Local and sex-specific biases in crossover vs. noncrossover outcomes at meiotic recombination hot spots in mice

Genes and Development

Volumn 29, Issue 16, 2015, Pages 1721-1733

  de Boer, Esther ^a,b   Jasin, Maria ^a   Keeney, Scott ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Crossing over; Gene conversion; Hot spot; Meiosis; Recombination; Spo11

Indexed keywords

RECOMBINANT DNA;

ARTICLE; CHROMOSOME 1; CONTROLLED STUDY; CROSSING OVER; DOUBLE STRANDED DNA BREAK; FEMALE; FREQUENCY; GENE CONVERSION; GENETIC RECOMBINATION; GENOME; HAPLOTYPE; MALE; MEIOTIC RECOMBINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECOMBINANT INBRED STRAIN; SEX DIFFERENCE; ANIMAL; C57BL MOUSE; CHROMOSOMAL MAPPING; GENETICS; MEIOSIS;

MAMMALIA; MUS;

ANIMALS; CHROMOSOME MAPPING; DNA BREAKS, DOUBLE-STRANDED; FEMALE; MALE; MEIOSIS; MICE; MICE, INBRED C57BL; RECOMBINATION, GENETIC; SEX FACTORS;

EID: 84940035439     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.265561.115     Document Type: Article

References (63)

1. Allers T, Lichten M. 2001. Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol Cell 8: 225-231.
2. Arbeithuber B, Betancourt AJ, Ebner T, Tiemann-Boege I. 2015. Crossovers are associated with mutation and biased gene conversion at recombination hotspots. Proc Natl Acad Sci 112: 2109-2114.
3. Baker CL, Walker M, Kajita S, Petkov PM, Paigen K. 2014. PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res 24: 724-732.
4. Baudat F, de Massy B. 2007a. Cis-and trans-acting elements regulate the mouse Psmb9 meiotic recombination hotspot. PLoS Genet 3: e100.
5. Baudat F, de Massy B. 2007b. Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res 15: 565-577.
6. Baudat F, de Massy B. 2009. Parallel detection of crossovers and noncrossovers in mouse germ cells. Methods Mol Biol 557: 305-322.
7. Baudat F, Buard J, Grey C, Fledel-Alon A, Ober C, Przeworski M, Coop G, de Massy B. 2010. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327: 836-840.
8. Baudat F, Imai Y, de Massy B. 2013. Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14: 794-806.
9. BillingsT, Sargent EE, Szatkiewicz JP, Leahy N, Kwak I-Y, Bektassova N, Walker M, Hassold T, Graber JH, Broman KW, et al. 2010. Patterns of recombination activity on mouse chromosome 11 revealed by high resolution mapping. PLoS One 5: e15340.
10. Bois PRJ. 2007. A highly polymorphic meiotic recombination mouse hot spot exhibits incomplete repair. Mol Cell Biol 27: 7053-7062.
11. 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.
12. Buchner DA, Trudeau M, George AL Jr, Sprunger LK, Meisler MH. 2003. High-resolution mapping of the sodium channel modifier Scnm1 on mouse chromosome 3 and identification of a 1. 3-kb recombination hot spot. Genomics 82: 452-459.
13. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, Vader G, Hochwagen A, Roeder GS, Fung JC. 2008. Global analysis of the meiotic crossover landscape. Dev Cell 15: 401-415.
14. Clement Y, Arndt PF. 2013. Meiotic recombination strongly influences GC-content evolution in short regions in the mouse genome. Mol Biol Evol 30: 2612-2618.
15. Cole F, Jasin M. 2011. Isolation of meiotic recombinants from mouse sperm. Methods Mol Biol 745: 251-282.
16. Cole F, Keeney S, Jasin M. 2010. Comprehensive, fine-scale dissection of homologous recombination outcomes at a hot spot in mouse meiosis. Mol Cell 39: 700-710.
17. Cole F, Baudat F, Grey C, Keeney S, de Massy B, Jasin M. 2014. Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat Genet 46: 1072-1080.
18. 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.
19. de Boer E, Stam P, Dietrich AJJ, Pastink A, Heyting C. 2006. Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci 103: 9607-9612.
20. de Boer E, Lhuissier FG, Heyting C. 2009. Cytological analysis of interference in mouse meiosis. Methods Mol Biol 558: 355-382.
21. de Boer E, Jasin M, Keeney S. 2013. Analysis of recombinants in female mouse meiosis. Methods Mol Biol 957: 19-45.
22. Dietrich AJ, Mulder RJ. 1983. A light-and electron microscopic analysis of meiotic prophase in female mice. Chromosoma 88: 377-385.
23. Drouaud J, Camilleri C, Bourguignon PY, Canaguier A, Berard A, Vezon D, Giancola S, Brunel D, Colot V, Prum B, et al. 2006. Variation in crossing-over rates across chromosome 4 of Arabidopsis thaliana reveals the presence of meiotic recombination 'hot spots'. Genome Res 16: 106-114.
24. Duret L, Galtier N. 2009. Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10: 285-311.
25. Eppig JJ, Schroeder AC. 1989. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod 41: 268-276.
26. Fowler KR, Sasaki M, Milman N, Keeney S, Smith GR. 2014. Evolutionarily diverse determinants of meiotic DNA break and recombination landscapes across the genome. Genome Res 24: 1650-1664.
27. Goldfarb T, Lichten M. 2010. Frequent and efficient use of the sister chromatid for DNAdouble-strand break repair during budding yeast meiosis. PLoS Biol 8: e1000520.
28. Grey C, Barthès P, Chauveau-Le Friec G, Langa F, Baudat F, de Massy B. 2011. Mouse PRDM9 DNA-binding specificity determines sites of histone H3 lysine 4 trimethylation for initiation of meiotic recombination. PLoS Biol 9: e1001176.
29. Guillon H, de Massy B. 2002. An initiation site for meiotic crossing-over and gene conversion in the mouse. Nat Genet 32: 296-299.
30. Guillon H, Baudat F, Grey C, Liskay RM, de Massy B. 2005. Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20: 563-573.
31. Holloway K, Lawson VE, Jeffreys AJ. 2006. Allelic recombination and de novo deletions in sperm in the human β-globin gene region. Hum Mol Genet 15: 1099-1111.
32. Hunter N, Kleckner N. 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.
33. HyppaRW, Smith GR. 2010. Crossover invariance determined by partner choice for meiotic DNA break repair. Cell 142: 243-255.
34. Jeffreys AJ, May CA. 2003. DNAenrichment by allele-specific hybridization (DEASH): a novel method for haplotyping and for detecting low-frequency base substitutional variants and recombinant DNA molecules. Genome Res 13: 2316-2324.
35. Jeffreys AJ, May CA. 2004. Intense and highly localized gene conversion activity in human meiotic crossover hot spots. Nat Genet 36: 151-156.
36. Jeffreys AJ, Neumann R. 2002. Reciprocal crossover asymmetry and meiotic drive in a human recombination hot spot. Nat Genet 31: 267-271.
37. Jeffreys AJ, Kauppi L, Neumann R. 2001. Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nat Genet 29: 217-222.
38. Jones GH, Franklin FC. 2006. Meiotic crossing-over: obligation and interference. Cell 126: 246-248.
39. Kauppi L, Jasin M, Keeney S. 2007. Meiotic crossover hotspots contained in haplotype block boundaries of the mouse genome. Proc Natl Acad Sci 104: 13396-13401.
40. Kauppi L, May CA, Jeffreys AJ. 2009. Analysis of meiotic recombination products from human sperm. Methods Mol Biol 557: 323-355.
41. Lam I, Keeney S. 2014. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb Perspect Biol 7: a016634.
42. Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM. 2013. Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature 502: 703-706.
43. Louis EJ, Haber JE. 1990. Mitotic recombination among subtelomeric Y′ repeats in Saccharomyces cerevisiae. Genetics 124: 547-559.
44. Louis EJ, Naumova ES, Lee A, Naumov G, Haber JE. 1994. The chromosome end in yeast: its mosaic nature and influence on recombinational dynamics. Genetics 136: 789-802.
45. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM. 2008. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
46. Martini E, BordeV, Legendre M, Audic S, Regnault B, Soubigou G, Dujon B, Llorente B. 2011. Genome-wide analysis of heteroduplex DNA in mismatch repair-deficient yeast cells reveals novel properties of meiotic recombination pathways. PLoS Genet 7: e1002305.
47. McClellan KA, Gosden R, Taketo T. 2003. Continuous loss of oocytes throughout meiotic prophase in the normal mouse ovary. Dev Biol 258: 334-348.
48. Myers S, Bowden R, Tumian A, Bontrop RE, Freeman C, MacFie TS, McVean G, Donnelly P. 2010. Drive against hotspot motifs in primates implicates the PRDM9gene in meiotic recombination. Science 327: 876-879.
49. Odenthal-Hesse L, Berg IL, Veselis A, Jeffreys AJ, May CA. 2014. Transmission distortion affecting human noncrossover but not crossover recombination: a hidden source of meiotic drive. PLoS Genet 10: e1004106.
50. Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SHS, Graber JH, Broman KW, Petkov PM. 2008. The recombinational anatomy of a mouse chromosome. PLoS Genet 4: e1000119.
51. Pratto F, Brick K, Khil P, Smagulova F, Petukhova GV, Camerini-Otero RD. 2014. DNA recombination. Recombination initiation maps of individual human genomes. Science 346: 1256442.
52. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, Holloway JK, Baudat F, de Massy B, Wang J, et al. 2013. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 45: 269-278.
53. Rouyer F, Simmler MC, Johnsson C, Vergnaud G, Cooke HJ, Weissenbach J. 1986. A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature 319: 291-295.
54. Sarbajna S, Denniff M, Jeffreys AJ, Neumann R, Soler Artigas M, Veselis A, May CA. 2012. A major recombination hotspot in the XqYq pseudoautosomal region gives new insight into processing of human gene conversion events. HumMol Genet 21: 2029-2038.
55. Schwacha A, Kleckner N. 1994. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.
56. Serrentino ME, Chaplais E, Sommermeyer V, Borde V. 2013. Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet 9: e1003416.
57. Shifman S, Bell JT, Copley RR, Taylor MS, Williams RW, Mott R, Flint J. 2006. A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol 4: e395.
58. Shiroishi T, Hanzawa N, Sagai T, Ishiura M, Gojobori T, Steinmetz M, Moriwaki K. 1990. Recombinational hotspot specific to female meiosis in the mouse major histocompatibility complex. Immunogenetics 31: 79-88.
59. Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV. 2011. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472: 375-378.
60. 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.
61. Wu ZK, Getun IV, Bois PR. 2010. Anatomy of mouse recombination hot spots. Nucleic Acids Res 38: 2346-2354.
62. Yauk CL, Bois PR, Jeffreys AJ. 2003. High-resolution sperm typing of meiotic recombination in the mouseMHCEβ gene. EMBOJ 22: 1389-1397.
63. Youds JL, Boulton SJ. 2011. The choice in meiosis-defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501-513.