Abstract
During meiosis, recombination is induced to promote connections between homologous chromosomes, thereby ensuring faithful chromosome segregation. These connections result from reciprocal recombination events or crossovers. Absence or defects of recombination can lead to genome instability, chromosome nondisjunction, aneuploid gametes, or reduced fertility. Recombination events are therefore highly regulated through mechanisms that are still poorly understood. The role of epigenetic modifications in meiotic recombination is suggested by several observations, particularly by the differences between male and female recombination as well as by interindividual variations in crossover rates. In this review, we describe features of meiotic recombination that might involve epigenetic controls. We then present the epigenetic marks and modifiers known to occur or to play a role during meiotic prophase when recombination takes place. Direct evidence of a functional link between histone modifications and recombination is highlighted by a recent analysis of the distribution of recombination showing that the protein PRDM9 targets chromatin modifications to specific sites in the genome where initiation of meiotic recombination takes place.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- Chr:
-
Chromosome
- cM:
-
Centi morgan
- CO:
-
Crossover
- DNMT:
-
DNA (cytosine-5)-methyltransferase
- DSB:
-
DNA double-strand break
- FISH:
-
Fluorescent in situ hybridization
- HAT:
-
Histone acetyl-transferase
- HDAC:
-
Histone deacetylase
- HDMT:
-
Histone demethylase
- Histone modifications:
-
Example H3K4Me3 is histone H3 with tri-methylated lysine 4
- HJ:
-
Holliday junction
- HMT:
-
Histone methyl-transferase
- Hp1:
-
Heterochromatin protein 1
- IAP:
-
Intracisternal A particle
- JMJD1a:
-
Jumonji domain-containing histone demethylase 1a
- KO:
-
Knock-out
- LD:
-
Linkage disequilibrium
- LINE:
-
Long interspersed element
- MAEL:
-
Maelstrom
- MSCI:
-
Meiotic sex chromosome inactivation
- Msuc:
-
Meiotic silencing of unsynapsed chromatin
- NCO:
-
Non crossover
- PiRNA:
-
Piwi-interacting RNA
- SC:
-
Synaptonemal complex
- SEI:
-
Single end invasion
- SNP:
-
Single nucleotide polymorphism
- TSA:
-
Trichostatin A
References
Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316:744–747
Arnheim N, Calabrese P, Tiemann-Boege I (2007) Mammalian meiotic recombination hot spots. Annu Rev Genet 41:369–399
Baarends WM, Grootegoed JA (2003) Chromatin dynamics in the male meiotic prophase. Cytogenet Genome Res 103:225–234
Baarends WM, Wassenaar E, Hoogerbrugge JW, van Cappellen G, Roest HP, Vreeburg J, Ooms M, Hoeijmakers JH, Grootegoed JA (2003) Loss of HR6B ubiquitin-conjugating activity results in damaged synaptonemal complex structure and increased crossing-over frequency during the male meiotic prophase. Mol Cell Biol 23:1151–1162
Baarends WM, Wassenaar E, van der Laan R, Hoogerbrugge J, Sleddens-Linkels E, Hoeijmakers JH, de Boer P, Grootegoed JA (2005) Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol 25:1041–1053
Barlow AL, Hulten MA (1998) Crossing over analysis at pachytene in man. Eur J Hum Genet 6:350–358
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(5967):836–840
Baudat F, de Massy B (2007a) Cis- and trans-acting elements regulate the mouse Psmb9 meiotic recombination hotspot. PLoS Genet 3:e100
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
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
Bayes JJ, Malik HS (2009) Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326:1538–1541
Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–417 (see comments)
Borde V, Robine N, Lin W, Bonfils S, Geli V, Nicolas A (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28:99–111
Bourc’his D, Bestor TH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431:96–99
Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539
Bramlage B, Kosciessa U, Doenecke D (1997) Differential expression of the murine histone genes H3.3A and H3.3B. Differentiation 62:13–20
Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 63:861–869
Buard J, Barthes P, Grey C, de Massy B (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28:2616–2624
Buard J, de Massy B (2007) Playing hide and seek with mammalian meiotic crossover hotspots. Trends Genet 23:301–309
Buard J, Shone AC, Jeffreys AJ (2000) Meiotic recombination and flanking marker exchange at the highly unstable human minisatellite CEB1 (D2S90). Am J Hum Genet 67:333–344
Burgoyne PS, Mahadevaiah SK, Turner JM (2009) The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10:207–216
Carmell MA, Girard A, van de Kant HJ, Bourc’his D, Bestor TH, de Rooij DG, Hannon GJ (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12:503–514
Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ, Redon C, Pilch DR, Olaru A, Eckhaus M, Camerini-Otero RD, Tessarollo L, Livak F, Manova K, Bonner WM, Nussenzweig MC, Nussenzweig A (2002) Genomic instability in mice lacking histone H2AX. Science 296:922–927
Cheng EY, Hunt PA, Naluai-Cecchini TA, Fligner CL, Fujimoto VY, Pasternack TL, Schwartz JM, Steinauer JE, Woodruff TJ, Cherry SM, Hansen TA, Vallente RU, Broman KW, Hassold TJ (2009) Meiotic recombination in human oocytes. PLoS Genet 5:e1000661
Cheung VG, Burdick JT, Hirschmann D, Morley M (2007) Polymorphic variation in human meiotic recombination. Am J Hum Genet 80:526–530
Chowdhury R, Bois PR, Feingold E, Sherman SL, Cheung VG (2009) Genetic analysis of variation in human meiotic recombination. PLoS Genet 5:e1000648
Clarke HJ, McLay DW, Mohamed OA (1998) Linker histone transitions during mammalian oogenesis and embryogenesis. Dev Genet 22:17–30
Coop G, Przeworski M (2007) An evolutionary view of human recombination. Nat Rev Genet 8:23–34
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
Cox A, Ackert-Bicknell C, Dumont BL, Ding Y, Tzenova Bell J, Brockmann GA, Wergedal JE, Bult C, Paigen B, Flint J, Tsaih SW, Churchill GA, Broman KW (2009) A new standard genetic map for the mouse. Genetics 182(4):1335–1344
de Boer E, Stam P, Dietrich AJ, Pastink A, Heyting C (2006) Two levels of interference in mouse meiotic recombination. Proc Natl Acad Sci USA 103:9607–9612
de Massy B (2003) Distribution of meiotic recombination sites. Trends Genet 19:514–522
de Massy B, Rocco V, Nicolas A (1995) The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J 14:4589–4598
Delaval K, Feil R (2004) Epigenetic regulation of mammalian genomic imprinting. Curr Opin Genet Dev 14:188–195
Deng W, Lin H (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2:819–830
Diaz RL, Alcid AD, Berger JM, Keeney S (2002) Identification of residues in yeast spo11p critical for meiotic DNA double-strand break formation. Mol Cell Biol 22:1106–1115
Fantz DA, Hatfield WR, Horvath G, Kistler MK, Kistler WS (2001) Mice with a targeted disruption of the H1t gene are fertile and undergo normal changes in structural chromosomal proteins during spermiogenesis. Biol Reprod 64:425–431
Fearnhead P, Harding RM, Schneider JA, Myers S, Donnelly P (2004) Application of coalescent methods to reveal fine-scale rate variation and recombination hotspots. Genetics 167:2067–2081
Fenic I, Sonnack V, Failing K, Bergmann M, Steger K (2004) In vivo effects of histone-deacetylase inhibitor trichostatin-a on murine spermatogenesis. J Androl 25:811–818
Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A (2003) H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4:497–508
Franklin SG, Zweidler A (1977) Non-allelic variants of histones 2a, 2b and 3 in mammals. Nature 266:273–275
Fu F, Sander JD, Maeder M, Thibodeau-Beganny S, Joung JK, Dobbs D, Miller L, Voytas DF (2009) Zinc Finger Database (ZiFDB): a repository for information on C2H2 zinc fingers and engineered zinc-finger arrays. Nucleic Acids Res 37:D279–D283
Girard A, Sachidanandam R, Hannon GJ, Carmell MA (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442:199–202
Godmann M, Auger V, Ferraroni-Aguiar V, Di Sauro A, Sette C, Behr R, Kimmins S (2007) Dynamic regulation of histone H3 methylation at lysine 4 in mammalian spermatogenesis. Biol Reprod 77:754–764
Godmann M, Lambrot R, Kimmins S (2009) The dynamic epigenetic program in male germ cells: its role in spermatogenesis, testis cancer, and its response to the environment. Microsc Res Tech 72:603–619
Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481–514
Grey C, Baudat F, de Massy B (2009) Genome-wide control of the distribution of meiotic recombination. PLoS Biol 7:e35
Grivna ST, Pyhtila B, Lin H (2006) MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci USA 103:13415–13420
Grunau C, Buard J, Brun ME, De Sario A (2006) Mapping of the juxtacentromeric heterochromatin-euchromatin frontier of human chromosome 21. Genome Res 16:1198–1207
Guillon H, Baudat F, Grey C, Liskay RM, de Massy B (2005) Crossover and noncrossover pathways in mouse meiosis. Mol Cell 20:563–573
Handel MA, Schimenti JC (2010) Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 11(2):124–136
Hata K, Kusumi M, Yokomine T, Li E, Sasaki H (2006) Meiotic and epigenetic aberrations in Dnmt3L-deficient male germ cells. Mol Reprod Dev 73:116–122
Hayashi K, Yoshida K, Matsui Y (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438:374–378
Hendzel MJ, Lever MA, Crawford E, Th’ng JP (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279:20028–20034
Hirota K, Mizuno K, Shibata T, Ohta K (2008) Distinct chromatin modulators regulate the formation of accessible and repressive chromatin at the fission yeast recombination hotspot ade6-M26. Mol Biol Cell 19:1162–1173
Hoog C, Schalling M, Grunder-Brundell E, Daneholt B (1991) Analysis of a murine male germ cell-specific transcript that encodes a putative zinc finger protein. Mol Reprod Dev 30:173–181
Hunter N (2007) Meiotic recombination. In: Aguilera A, Rothstein R (eds) Molecular genetics of recombination. Springer, Berlin, pp 381–442
Irie S, Tsujimura A, Miyagawa Y, Ueda T, Matsuoka Y, Matsui Y, Okuyama A, Nishimune Y, Tanaka H (2009) Single nucleotide polymorphisms in PRDM9 (MEISETZ) in patients with nonobstructive azoospermia. J Androl 30(4):426–431
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
Jeffreys AJ, Neumann R (2002) Reciprocal crossover asymmetry and meiotic drive in a human recombination hot spot. Nat Genet 31:267–271
Jeffreys AJ, Neumann R (2005) Factors influencing recombination frequency and distribution in a human meiotic crossover hotspot. Hum Mol Genet 14:2277–2287
Jeffreys AJ, Neumann R (2009) The rise and fall of a human recombination hot spot. Nat Genet 41(5):625–629
Kaneda M, Sado T, Hata K, Okano M, Tsujimoto N, Li E, Sasaki H (2004) Role of de novo DNA methyltransferases in initiation of genomic imprinting and X-chromosome inactivation. Cold Spring Harb Symp Quant Biol 69:125–129
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
Khadake JR, Rao MR (1995) DNA- and chromatin-condensing properties of rat testes H1a and H1t compared to those of rat liver H1bdec; H1t is a poor condenser of chromatin. Biochemistry 34:15792–15801
Khalil AM, Wahlestedt C (2008) Epigenetic mechanisms of gene regulation during mammalian spermatogenesis. Epigenetics 3:21–28
Kimmins S, Sassone-Corsi P (2005) Chromatin remodelling and epigenetic features of germ cells. Nature 434:583–589
Kleckner N, Storlazzi A, Zickler D (2003) Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19:623–628
Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, Sigurdardottir S, Barnard J, Hallbeck B, Masson G, Shlien A, Palsson ST, Frigge ML, Thorgeirsson TE, Gulcher JR, Stefansson K (2002) A high-resolution recombination map of the human genome. Nat Genet 31:241–247
Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, Gudbjartsson DF, Jonsdottir GM, Gudjonsson SA, Sverrisson S, Thorlacius T, Jonasdottir A, Hardarson GA, Palsson ST, Frigge ML, Gulcher JR, Thorsteinsdottir U, Stefansson K (2008) Sequence variants in the RNF212 gene associate with genomewide recombination rate. Science 319(5868):1398–1401
Kong X, Murphy K, Raj T, He C, White PS, Matise TC (2004) A combined linkage-physical map of the human genome. Am J Hum Genet 75:1143–1148
Kono T, Obata Y, Yoshimzu T, Nakahara T, Carroll J (1996) Epigenetic modifications during oocyte growth correlates with extended parthenogenetic development in the mouse. Nat Genet 13:91–94
Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131:839–849
Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, Hata K, Li E, Matsuda Y, Kimura T, Okabe M, Sakaki Y, Sasaki H, Nakano T (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22:908–917
La Salle S, Oakes CC, Neaga OR, Bourc’his D, Bestor TH, Trasler JM (2007) Loss of spermatogonia and wide-spread DNA methylation defects in newborn male mice deficient in DNMT3L. BMC Dev Biol 7:104
La Salle S, Trasler JM (2006) Dynamic expression of DNMT3a and DNMT3b isoforms during male germ cell development in the mouse. Dev Biol 296:71–82
Lenzi ML, Smith J, Snowden T, Kim M, Fishel R, Poulos BK, Cohen PE (2005) Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis I in human oocytes. Am J Hum Genet 76:112–127
Lercher MJ, Hurst LD (2003) Imprinted chromosomal regions of the human genome have unusually high recombination rates. Genetics 165:1629–1632
Li E, Bestor TH, Jaenisch R (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915–926
Lichten M (2008) Meiotic chromatin: the substrate for recombination initiation. In: Lankenau DK (ed) Genome dynamics and stability, vol 3. Springer, Berlin
Liu J, Wu TC, Lichten M (1995) The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO J 14:4599–4608
Lucifero D, Mertineit C, Clarke HJ, Bestor TH, Trasler JM (2002) Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79:530–538
Lynn A, Ashley T, Hassold T (2004) Variation in human meiotic recombination. Annu Rev Genomics Hum Genet 5:317–349
Lynn A, Koehler KE, Judis L, Chan ER, Cherry JP, Schwartz S, Seftel A, Hunt PA, Hassold TJ (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 6:6
Lynn A, Schrump S, Cherry J, Hassold T, Hunt P (2005) Sex, not genotype, determines recombination levels in mice. Am J Hum Genet 77:670–675
Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27:271–276
Maloisel L, Rossignol JL (1998) Suppression of crossing-over by DNA methylation in Ascobolus. Genes Dev 12:1381–1389
Marcon E, Moens P (2003) MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165:2283–2287
Martini E, Diaz RL, Hunter N, Keeney S (2006) Crossover homeostasis in yeast meiosis. Cell 126:285–295
Matise TC, Chen F, Chen W, De La Vega FM, Hansen M, He C, Hyland FC, Kennedy GC, Kong X, Murray SS, Ziegle JS, Stewart WC, Buyske S (2007) A second-generation combined linkage physical map of the human genome. Genome Res 17:1783–1786
McDougall A, Elliott JE, Hunter N (2005) Meeting report. EMBO Rep 6:120–125
McKittrick E, Gafken PR, Ahmad K, Henikoff S (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci USA 101:1525–1530
McVean GA, Myers SR, Hunt S, Deloukas P, Bentley DR, Donnelly P (2004) The fine-scale structure of recombination rate variation in the human genome. Science 304:581–584
Merker JD, Dominska M, Greenwell PW, Rinella E, Bouck DC, Shibata Y, Strahl BD, Mieczkowski P, Petes TD (2008) The histone methylase Set2p and the histone deacetylase Rpd3p repress meiotic recombination at the HIS4 meiotic recombination hotspot in Saccharomyces cerevisiae. DNA Repair (Amst) 7(8):1298–1308
Mets DG, Meyer BJ (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139:73–86
Mieczkowski PA, Dominska M, Buck MJ, Lieb JD, Petes TD (2007) Loss of a histone deacetylase dramatically alters the genomic distribution of Spo11p-catalyzed DNA breaks in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 104:3955–3960
Mihola O, Trachtulec Z, Vlcek C, Schimenti JC, Forejt J (2009) A mouse speciation gene encodes a meiotic histone H3 methyltransferase. Science 323:373–375
Miyamoto T, Koh E, Sakugawa N, Sato H, Hayashi H, Namiki M, Sengoku K (2008) Two single nucleotide polymorphisms in PRDM9 (MEISETZ) gene may be a genetic risk factor for Japanese patients with azoospermia by meiotic arrest. J Assist Reprod Genet 25:553–557
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
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 PRDM9 gene in meiotic recombination. Science 327(5967):876–879
Myers S, Freeman C, Auton A, Donnelly P, McVean G (2008) A common sequence motif associated with recombination hot spots and genome instability in humans. Nat Genet 40:1124–1129
Neumann R, Jeffreys AJ (2006) Polymorphism in the activity of human crossover hotspots independent of local DNA sequence variation. Hum Mol Genet 15:1401–1411
Ohta K, Shibata T, Nicolas A (1994) Changes in chromatin structure at recombination initiation sites during yeast meiosis. EMBO J 13:5754–5763
Okada Y, Scott G, Ray MK, Mishina Y, Zhang Y (2007) Histone demethylase JHDM2A is critical for Tnp1 and Prm1 transcription and spermatogenesis. Nature 450:119–123
Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257
Oliver PL, Goodstadt L, Bayes JJ, Birtle Z, Roach KC, Phadnis N, Beatson SA, Lunter G, Malik HS, Ponting CP (2009) Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet 5:e1000753
Paigen K, Szatkiewicz JP, Sawyer K, Leahy N, Parvanov ED, Ng SH, Graber JH, Broman KW, Petkov PM (2008) The recombinational anatomy of a mouse chromosome. PLoS Genet 4:e1000119
Paldi A, Gyapay G, Jami J (1995) Imprinted chromosomal regions of the human genome display sex-specific meiotic recombination frequencies. Curr Biol 5:1030–1035
Panning B, Jaenisch R (1996) DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev 10:1991–2002
Pardo-Manuel De Villena F, Sapienza C (2001) Recombination is proportional to the number of chromosome arms in mammals. Mamm Genome 12:318–322
Parvanov ED, Ng SH, Petkov PM, Paigen K (2009) Trans-regulation of mouse meiotic recombination hotspots by Rcr1. PLoS Biol 7:e36
Parvanov ED, Petkov PM, Paigen K (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327(5967):835
Peters AH, O’Carroll D, Scherthan H, Mechtler K, Sauer S, Schofer C, Weipoltshammer K, Pagani M, Lachner M, Kohlmaier A, Opravil S, Doyle M, Sibilia M, Jenuwein T (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337
Petes TD (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2:360–369
Petronczki M, Siomos MF, Nasmyth K (2003) Un Menage a Quatre. The molecular biology of chromosome segregation in meiosis. Cell 112:423–440
Phillips MS, Lawrence R, Sachidanandam R, Morris AP, Balding DJ, Donaldson MA, Studebaker JF, Ankener WM, Alfisi SV, Kuo FS, Camisa AL, Pazorov V, Scott KE, Carey BJ, Faith J, Katari G, Bhatti HA, Cyr JM, Derohannessian V, Elosua C, Forman AM, Grecco NM, Hock CR, Kuebler JM, Lathrop JA, Mockler MA, Nachtman EP, Restine SL, Varde SA, Hozza MJ, Gelfand CA, Broxholme J, Abecasis GR, Boyce-Jacino MT, Cardon LR (2003) Chromosome-wide distribution of haplotype blocks and the role of recombination hot spots. Nat Genet 33:382–387
Polo SE, Roche D, Almouzni G (2006) New histone incorporation marks sites of UV repair in human cells. Cell 127:481–493
Pradeepa MM, Rao MR (2007) Chromatin remodeling during mammalian spermatogenesis: role of testis specific histone variants and transition proteins. Soc Reprod Fertil Suppl 63:1–10
Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W (2002) Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 12:162–169
Riches LC, Lynch AM, Gooderham NJ (2008) Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 23:331–339
Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MH, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JT, Baarends WM, Bootsma D, Grootegoed JA, Hoeijmakers JH (1996) Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 86:799–810
Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–5868
Romanienko PJ, Camerini-Otero RD (2000) The mouse spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975–987
Sakai Y, Suetake I, Shinozaki F, Yamashina S, Tajima S (2004) Co-expression of de novo DNA methyltransferases Dnmt3a2 and Dnmt3L in gonocytes of mouse embryos. Gene Expr Patterns 5:231–237
Sandovici I, Kassovska-Bratinova S, Vaughan JE, Stewart R, Leppert M, Sapienza C (2006) Human imprinted chromosomal regions are historical hot-spots of recombination. PLoS Genet 2:e101
Schaefer M, Lyko F (2009) Solving the Dnmt2 enigma. Chromosoma 119(1):35–40
Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941–953
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
Sollier J, Lin W, Soustelle C, Suhre K, Nicolas A, Geli V, de La Roche Saint-Andre C (2004) Set1 is required for meiotic S-phase onset, double-strand break formation and middle gene expression. EMBO J 23:1957–1967
Soper SF, van der Heijden GW, Hardiman TC, Goodheart M, Martin SL, de Boer P, Bortvin A (2008) Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev Cell 15:285–297
Stumpf MP, McVean GA (2003) Estimating recombination rates from population-genetic data. Nat Rev Genet 4:959–968
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
Tachibana M, Nozaki M, Takeda N, Shinkai Y (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J 26:3346–3359
Tadokoro Y, Yomogida K, Yagura Y, Yamada S, Okabe M, Nishimune Y (2003) Characterization of histone H2A.X expression in testis and specific labeling of germ cells at the commitment stage of meiosis with histone H2A.X promoter-enhanced green fluorescent protein transgene. Biol Reprod 11:11
Tease C, Hartshorne GM, Hulten MA (2002) Patterns of meiotic recombination in human fetal oocytes. Am J Hum Genet 70:1469–1479
Trostle-Weige PK, Meistrich ML, Brock WA, Nishioka K (1984) Isolation and characterization of TH3, a germ cell-specific variant of histone 3 in rat testis. J Biol Chem 259:8769–8776
Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37:41–47
Unni E, Mayerhofer A, Zhang Y, Bhatnagar YM, Russell LD, Meistrich ML (1995) Increased accessibility of the N-terminus of testis-specific histone TH2B to antibodies in elongating spermatids. Mol Reprod Dev 42:210–219
Vergnaud G, Denoeud F (2000) Minisatellites: mutability and genome architecture. Genome Res 10:899–907
Vergnaud G, Mariat D, Apiou F, Aurias A, Lathrop M, Lauthier V (1991) The use of synthetic tandem repeats to isolate new VNTR loci: cloning of a human hypermutable sequence. Genomics 11:135–144
Walsh CP, Bestor TH (1999) Cytosine methylation and mammalian development. Genes Dev 13: 26–34
Walsh CP, Chaillet JR, Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20:116–117
Wang J, Scully K, Zhu X, Cai L, Zhang J, Prefontaine GG, Krones A, Ohgi KA, Zhu P, Garcia-Bassets I, Liu F, Taylor H, Lozach J, Jayes FL, Korach KS, Glass CK, Fu XD, Rosenfeld MG (2007) Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 446:882–887
Webster KE, O’Bryan MK, Fletcher S, Crewther PE, Aapola U, Craig J, Harrison DK, Aung H, Phutikanit N, Lyle R, Meachem SJ, Antonarakis SE, de Kretser DM, Hedger MP, Peterson P, Carroll BJ, Scott HS (2005) Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci USA 102:4068–4073
Westphal T, Reuter G (2002) Recombinogenic effects of suppressors of position-effect variegation in Drosophila. Genetics 160:609–621
Wu T-C, Lichten M (1994) Meiosis-induced double-strand break sites determined by yeast chromatin structure. Science 263:515–517
Xu D, Bai J, Duan Q, Costa M, Dai W (2009) Covalent modifications of histones during mitosis and meiosis. Cell Cycle 8(22):3688–3694
Yamada T, Mizuno KI, Hirota K, Kon N, Wahls WP, Hartsuiker E, Murofushi H, Shibata T, Ohta K (2004) Roles of histone acetylation and chromatin remodeling factor in a meiotic recombination hotspot. EMBO J 23:1792–1803
Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y (2006) JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125:483–495
Yamashita K, Shinohara M, Shinohara A (2004) Rad6-Bre1-mediated histone H2B ubiquitylation modulates the formation of double-strand breaks during meiosis. Proc Natl Acad Sci USA 101:11380–11385
Yoshida K, Yoshida SH, Shimoda C, Morita T (2003) Expression and radiation-induced phosphorylation of histone H2AX in mammalian cells. J Radiat Res (Tokyo) 44:47–51
Zalensky AO, Siino JS, Gineitis AA, Zalenskaya IA, Tomilin NV, Yau P, Bradbury EM (2002) Human testis/sperm-specific histone H2B (hTSH2B). Molecular cloning and characterization. J Biol Chem 277:43474–43480
Zamudio NM, Chong S, O’Bryan MK (2008) Epigenetic regulation in male germ cells. Reproduction 136:131–146
Zhang Y, Kwon S, Yamaguchi T, Cubizolles F, Rousseaux S, Kneissel M, Cao C, Li N, Cheng HL, Chua K, Lombard D, Mizeracki A, Matthias G, Alt FW, Khochbin S, Matthias P (2008) Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol Cell Biol 28:1688–1701
Acknowledgments
We thank F. Baudat and C. Grey for discussions and comments on the manuscript. P. B is supported by a PhD grant from the French MENRT. This work was funded by grants from CNRS, EDF, ANR-06-BLAN-0160-01, ANR-09-BLAN-0269-01, and ARC3939 to BdM.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Berlin Heidelberg
About this chapter
Cite this chapter
Barthès, P., Buard, J., de Massy, B. (2011). Epigenetic Factors and Regulation of Meiotic Recombination in Mammals. In: Rousseaux, S., Khochbin, S. (eds) Epigenetics and Human Reproduction. Epigenetics and Human Health. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-14773-9_6
Download citation
DOI: https://doi.org/10.1007/978-3-642-14773-9_6
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-14772-2
Online ISBN: 978-3-642-14773-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)