{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T18:38:28Z","timestamp":1791225508613,"version":"4.1.0"},"reference-count":70,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2015,4,18]],"date-time":"2015-04-18T00:00:00Z","timestamp":1429315200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Chromosoma"],"published-print":{"date-parts":[[2015,9]]},"DOI":"10.1007\/s00412-015-0511-3","type":"journal-article","created":{"date-parts":[[2015,4,17]],"date-time":"2015-04-17T03:37:14Z","timestamp":1429241834000},"page":"397-415","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":65,"title":["Nuclear localization of PRDM9 and its role in meiotic chromatin modifications and homologous synapsis"],"prefix":"10.1007","volume":"124","author":[{"given":"Fengyun","family":"Sun","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yasuhiro","family":"Fujiwara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura G.","family":"Reinholdt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianjun","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruth L.","family":"Saxl","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher L.","family":"Baker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petko M.","family":"Petkov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenneth","family":"Paigen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mary Ann","family":"Handel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2015,4,18]]},"reference":[{"key":"511_CR1","doi-asserted-by":"crossref","first-page":"14976","DOI":"10.1073\/pnas.0807297105","volume":"105","author":"EL Anderson","year":"2008","unstructured":"Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM, Page DC (2008) Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci U S A 105:14976\u201314980","journal-title":"Proc Natl Acad Sci U S A"},{"key":"511_CR2","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/BF00352222","volume":"104","author":"T Ashley","year":"1995","unstructured":"Ashley T, Plug AW, Xu JH, Solari AJ, Reddy G, Golub EI, Ward DC (1995) Dynamic changes in Rad51 distribution on chromatin during meiosis in male and female vertebrates. Chromosoma 104:19\u201328","journal-title":"Chromosoma"},{"key":"511_CR3","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 HJ, 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":"511_CR4","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1101\/gr.170167.113","volume":"24","author":"CL Baker","year":"2014","unstructured":"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\u2013732","journal-title":"Genome Res"},{"key":"511_CR5","doi-asserted-by":"crossref","first-page":"e105","DOI":"10.1371\/journal.pbio.0050105","volume":"5","author":"L Bannister","year":"2007","unstructured":"Bannister L, Pezza R, Donaldson J, de Rooij DG, Schimenti K, Camerini-Otero RD, Schimenti JC (2007) Male-specific sterility in mice carrying a dominant, recombination-defective allele of the RecA homolog Dmc1. PLoS Biol 5:e105","journal-title":"PLoS Biol"},{"key":"511_CR6","doi-asserted-by":"crossref","first-page":"7203","DOI":"10.1128\/MCB.25.16.7203-7215.2005","volume":"25","author":"M Barchi","year":"2005","unstructured":"Barchi M, Mahadevaiah S, Di Giacomo M, Baudat F, de Rooij DG, Burgoyne PS, Jasin M, Keeney S (2005) Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol Cell Biol 25:7203\u20137215","journal-title":"Mol Cell Biol"},{"key":"511_CR7","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1016\/S1097-2765(00)00098-8","volume":"6","author":"F Baudat","year":"2000","unstructured":"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\u2013998","journal-title":"Mol Cell"},{"key":"511_CR8","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1126\/science.1183439","volume":"327","author":"F Baudat","year":"2010","unstructured":"Baudat F, Buard J, 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\u2013840","journal-title":"Science"},{"key":"511_CR9","doi-asserted-by":"crossref","first-page":"794","DOI":"10.1038\/nrg3573","volume":"14","author":"F Baudat","year":"2013","unstructured":"Baudat F, Imai Y, de Massy B (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14:794\u2013806","journal-title":"Nat Rev Genet"},{"key":"511_CR10","doi-asserted-by":"crossref","first-page":"E468","DOI":"10.1073\/pnas.1219126110","volume":"110","author":"T Bhattacharyya","year":"2013","unstructured":"Bhattacharyya T, Gregorova S, Mihola O, Anger M, Sebestova J, Denny P, Simecek P, Forejt J (2013) Mechanistic basis of infertility of mouse intersubspecific hybrids. Proc Natl Acad Sci U S A 110:E468\u2013E477","journal-title":"Proc Natl Acad Sci U S A"},{"key":"511_CR11","doi-asserted-by":"crossref","first-page":"e1004088","DOI":"10.1371\/journal.pgen.1004088","volume":"10","author":"T Bhattacharyya","year":"2014","unstructured":"Bhattacharyya T, Reifova R, Gregorova S, Simecek P, Gergelits V, Mistrik M, Martincova I, Pialek J, Forejt J (2014) X chromosome control of meiotic chromosome synapsis in mouse inter-subspecific hybrids. PLoS Genet 10:e1004088","journal-title":"PLoS Genet"},{"key":"511_CR12","doi-asserted-by":"crossref","first-page":"R35","DOI":"10.1186\/gb-2013-14-4-r35","volume":"14","author":"T Billings","year":"2013","unstructured":"Billings T, Parvanov ED, Baker CL, Walker M, Paigen K, Petkov PM (2013) DNA binding specificities of the long zinc-finger recombination protein PRDM9. Genome Biol 14:R35","journal-title":"Genome Biol"},{"key":"511_CR13","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.devcel.2012.12.002","volume":"24","author":"KA Boateng","year":"2013","unstructured":"Boateng KA, Bellani MA, Gregoretti IV, Pratto F, Camerini-Otero RD (2013) Homologous pairing preceding SPO11-mediated double-strand breaks in mice. Dev Cell 24:196\u2013205","journal-title":"Dev Cell"},{"key":"511_CR14","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/B978-0-12-394309-5.00005-5","volume":"298","author":"E Bolcun-Filas","year":"2012","unstructured":"Bolcun-Filas E, Schimenti JC (2012) Genetics of meiosis and recombination in mice. Int Rev Cell Mol Biol 298:179\u2013227","journal-title":"Int Rev Cell Mol Biol"},{"key":"511_CR15","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.gde.2012.12.002","volume":"23","author":"V Borde","year":"2013","unstructured":"Borde V, de Massy B (2013) Programmed induction of DNA double strand breaks during meiosis: setting up communication between DNA and the chromosome structure. Curr Opin Genet Dev 23:147\u2013155","journal-title":"Curr Opin Genet Dev"},{"key":"511_CR16","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1038\/nature11089","volume":"485","author":"K Brick","year":"2012","unstructured":"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\u2013645","journal-title":"Nature"},{"key":"511_CR17","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1038\/ng1366","volume":"36","author":"FW Buaas","year":"2004","unstructured":"Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE (2004) Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 36:647\u2013652","journal-title":"Nat Genet"},{"key":"511_CR18","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":"511_CR19","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1677\/jme.0.0250169","volume":"25","author":"SA Bustin","year":"2000","unstructured":"Bustin SA (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25:169\u2013193","journal-title":"J Mol Endocrinol"},{"key":"511_CR20","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1002\/(SICI)1098-2795(199704)46:4<489::AID-MRD7>3.0.CO;2-K","volume":"46","author":"J Cobb","year":"1997","unstructured":"Cobb J, Reddy RK, Park C, Handel MA (1997) Analysis of expression and function of topoisomerase I and II during meiosis in male mice. Mol Reprod Dev 46:489\u2013498","journal-title":"Mol Reprod Dev"},{"key":"511_CR21","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1006\/dbio.1998.9101","volume":"205","author":"J Cobb","year":"1999","unstructured":"Cobb J, Cargile B, Handel MA (1999) Acquisition of competence to condense metaphase I chromosomes during spermatogenesis. Dev Biol 205:49\u201364","journal-title":"Dev Biol"},{"key":"511_CR22","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1210\/er.2005-0017","volume":"27","author":"PE Cohen","year":"2006","unstructured":"Cohen PE, Pollack SE, Pollard JW (2006) Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr Rev 27:398\u2013426","journal-title":"Endocr Rev"},{"key":"511_CR23","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":"511_CR24","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1146\/annurev-genet-110711-155423","volume":"47","author":"B Massy de","year":"2013","unstructured":"de Massy B (2013) Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet 47:563\u2013599","journal-title":"Annu Rev Genet"},{"key":"511_CR25","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1101\/gad.329705","volume":"19","author":"FA Vries de","year":"2005","unstructured":"de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu JG, van Zeeland AA, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376\u20131389","journal-title":"Genes Dev"},{"key":"511_CR26","doi-asserted-by":"crossref","first-page":"2953","DOI":"10.1242\/jcs.114.16.2953","volume":"114","author":"S Eaker","year":"2001","unstructured":"Eaker S, Pyle A, Cobb J, Handel MA (2001) Evidence for meiotic spindle checkpoint from analysis of spermatocytes from Robertsonian-chromosome heterozygous mice. J Cell Sci 114:2953\u20132965","journal-title":"J Cell Sci"},{"key":"511_CR27","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1083\/jcb.200212080","volume":"160","author":"M Eijpe","year":"2003","unstructured":"Eijpe M, Offenberg H, Jessberger R, Revenkova E, Heyting C (2003) Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1 beta and SMC3. J Cell Biol 160:657\u2013670","journal-title":"J Cell Biol"},{"key":"511_CR28","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1095\/biolreprod.112.107110","volume":"88","author":"Y Fujiwara","year":"2013","unstructured":"Fujiwara Y, Ogonuki N, Inoue K, Ogura A, Handel MA, Noguchi J, Kunieda T (2013) t-SNARE Syntaxin2 (STX2) is implicated in intracellular transport of sulfoglycolipids during meiotic prophase in mouse spermatogenesis. Biol Reprod 88:141","journal-title":"Biol Reprod"},{"key":"511_CR29","doi-asserted-by":"crossref","first-page":"1243","DOI":"10.1002\/embj.201387329","volume":"33","author":"T Fukuda","year":"2014","unstructured":"Fukuda T, Fukuda N, Agostinho A, Hernandez-Hernandez A, Kouznetsova A, Hoog C (2014) STAG3-mediated stabilization of REC8 cohesin complexes promotes chromosome synapsis during meiosis. EMBO J 33:1243\u20131255","journal-title":"EMBO J"},{"key":"511_CR30","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.4161\/cc.10.9.15515","volume":"10","author":"C Gutierrez-Caballero","year":"2011","unstructured":"Gutierrez-Caballero C, Herran Y, Sanchez-Martin M, Suja JA, Barbero JL, Llano E, Pendas AM (2011) Identification and molecular characterization of the mammalian alpha-kleisin RAD21L. Cell Cycle 10:1477\u20131487","journal-title":"Cell Cycle"},{"key":"511_CR31","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":"511_CR32","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.mce.2005.12.046","volume":"250","author":"MA Handel","year":"2006","unstructured":"Handel MA, Lessard C, Reinholdt L, Schimenti J, Eppig JJ (2006) Mutagenesis as an unbiased approach to identify novel contraceptive targets. Mol Cell Endocrinol 250:201\u2013205","journal-title":"Mol Cell Endocrinol"},{"key":"511_CR33","doi-asserted-by":"crossref","first-page":"615","DOI":"10.4161\/cc.5.6.2572","volume":"5","author":"K Hayashi","year":"2006","unstructured":"Hayashi K, Matsui Y (2006) Meisetz, a novel histone tri-methyltransferase, regulates meiosis-specific epigenesis. Cell Cycle 5:615\u2013620","journal-title":"Cell Cycle"},{"key":"511_CR34","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1038\/nature04112","volume":"438","author":"K Hayashi","year":"2005","unstructured":"Hayashi K, Yoshida K, Matsui Y (2005) A histone H3 methyltransferase controls epigenetic events required for meiotic prophase. Nature 438:374\u2013378","journal-title":"Nature"},{"key":"511_CR35","doi-asserted-by":"crossref","first-page":"3091","DOI":"10.1038\/emboj.2011.222","volume":"30","author":"Y Herran","year":"2011","unstructured":"Herran Y, Gutierrez-Caballero C, Sanchez-Martin M, Hernandez T, Viera A, Barbero JL, de Alava E, de Rooij DG, Suja JA, Llano E, Pendas AM (2011) The cohesin subunit RAD21L functions in meiotic synapsis and exhibits sexual dimorphism in fertility. EMBO J 30:3091\u20133105","journal-title":"EMBO J"},{"key":"511_CR36","doi-asserted-by":"crossref","first-page":"e1004413","DOI":"10.1371\/journal.pgen.1004413","volume":"10","author":"J Hopkins","year":"2014","unstructured":"Hopkins J, Hwang G, Jacob J, Sapp N, Bedigian R, Oka K, Overbeek P, Murray S, Jordan PW (2014) Meiosis-specific cohesin component, Stag3 is essential for maintaining centromere chromatid cohesion, and required for DNA repair and synapsis between homologous chromosomes. PLoS Genet 10:e1004413","journal-title":"PLoS Genet"},{"key":"511_CR37","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":"511_CR38","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1038\/embor.2011.2","volume":"12","author":"K Ishiguro","year":"2011","unstructured":"Ishiguro K, Kim J, Fujiyama-Nakamura S, Kato S, Watanabe Y (2011) A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing. EMBO Rep 12:267\u2013275","journal-title":"EMBO Rep"},{"key":"511_CR39","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1083\/jcb.200810107","volume":"186","author":"H Jin","year":"2009","unstructured":"Jin H, Guacci V, Yu HG (2009) Pds5 is required for homologue pairing and inhibits synapsis of sister chromatids during yeast meiosis. J Cell Biol 186:713\u2013725","journal-title":"J Cell Biol"},{"key":"511_CR40","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1101\/gad.213652.113","volume":"27","author":"L Kauppi","year":"2013","unstructured":"Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27:873\u2013886","journal-title":"Genes Dev"},{"key":"511_CR41","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1038\/nmeth1204-249","volume":"1","author":"N Kotaja","year":"2004","unstructured":"Kotaja N, Kimmins S, Brancorsini S, Hentsch D, Vonesch J-L, Davidson I, Parvinen M, Sassone-Corsi P (2004) Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1:249\u2013254","journal-title":"Nat Methods"},{"key":"511_CR42","doi-asserted-by":"crossref","first-page":"e1004541","DOI":"10.1371\/journal.pgen.1004541","volume":"10","author":"J Koubova","year":"2014","unstructured":"Koubova J, Hu YC, Bhattacharyya T, Soh YQ, Gill ME, Goodheart ML, Hogarth CA, Griswold MD, Page DC (2014) Retinoic acid activates two pathways required for meiosis in mice. PLoS Genet 10:e1004541","journal-title":"PLoS Genet"},{"key":"511_CR43","doi-asserted-by":"crossref","unstructured":"La Salle S, Sun F, Handel MA (2009) Isolation and short-term culture of mouse spermatocytes for analysis of meiosis. In: Keeney S (ed) Methods in molecular biology, molecular medicine and biotechnology: Meiosis Protocols Humana Press, pp 279\u2013297","DOI":"10.1007\/978-1-60761-103-5_17"},{"key":"511_CR44","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1083\/jcb.201201100","volume":"197","author":"E Llano","year":"2012","unstructured":"Llano E, Herran Y, Garcia-Tunon I, Gutierrez-Caballero C, de Alava E, Barbero JL, Schimenti J, de Rooij DG, Sanchez-Martin M, Pendas AM (2012) Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol 197:877\u2013885","journal-title":"J Cell Biol"},{"key":"511_CR45","doi-asserted-by":"crossref","first-page":"3421","DOI":"10.1093\/hmg\/ddu051","volume":"23","author":"E Llano","year":"2014","unstructured":"Llano E, Gomez HL, Garcia-Tunon I, Sanchez-Martin M, Caburet S, Barbero JL, Schimenti JC, Veitia RA, Pendas AM (2014) STAG3 is a strong candidate gene for male infertility. Hum Mol Genet 23:3421\u20133431","journal-title":"Hum Mol Genet"},{"key":"511_CR46","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1038\/85830","volume":"27","author":"SK Mahadevaiah","year":"2001","unstructured":"Mahadevaiah SK, Turner JMA, 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\u2013276","journal-title":"Nat Genet"},{"key":"511_CR47","doi-asserted-by":"crossref","first-page":"1668","DOI":"10.1016\/j.bbamcr.2011.03.008","volume":"1813","author":"AT Major","year":"2011","unstructured":"Major AT, Whiley PA, Loveland KL (2011) Expression of nucleocytoplasmic transport machinery: clues to regulation of spermatogenic development. Biochim Biophys Acta 1813:1668\u20131688","journal-title":"Biochim Biophys Acta"},{"key":"511_CR48","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1083\/jcb.200706136","volume":"180","author":"I Novak","year":"2008","unstructured":"Novak I, Wang H, Revenkova E, Jessberger R, Scherthan H, Hoog C (2008) Cohesin Smc1beta determines meiotic chromatin axis loop organization. J Cell Biol 180:83\u201390","journal-title":"J Cell Biol"},{"key":"511_CR49","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/nrg2712","volume":"11","author":"K Paigen","year":"2010","unstructured":"Paigen K, Petkov P (2010) Mammalian recombination hot spots: properties, control and evolution. Nat Rev Genet 11:221\u2013233","journal-title":"Nat Rev Genet"},{"key":"511_CR50","doi-asserted-by":"crossref","first-page":"835","DOI":"10.1126\/science.1181495","volume":"327","author":"ED Parvanov","year":"2010","unstructured":"Parvanov ED, Petkov PM, Paigen K (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327:835","journal-title":"Science"},{"key":"511_CR51","first-page":"142","volume-title":"Methods toxicol","author":"M Parvinen","year":"1993","unstructured":"Parvinen M, Toppari J, Lahdetie J (1993) Transillumination phase contrast microscope techniques for evaluation of male germ cell toxicity and mutagenicity. In: Heindel JJ (ed) Methods toxicol. Academic, San Diego, pp 142\u2013165"},{"key":"511_CR52","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1023\/A:1018445520117","volume":"5","author":"AHFM Peters","year":"1997","unstructured":"Peters AHFM, 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. Chromosom Res 5:66\u201371","journal-title":"Chromosom Res"},{"key":"511_CR53","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1096\/fasebj.14.3.581","volume":"14","author":"N Pezzi","year":"2000","unstructured":"Pezzi N, Prieto I, Kremer L, Jurado LAP, Valero C, Del Mazo J, Martinez C, Barbero JL (2000) STAG3, a novel gene encoding a protein involved in meiotic chromosome pairing and location of STAG3-related genes flanking the Williams-Beuren syndrome deletion. FASEB J 14:581\u2013592","journal-title":"FASEB J"},{"key":"511_CR54","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1016\/S1097-2765(00)80069-6","volume":"1","author":"DL Pittman","year":"1998","unstructured":"Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E, Handel MA, Schimenti JC (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1:697\u2013705","journal-title":"Mol Cell"},{"key":"511_CR55","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1038\/35087082","volume":"3","author":"I Prieto","year":"2001","unstructured":"Prieto I, Suja JA, Pezzi N, Kremer L, Martinez C, Rufas JS, Barbero JL (2001) Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nat Cell Biol 3:761\u2013766","journal-title":"Nat Cell Biol"},{"key":"511_CR56","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s00412-006-0060-x","volume":"115","author":"E Revenkova","year":"2006","unstructured":"Revenkova E, Jessberger R (2006) Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins. Chromosoma 115:235\u2013240","journal-title":"Chromosoma"},{"key":"511_CR57","doi-asserted-by":"crossref","first-page":"6984","DOI":"10.1128\/MCB.21.20.6984-6998.2001","volume":"21","author":"E Revenkova","year":"2001","unstructured":"Revenkova E, Eijpe M, Heyting C, Gross B, Jessberger R (2001) Novel meiosis-specific isoform of mammalian SMC1. Mol Cell Biol 21:6984\u20136998","journal-title":"Mol Cell Biol"},{"key":"511_CR58","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":"511_CR59","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1016\/S1097-2765(00)00097-6","volume":"6","author":"PJ Romanienko","year":"2000","unstructured":"Romanienko PJ, Camerini-Otero RD (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell 6:975\u2013987","journal-title":"Mol Cell"},{"key":"511_CR60","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1016\/0168-9525(93)90162-B","volume":"9","author":"B Rosen","year":"1993","unstructured":"Rosen B, Beddington RS (1993) Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions. Trends Genet 9:162\u2013167","journal-title":"Trends Genet"},{"key":"511_CR61","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1038\/35085086","volume":"2","author":"H Scherthan","year":"2001","unstructured":"Scherthan H (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2:621\u2013627","journal-title":"Nat Rev Mol Cell Biol"},{"key":"511_CR62","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1038\/nmeth.2019","volume":"9","author":"J Schindelin","year":"2012","unstructured":"Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676\u2013682","journal-title":"Nat Methods"},{"key":"511_CR63","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1007\/s00412-008-0167-3","volume":"117","author":"F Sun","year":"2008","unstructured":"Sun F, Handel MA (2008) Regulation of the meiotic prophase I to metaphase I transition in mouse spermatocytes. Chromosoma 117:471\u2013485","journal-title":"Chromosoma"},{"key":"511_CR64","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1242\/dev.000018","volume":"134","author":"JM Turner","year":"2007","unstructured":"Turner JM (2007) Meiotic sex chromosome inactivation. Development 134:1823\u20131831","journal-title":"Development"},{"key":"511_CR65","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/ng1484","volume":"37","author":"JMA Turner","year":"2005","unstructured":"Turner JMA, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng C-X, Burgoyne PS (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37:41\u201347","journal-title":"Nat Genet"},{"key":"511_CR66","doi-asserted-by":"crossref","first-page":"e1004949","DOI":"10.1371\/journal.pgen.1004949","volume":"11","author":"LA Vrooman","year":"2015","unstructured":"Vrooman LA, Oatley JM, Griswold JE, Hassold TJ, Hunt PA (2015) Estrogenic exposure alters the spermatogonial stem cells in the developing testis, permanently reducing crossover levels in the adult. PLoS Genet 11:e1004949","journal-title":"PLoS Genet"},{"key":"511_CR67","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1007\/s00335-011-9388-5","volume":"23","author":"J Weiss","year":"2012","unstructured":"Weiss J, Hurley LA, Harris RM, Finlayson C, Tong M, Fisher LA, Moran JL, Beier DR, Mason C, Jameson JL (2012) ENU mutagenesis in mice identifies candidate genes for hypogonadism. Mamm Genome 23:346\u2013355","journal-title":"Mamm Genome"},{"key":"511_CR68","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1016\/j.devcel.2005.03.018","volume":"8","author":"H Xu","year":"2005","unstructured":"Xu H, Beasley MD, Warren WD, van der Horst GT, McKay MJ (2005) Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev Cell 8:949\u2013961","journal-title":"Dev Cell"},{"key":"511_CR69","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1242\/dev.113.2.689","volume":"113","author":"K Yoshinaga","year":"1991","unstructured":"Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S-I, Kunisada T, Fujimoto T, Nishikawa S-I (1991) Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113:689\u2013699","journal-title":"Development"},{"key":"511_CR70","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1095\/biolreprod.107.064337","volume":"78","author":"Q Zhou","year":"2008","unstructured":"Zhou Q, Li Y, Nie R, Friel P, Mitchell D, Evanoff RM, Pouchnik DJ, Banasik B, McCarrey JR, Small C, Griswold MD (2008) Expression of Stimulated by retinoic acid gene 8 (Stra8) and maturation of murine gonocytes and spermatogonia induced by retinoic acid in vitro. Biol Reprod 78:537\u2013545","journal-title":"Biol Reprod"}],"container-title":["Chromosoma"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00412-015-0511-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00412-015-0511-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00412-015-0511-3","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,5]],"date-time":"2022-05-05T08:13:06Z","timestamp":1651738386000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00412-015-0511-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,4,18]]},"references-count":70,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2015,9]]}},"alternative-id":["511"],"URL":"https:\/\/doi.org\/10.1007\/s00412-015-0511-3","relation":{},"ISSN":["0009-5915","1432-0886"],"issn-type":[{"value":"0009-5915","type":"print"},{"value":"1432-0886","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,4,18]]}}}