{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,27]],"date-time":"2026-08-27T10:37:05Z","timestamp":1787827025316,"version":"build-2784847793"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2015,12,28]],"date-time":"2015-12-28T00:00:00Z","timestamp":1451260800000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100000265","name":"Medical Research Council (GB)","doi-asserted-by":"publisher","award":["U117588498"],"award-info":[{"award-number":["U117588498"]}],"id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Chromosoma"],"published-print":{"date-parts":[[2016,6]]},"DOI":"10.1007\/s00412-015-0568-z","type":"journal-article","created":{"date-parts":[[2015,12,28]],"date-time":"2015-12-28T05:08:10Z","timestamp":1451279290000},"page":"215-226","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Mammalian meiotic silencing exhibits sexually dimorphic features"],"prefix":"10.1007","volume":"125","author":[{"given":"J. M.","family":"Cloutier","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. K.","family":"Mahadevaiah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E.","family":"ElInati","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A.","family":"T\u00f3th","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James","family":"Turner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2015,12,28]]},"reference":[{"key":"568_CR1","first-page":"67","volume-title":"Handbook of experimental pharmacology","author":"AP Arnold","year":"2012","unstructured":"Arnold AP, Chen X, Itoh Y (2012) What a difference an X or Y makes: sex chromosomes, gene dose, and epigenetics in sexual differentiation. In: Handbook of experimental pharmacology., pp 67\u201388"},{"key":"568_CR2","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1128\/MCB.25.3.1041-1053.2005","volume":"25","author":"WM Baarends","year":"2005","unstructured":"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\u20131053","journal-title":"Mol Cell Biol"},{"key":"568_CR3","doi-asserted-by":"crossref","first-page":"e1003435","DOI":"10.1371\/journal.pgen.1003435","volume":"9","author":"OJ Becherel","year":"2013","unstructured":"Becherel OJ, Yeo AJ, Stellati A, Heng EY, Luff J, Suraweera AM, Woods R, Fleming J, Carrie D, McKinney K, Xu X, Deng C, Lavin MF (2013) Senataxin plays an essential role with DNA damage response proteins in meiotic recombination and gene silencing. PLoS Genet 9:e1003435","journal-title":"PLoS Genet"},{"key":"568_CR4","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1530\/jrf.0.0750633","volume":"75","author":"PS Burgoyne","year":"1985","unstructured":"Burgoyne PS, Baker TG (1985) Perinatal oocyte loss in XO mice and its implications for the aetiology of gonadal dysgenesis in XO women. J Reprod Fertil 75:633\u2013645","journal-title":"J Reprod Fertil"},{"key":"568_CR5","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1439-0272.1992.tb02602.x","volume":"24","author":"PS Burgoyne","year":"1992","unstructured":"Burgoyne PS, Sutcliffe MJ, Mahadevaiah SK (1992) The role of unpaired sex chromosomes in spermatogenic failure. Andrologia 24:17\u201320","journal-title":"Andrologia"},{"key":"568_CR6","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nrg2505","volume":"10","author":"PS Burgoyne","year":"2009","unstructured":"Burgoyne PS, Mahadevaiah SK, Turner JM (2009) The consequences of asynapsis for mammalian meiosis. Nat Rev Genet 10:207\u2013216","journal-title":"Nat Rev Genet"},{"key":"568_CR7","doi-asserted-by":"crossref","first-page":"922","DOI":"10.1126\/science.1069398","volume":"296","author":"A Celeste","year":"2002","unstructured":"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\u2013927","journal-title":"Science"},{"key":"568_CR8","doi-asserted-by":"crossref","unstructured":"Cloutier JM, Mahadevaiah SK, ElInati E, Nussenzweig A, Toth A, Turner JM (2015) Histone H2AFX links meiotic chromosome asynapsis to prophase I oocyte loss in mammals. PLoS Genet 11:e1005462","DOI":"10.1371\/journal.pgen.1005462"},{"key":"568_CR9","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1038\/ncb2213","volume":"13","author":"K Daniel","year":"2011","unstructured":"Daniel K, Lange J, Hached K, Fu J, Anastassiadis K, Roig I, Cooke HJ, Stewart AF, Wassmann K, Jasin M, Keeney S, Toth A (2011) Meiotic homologue alignment and its quality surveillance are controlled by mouse HORMAD1. Nat Cell Biol 13:599\u2013610","journal-title":"Nat Cell Biol"},{"key":"568_CR10","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1159\/000133152","volume":"57","author":"EM Eicher","year":"1991","unstructured":"Eicher EM, Hale DW, Hunt PA, Lee BK, Tucker PK, King TR, Eppig JT, Washburn LL (1991) The mouse Y* chromosome involves a complex rearrangement, including interstitial positioning of the pseudoautosomal region. Cytogenet Cell Genet 57:221\u2013230","journal-title":"Cytogenet Cell Genet"},{"key":"568_CR11","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.yexcr.2009.08.007","volume":"316","author":"T Fukuda","year":"2010","unstructured":"Fukuda T, Daniel K, Wojtasz L, Toth A, Hoog C (2010) A novel mammalian HORMA domain-containing protein, HORMAD1, preferentially associates with unsynapsed meiotic chromosomes. Exp Cell Res 316:158\u2013171","journal-title":"Exp Cell Res"},{"key":"568_CR12","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/S1472-6483(10)60422-1","volume":"18","author":"R Garcia-Cruz","year":"2009","unstructured":"Garcia-Cruz R, Roig I, Robles P, Scherthan H, Garcia Caldes M (2009) ATR, BRCA1 and gammaH2AX localize to unsynapsed chromosomes at the pachytene stage in human oocytes. Reprod Biomed Online 18:37\u201344","journal-title":"Reprod Biomed Online"},{"key":"568_CR13","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1038\/nrg2723","volume":"11","author":"MA Handel","year":"2010","unstructured":"Handel MA, Schimenti JC (2010) Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat Rev Genet 11:124\u2013136","journal-title":"Nat Rev Genet"},{"key":"568_CR14","doi-asserted-by":"crossref","first-page":"2181","DOI":"10.1126\/science.1071907","volume":"296","author":"PA Hunt","year":"2002","unstructured":"Hunt PA, Hassold TJ (2002) Sex matters in meiosis. Science 296:2181\u20132183","journal-title":"Science"},{"key":"568_CR15","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1101\/gad.2030811","volume":"25","author":"Y Ichijima","year":"2011","unstructured":"Ichijima Y, Ichijima M, Lou Z, Nussenzweig A, Camerini-Otero RD, Chen J, Andreassen PR, Namekawa SH (2011) MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cells. Genes Dev 25:959\u2013971","journal-title":"Genes Dev"},{"key":"568_CR16","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1159\/000078188","volume":"105","author":"NK Kolas","year":"2004","unstructured":"Kolas NK, Yuan L, Hoog C, Heng HH, Marcon E, Moens PB (2004) Male mouse meiotic chromosome cores deficient in structural proteins SYCP3 and SYCP2 align by homology but fail to synapse and have possible impaired specificity of chromatin loop attachment. Cytogenet Genome Res 105:182\u2013188","journal-title":"Cytogenet Genome Res"},{"key":"568_CR17","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1038\/ng2065","volume":"39","author":"A Kouznetsova","year":"2007","unstructured":"Kouznetsova A, Lister L, Nordenskjold M, Herbert M, Hoog C (2007) Bi-orientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat Genet 39:966\u2013968","journal-title":"Nat Genet"},{"key":"568_CR18","doi-asserted-by":"crossref","first-page":"2446","DOI":"10.1242\/jcs.049353","volume":"122","author":"A Kouznetsova","year":"2009","unstructured":"Kouznetsova A, Wang H, Bellani M, Camerini-Otero RD, Jessberger R, Hoog C (2009) BRCA1-mediated chromatin silencing is limited to oocytes with a small number of asynapsed chromosomes. J Cell Sci 122:2446\u20132452","journal-title":"J Cell Sci"},{"key":"568_CR19","doi-asserted-by":"crossref","first-page":"1611","DOI":"10.1083\/jcb.139.7.1611","volume":"139","author":"R LeMaire-Adkins","year":"1997","unstructured":"LeMaire-Adkins R, Radke K, Hunt PA (1997) Lack of checkpoint control at the metaphase\/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J Cell Biol 139:1611\u20131619","journal-title":"J Cell Biol"},{"key":"568_CR20","doi-asserted-by":"crossref","first-page":"2275","DOI":"10.1242\/dev.124.11.2275","volume":"124","author":"SW Luoh","year":"1997","unstructured":"Luoh SW, Bain PA, Polakiewicz RD, Goodheart ML, Gardner H, Jaenisch R, Page DC (1997) Zfx mutation results in small animal size and reduced germ cell number in male and female mice. Development 124:2275\u20132284","journal-title":"Development"},{"key":"568_CR21","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1093\/hmg\/7.4.715","volume":"7","author":"SK Mahadevaiah","year":"1998","unstructured":"Mahadevaiah SK, Odorisio T, Elliott DJ, Rattigan A, Szot M, Laval SH, Washburn LL, McCarrey JR, Cattanach BM, Lovell-Badge R, Burgoyne PS (1998) Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids, and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities. Hum Mol Genet 7:715\u2013727","journal-title":"Hum Mol Genet"},{"key":"568_CR22","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1083\/jcb.200710195","volume":"182","author":"SK Mahadevaiah","year":"2008","unstructured":"Mahadevaiah SK, Bourc\u2019his D, de Rooij DG, Bestor TH, Turner JM, Burgoyne PS (2008) Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. J Cell Biol 182:263\u2013276","journal-title":"J Cell Biol"},{"key":"568_CR23","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1007\/978-1-60761-103-5_25","volume":"558","author":"SK Mahadevaiah","year":"2009","unstructured":"Mahadevaiah SK, Costa Y, Turner JM (2009) Using RNA FISH to study gene expression during mammalian meiosis. Methods Mol Biol 558:433\u2013444","journal-title":"Methods Mol Biol"},{"key":"568_CR24","doi-asserted-by":"crossref","first-page":"e1000625","DOI":"10.1371\/journal.pgen.1000625","volume":"5","author":"M Manterola","year":"2009","unstructured":"Manterola M, Page J, Vasco C, Berrios S, Parra MT, Viera A, Rufas JS, Zuccotti M, Garagna S, Fernandez-Donoso R (2009) A high incidence of meiotic silencing of unsynapsed chromatin is not associated with substantial pachytene loss in heterozygous male mice carrying multiple simple robertsonian translocations. PLoS Genet 5:e1000625","journal-title":"PLoS Genet"},{"key":"568_CR25","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/BF00356023","volume":"102","author":"BD McKee","year":"1993","unstructured":"McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin conformation. Chromosoma 102:71\u201380","journal-title":"Chromosoma"},{"key":"568_CR26","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.devcel.2012.07.003","volume":"23","author":"AJ Modzelewski","year":"2012","unstructured":"Modzelewski AJ, Holmes RJ, Hilz S, Grimson A, Cohen PE (2012) AGO4 regulates entry into meiosis and influences silencing of sex chromosomes in the male mouse germline. Dev Cell 23:251\u2013264","journal-title":"Dev Cell"},{"key":"568_CR27","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1530\/rep.1.00865","volume":"130","author":"MA Morelli","year":"2005","unstructured":"Morelli MA, Cohen PE (2005) Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130:761\u2013781","journal-title":"Reproduction"},{"key":"568_CR28","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1016\/j.cub.2011.03.003","volume":"21","author":"SI Nagaoka","year":"2011","unstructured":"Nagaoka SI, Hodges CA, Albertini DF, Hunt PA (2011) Oocyte-specific differences in cell-cycle control create an innate susceptibility to meiotic errors. Curr Biol 21:651\u2013657","journal-title":"Curr Biol"},{"key":"568_CR29","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1038\/nrg3245","volume":"13","author":"SI Nagaoka","year":"2012","unstructured":"Nagaoka SI, Hassold TJ, Hunt PA (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13:493\u2013504","journal-title":"Nat Rev Genet"},{"key":"568_CR30","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1126\/science.1114535","volume":"309","author":"A O\u2019Doherty","year":"2005","unstructured":"O\u2019Doherty A, Ruf S, Mulligan C, Hildreth V, Errington ML, Cooke S, Sesay A, Modino S, Vanes L, Hernandez D, Linehan JM, Sharpe PT, Brandner S, Bliss TV, Henderson DJ, Nizetic D, Tybulewicz VL, Fisher EM (2005) An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science 309:2033\u20132037","journal-title":"Science"},{"key":"568_CR31","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/s00412-004-0311-7","volume":"113","author":"RS Rogers","year":"2004","unstructured":"Rogers RS, Inselman A, Handel MA, Matunis MJ (2004) SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 113:233\u2013243","journal-title":"Chromosoma"},{"key":"568_CR32","doi-asserted-by":"crossref","first-page":"2117","DOI":"10.1016\/j.cub.2010.11.010","volume":"20","author":"H Royo","year":"2010","unstructured":"Royo H, Polikiewicz G, Mahadevaiah SK, Prosser H, Mitchell M, Bradley A, de Rooij DG, Burgoyne PS, Turner JM (2010) Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr Biol 20:2117\u20132123","journal-title":"Curr Biol"},{"key":"568_CR33","doi-asserted-by":"crossref","first-page":"1484","DOI":"10.1101\/gad.219477.113","volume":"27","author":"H Royo","year":"2013","unstructured":"Royo H, Prosser H, Ruzankina Y, Mahadevaiah SK, Cloutier JM, Baumann M, Fukuda T, Hoog C, Toth A, de Rooij DG, Bradley A, Brown EJ, Turner JM (2013) ATR acts stage specifically to regulate multiple aspects of mammalian meiotic silencing. Genes Dev 27:1484\u20131494","journal-title":"Genes Dev"},{"key":"568_CR34","doi-asserted-by":"crossref","unstructured":"Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F, Wang PJ, Meistrich ML, Rajkovic A (2010) Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet 6:e1001190","DOI":"10.1371\/journal.pgen.1001190"},{"key":"568_CR35","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1007\/s00412-013-0415-z","volume":"122","author":"T Taketo","year":"2013","unstructured":"Taketo T, Naumova AK (2013) Oocyte heterogeneity with respect to the meiotic silencing of unsynapsed X chromosomes in the XY female mouse. Chromosoma 122:337\u2013349","journal-title":"Chromosoma"},{"key":"568_CR36","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1016\/j.cub.2004.11.032","volume":"14","author":"JM Turner","year":"2004","unstructured":"Turner JM, Aprelikova O, Xu X, Wang R, Kim S, Chandramouli GV, Barrett JC, Burgoyne PS, Deng CX (2004) BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14:2135\u20132142","journal-title":"Curr Biol"},{"key":"568_CR37","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/ng1484","volume":"37","author":"JM Turner","year":"2005","unstructured":"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\u201347","journal-title":"Nat Genet"},{"key":"568_CR38","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1016\/j.cub.2011.03.057","volume":"21","author":"N Vernet","year":"2011","unstructured":"Vernet N, Mahadevaiah SK, Ojarikre OA, Longepied G, Prosser HM, Bradley A, Mitchell MJ, Burgoyne PS (2011) The Y-encoded gene zfy2 acts to remove cells with unpaired chromosomes at the first meiotic metaphase in male mice. Curr Biol 21:787\u2013793","journal-title":"Curr Biol"},{"key":"568_CR39","doi-asserted-by":"crossref","first-page":"480","DOI":"10.1016\/j.ydbio.2005.03.034","volume":"282","author":"M Vigodner","year":"2005","unstructured":"Vigodner M, Morris PL (2005) Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in spermatogenesis: silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping. Dev Biol 282:480\u2013492","journal-title":"Dev Biol"},{"key":"568_CR40","doi-asserted-by":"crossref","unstructured":"Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, Eckmann CR, Cooke HJ, Jasin M, Keeney S, McKay MJ, Toth A (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5:e1000702","DOI":"10.1371\/journal.pgen.1000702"},{"key":"568_CR41","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1101\/gad.187559.112","volume":"26","author":"L Wojtasz","year":"2012","unstructured":"Wojtasz L, Cloutier JM, Baumann M, Daniel K, Varga J, Fu J, Anastassiadis K, Stewart AF, Remenyi A, Turner JM, Toth A (2012) Meiotic DNA double-strand breaks and chromosome asynapsis in mice are monitored by distinct HORMAD2-independent and -dependent mechanisms. Genes Dev 26:958\u2013973","journal-title":"Genes Dev"}],"container-title":["Chromosoma"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00412-015-0568-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00412-015-0568-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00412-015-0568-z","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,30]],"date-time":"2022-05-30T20:23:39Z","timestamp":1653942219000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00412-015-0568-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,12,28]]},"references-count":41,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2016,6]]}},"alternative-id":["568"],"URL":"https:\/\/doi.org\/10.1007\/s00412-015-0568-z","relation":{},"ISSN":["0009-5915","1432-0886"],"issn-type":[{"value":"0009-5915","type":"print"},{"value":"1432-0886","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,12,28]]}}}