break repair and the regulation of crossing over. PLoS genetics 4: e1000042.
61. Peters AH, Plug AW, van Vugt MJ, de Boer P, (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5: 66-68.
62. Novak I, Wang H, Revenkova E, Jessberger R, Scherthan H, et al. (2008) Cohesin Smc1beta determines meiotic chromatin axis loop organization. The Journal of cell biology 180: 83-90.