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PMID: 19644444 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Distinct histone modifications define initiation and repair of meiotic recombination in the mouse.

The EMBO journal ·Vol. 28 ·No. 17 ·2009-09-02 ·Pages 2616-24

Buard J, Barthès P, Grey C, de Massy B

Abstract

Little is known about the factors determining the location and activity of the rapidly evolving meiotic crossover hotspots that shape genome diversity. Here, we show that several histone modifications are enriched at the active mouse Psmb9 hotspot, and we distinguish those marks that precede from those that follow hotspot recombinational activity. H3K4Me3, H3K4Me2 and H3K9Ac are specifically enriched in the chromatids that carry an active initiation site, and in the absence of DNA double-strand breaks (DSBs) in Spo11(-/-) mice. We thus propose that these marks are part of the substrate for recombination initiation at the Psmb9 hotspot. In contrast, hyperacetylation of H4 is increased as a consequence of DSB formation, as shown by its dependency on Spo11 and by the enrichment detected on both recombining chromatids. In addition, the comparison with another hotspot, Hlx1, strongly suggests that H3K4Me3 and H4 hyperacetylation are common features of DSB formation and repair, respectively. Altogether, the chromatin signatures of the Psmb9 and Hlx1 hotspots provide a basis for understanding the distribution of meiotic recombination.

MeSH Terms
Animals Crossing Over, Genetic DNA Breaks, Double-Stranded DNA Repair Histones/metabolism Meiosis/genetics Mice Mice, Inbred Strains Recombination, Genetic
Chemicals
Histones
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Buard Jérôme
Institut de Génétique Humaine, CNRS UPR 1142, Montpellier, France. [email protected]
Barthès Pauline
Grey Corinne
de Massy Bernard
References (52)
52 references, click to expand
  1. High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans.
    Science. 2008 Mar 7;319(5868):1395-8 PMID: 18239090
  2. A fine-scale map of recombination rates and hotspots across the human genome.
    Science. 2005 Oct 14;310(5746):321-4 PMID: 16224025
  3. Identification of residues in yeast Spo11p critical for meiotic DNA double-strand break formation.
    Mol Cell Biol. 2002 Feb;22(4):1106-15 PMID: 11809802
  4. Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites.
    EMBO J. 2009 Jan 21;28(2):99-111 PMID: 19078966
  5. An initiation site for meiotic crossing-over and gene conversion in the mouse.
    Nat Genet. 2002 Oct;32(2):296-9 PMID: 12244318
  6. Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression.
    EMBO J. 2004 May 5;23(9):1957-67 PMID: 15071505
  7. Polymorphism in the activity of human crossover hotspots independent of local DNA sequence variation.
    Hum Mol Genet. 2006 May 1;15(9):1401-11 PMID: 16543360
  8. The mouse Spo11 gene is required for meiotic chromosome synapsis.
    Mol Cell. 2000 Nov;6(5):975-87 PMID: 11106738
  9. Cis- and trans-acting elements regulate the mouse Psmb9 meiotic recombination hotspot.
    PLoS Genet. 2007 Jun;3(6):e100 PMID: 17590084
  10. Recombinational DNA double-strand breaks in mice precede synapsis.
    Nat Genet. 2001 Mar;27(3):271-6 PMID: 11242108
  11. The histone code at DNA breaks: a guide to repair?
    Nat Rev Mol Cell Biol. 2005 Oct;6(10):757-65 PMID: 16167054
  12. The role of chromatin during transcription.
    Cell. 2007 Feb 23;128(4):707-19 PMID: 17320508
  13. Chromatin modifications and their function.
    Cell. 2007 Feb 23;128(4):693-705 PMID: 17320507
  14. Clustering of meiotic double-strand breaks on yeast chromosome III.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5213-8 PMID: 9144217
  15. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark.
    Mol Cell. 2007 Jan 12;25(1):15-30 PMID: 17218268
  16. Meiotic recombination hot spots and cold spots.
    Nat Rev Genet. 2001 May;2(5):360-9 PMID: 11331902
  17. Temporal and spatial control of the Sycp1 gene transcription in the mouse meiosis: regulatory elements active in the male are not sufficient for expression in the female gonad.
    Mech Dev. 1999 Jan;80(1):29-39 PMID: 10096061
  18. Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2007 Mar 6;104(10):3955-60 PMID: 17360459
  19. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11.
    Mol Cell. 2000 Nov;6(5):989-98 PMID: 11106739
  20. Distinct chromatin modulators regulate the formation of accessible and repressive chromatin at the fission yeast recombination hotspot ade6-M26.
    Mol Biol Cell. 2008 Mar;19(3):1162-73 PMID: 18199689
  21. Changes in chromatin structure at recombination initiation sites during yeast meiosis.
    EMBO J. 1994 Dec 1;13(23):5754-63 PMID: 7988571
  22. Trans-regulation of mouse meiotic recombination hotspots by Rcr1.
    PLoS Biol. 2009 Feb 17;7(2):e36 PMID: 19226189
  23. Crossover and noncrossover pathways in mouse meiosis.
    Mol Cell. 2005 Nov 23;20(4):563-73 PMID: 16307920
  24. An atypical topoisomerase II from Archaea with implications for meiotic recombination.
    Nature. 1997 Mar 27;386(6623):414-7 PMID: 9121560
  25. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells.
    Nature. 2007 Aug 2;448(7153):553-60 PMID: 17603471
  26. Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis.
    Chromosome Res. 2007;15(5):565-77 PMID: 17674146
  27. The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae.
    EMBO J. 1995 Sep 15;14(18):4589-98 PMID: 7556102
  28. The recombinational anatomy of a mouse chromosome.
    PLoS Genet. 2008 Jul 11;4(7):e1000119 PMID: 18617997
  29. Molecular implementation and physiological roles for histone H3 lysine 4 (H3K4) methylation.
    Curr Opin Cell Biol. 2008 Jun;20(3):341-8 PMID: 18508253
  30. Histone modifications in response to DNA damage.
    Mutat Res. 2007 May 1;618(1-2):81-90 PMID: 17306843
  31. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  32. Meiosis-induced double-strand break sites determined by yeast chromatin structure.
    Science. 1994 Jan 28;263(5146):515-8 PMID: 8290959
  33. A common sequence motif associated with recombination hot spots and genome instability in humans.
    Nat Genet. 2008 Sep;40(9):1124-9 PMID: 19165926
  34. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11383-90 PMID: 11027339
  35. Genetic control of sex-dependent meiotic recombination in the major histocompatibility complex of the mouse.
    EMBO J. 1991 Mar;10(3):681-6 PMID: 2001681
  36. Molecular analysis of a recombinational hotspot adjacent to Lmp2 gene in the mouse MHC: fine location and chromatin structure.
    Mamm Genome. 1996 Jul;7(7):490-6 PMID: 8672125
  37. Playing hide and seek with mammalian meiotic crossover hotspots.
    Trends Genet. 2007 Jun;23(6):301-9 PMID: 17434233
  38. Un ménage à quatre: the molecular biology of chromosome segregation in meiosis.
    Cell. 2003 Feb 21;112(4):423-40 PMID: 12600308
  39. Meisetz, a novel histone tri-methyltransferase, regulates meiosis-specific epigenesis.
    Cell Cycle. 2006 Mar;5(6):615-20 PMID: 16582607
  40. The histone H3 lysine 27-specific demethylase Jmjd3 is required for neural commitment.
    PLoS One. 2008 Aug 21;3(8):e3034 PMID: 18716661
  41. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation.
    Biochem Soc Trans. 2006 Aug;34(Pt 4):523-5 PMID: 16856850
  42. Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis.
    Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11380-5 PMID: 15280549
  43. The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae.
    DNA Repair (Amst). 2008 Aug 2;7(8):1298-308 PMID: 18515193
  44. Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot.
    EMBO J. 2004 Apr 21;23(8):1792-803 PMID: 14988732
  45. Genome-wide control of the distribution of meiotic recombination.
    PLoS Biol. 2009 Feb 17;7(2):e35 PMID: 19226188
  46. A histone H3 methyltransferase controls epigenetic events required for meiotic prophase.
    Nature. 2005 Nov 17;438(7066):374-8 PMID: 16292313
  47. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals.
    Nature. 2009 Mar 12;458(7235):223-7 PMID: 19182780
  48. The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate.
    EMBO J. 1995 Sep 15;14(18):4599-608 PMID: 7556103
  49. Site-specific analysis of histone methylation and acetylation.
    Methods Mol Biol. 2004;287:99-120 PMID: 15273407
  50. A discrete class of intergenic DNA dictates meiotic DNA break hotspots in fission yeast.
    PLoS Genet. 2007 Aug;3(8):e141 PMID: 17722984
  51. Rad51 immunocytology in rat and mouse spermatocytes and oocytes.
    Chromosoma. 1997 Sep;106(4):207-15 PMID: 9254722
  52. Meiotic recombination hotspots of fission yeast are directed to loci that express non-coding RNA.
    PLoS One. 2008 Aug 06;3(8):e2887 PMID: 18682829
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
1460-2075
Published
2009-09-02
Epub
2009-00-30
Pages
2616-24
Language
English
Region
England
NLM ID
8208664
PMCID
PMC2738703
Subset
IM
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