{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T03:46:53Z","timestamp":1791172013670,"version":"4.1.0"},"reference-count":76,"publisher":"Oxford University Press (OUP)","issue":"17","license":[{"start":{"date-parts":[[2024,8,20]],"date-time":"2024-08-20T00:00:00Z","timestamp":1724112000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2021YFC2700200"],"award-info":[{"award-number":["2021YFC2700200"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82371613"],"award-info":[{"award-number":["82371613"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100022963","name":"Key Research and Development Program of Zhejiang Province","doi-asserted-by":"publisher","award":["2023C03035"],"award-info":[{"award-number":["2023C03035"]}],"id":[{"id":"10.13039\/100022963","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100016692","name":"Key Research and Development Program of Ningxia Hui Autonomous Region","doi-asserted-by":"publisher","award":["2021BEG02029"],"award-info":[{"award-number":["2021BEG02029"]}],"id":[{"id":"10.13039\/100016692","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82301798"],"award-info":[{"award-number":["82301798"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002858","name":"China Postdoctoral Science Foundation","doi-asserted-by":"publisher","award":["2022M722767"],"award-info":[{"award-number":["2022M722767"]}],"id":[{"id":"10.13039\/501100002858","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Fellowship of China National Postdoctoral Program for Innovative Talants","award":["BX20230314"],"award-info":[{"award-number":["BX20230314"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,9,23]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Pachynema progression contributes to the completion of prophase I. Nevertheless, the regulation of this significant meiotic process remains poorly understood. In this study, we identified a novel testis-specific protein HSF5, which regulates pachynema progression during male meiosis in a manner dependent on chromatin-binding. Deficiency of HSF5 results in meiotic arrest and male infertility, characterized as unconventional pachynema arrested at the mid-to-late stage, with extensive spermatocyte apoptosis. Our scRNA-seq data confirmed consistent expressional alterations of certain driver genes (Sycp1, Msh4, Meiob, etc.) crucial for pachynema progression in Hsf5\u2212\/\u2212 individuals. HSF5 was revealed to primarily bind to promoter regions of such key divers by CUT&amp;Tag analysis. Also, our results demonstrated that HSF5 biologically interacted with SMARCA5, SMARCA4\u00a0and SMARCE1, and it could function as a transcription factor for pachynema progression during meiosis. Therefore, our study underscores the importance of the chromatin-associated HSF5 for the differentiation of spermatocytes, improving the protein regulatory network of the pachynema progression.<\/jats:p>","DOI":"10.1093\/nar\/gkae701","type":"journal-article","created":{"date-parts":[[2024,8,20]],"date-time":"2024-08-20T11:01:01Z","timestamp":1724151661000},"page":"10255-10275","source":"Crossref","is-referenced-by-count":16,"title":["Meiotic chromatin-associated HSF5 is indispensable for pachynema progression and male fertility"],"prefix":"10.1093","volume":"52","author":[{"ORCID":"https:\/\/orcid.org\/0009-0005-0397-1640","authenticated-orcid":false,"given":"Chunhai","family":"Luo","sequence":"first","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haoran","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ziqi","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dalin","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danyang","family":"Zhong","sequence":"additional","affiliation":[{"name":"Department of General Surgery, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shumin","family":"Zhou","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Beibei","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junfeng","family":"Zhan","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fei","family":"Sun","sequence":"additional","affiliation":[{"name":"Department of Urology & Andrology, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine , Hangzhou , Zhejiang\u00a0 310016 , China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,8,20]]},"reference":[{"key":"2024092307420105700_B1","doi-asserted-by":"crossref","first-page":"a016626","DOI":"10.1101\/cshperspect.a016626","article-title":"Recombination, pairing, and synapsis of homologs during meiosis","volume":"7","author":"Zickler","year":"2015","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"2024092307420105700_B2","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1038\/nrg2723","article-title":"Genetics of mammalian meiosis: regulation, dynamics and impact on fertility","volume":"11","author":"Handel","year":"2010","journal-title":"Nat. Rev. Genet."},{"key":"2024092307420105700_B3","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/S0092-8674(00)81876-0","article-title":"Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family","volume":"88","author":"Keeney","year":"1997","journal-title":"Cell"},{"key":"2024092307420105700_B4","doi-asserted-by":"crossref","first-page":"2029","DOI":"10.1073\/pnas.1414814112","article-title":"Elucidation of synaptonemal complex organization by super-resolution imaging with isotropic resolution","volume":"112","author":"Schucker","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2024092307420105700_B5","doi-asserted-by":"crossref","first-page":"E6857","DOI":"10.1073\/pnas.1705623114","article-title":"Superresolution expansion microscopy reveals the three-dimensional organization of the Drosophila synaptonemal complex","volume":"114","author":"Cahoon","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2024092307420105700_B6","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1038\/nsmb.3208","article-title":"Regulating the construction and demolition of the synaptonemal complex","volume":"23","author":"Cahoon","year":"2016","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2024092307420105700_B7","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1242\/jcs.65.1.249","article-title":"Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse","volume":"65","author":"Goetz","year":"1984","journal-title":"J. Cell Sci."},{"key":"2024092307420105700_B8","doi-asserted-by":"crossref","first-page":"794","DOI":"10.1038\/nrg3573","article-title":"Meiotic recombination in mammals: localization and regulation","volume":"14","author":"Baudat","year":"2013","journal-title":"Nat. Rev. Genet."},{"key":"2024092307420105700_B9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1152\/physrev.00013.2015","article-title":"Spermatogenesis: the commitment to meiosis","volume":"96","author":"Griswold","year":"2016","journal-title":"Physiol. Rev."},{"key":"2024092307420105700_B10","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1093\/biolre\/ioz088","article-title":"What has single-cell RNA-seq taught us about mammalian spermatogenesis?","volume":"101","author":"Suzuki","year":"2019","journal-title":"Biol. Reprod."},{"key":"2024092307420105700_B11","doi-asserted-by":"crossref","first-page":"4595","DOI":"10.1242\/dev.124.22.4595","article-title":"HSP70-2 is required for desynapsis of synaptonemal complexes during meiotic prophase in juvenile and adult mouse spermatocytes","volume":"124","author":"Dix","year":"1997","journal-title":"Development"},{"key":"2024092307420105700_B12","doi-asserted-by":"crossref","first-page":"110540","DOI":"10.1016\/j.celrep.2022.110540","article-title":"ZFP541 maintains the repression of pre-pachytene transcriptional programs and promotes male meiosis progression","volume":"38","author":"Xu","year":"2022","journal-title":"Cell Rep."},{"key":"2024092307420105700_B13","doi-asserted-by":"crossref","first-page":"e2025421118","DOI":"10.1073\/pnas.2025421118","article-title":"The male germline-specific protein MAPS is indispensable for pachynema progression and fertility","volume":"118","author":"Li","year":"2021","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"2024092307420105700_B14","doi-asserted-by":"crossref","first-page":"a016675","DOI":"10.1101\/cshperspect.a016675","article-title":"The meiotic checkpoint network: step-by-step through meiotic prophase","volume":"6","author":"Subramanian","year":"2014","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"2024092307420105700_B15","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/S0168-9525(00)02080-1","article-title":"The pachytene checkpoint","volume":"16","author":"Roeder","year":"2000","journal-title":"Trends Genet."},{"key":"2024092307420105700_B16","doi-asserted-by":"crossref","first-page":"103682","DOI":"10.1016\/j.mcn.2021.103682","article-title":"Kinetic monitoring of neuronal stress response to proteostasis dysfunction","volume":"118","author":"Santiago-Lopez","year":"2022","journal-title":"Mol. Cell. Neurosci."},{"key":"2024092307420105700_B17","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1007\/978-3-031-12966-7_11","article-title":"Heat shock factors in protein quality control and spermatogenesis","volume":"1391","author":"Nelson","year":"2022","journal-title":"Adv. Exp. Med. Biol."},{"key":"2024092307420105700_B18","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1038\/nrm.2017.73","article-title":"Regulation of heat shock transcription factors and their roles in physiology and disease","volume":"19","author":"Gomez-Pastor","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2024092307420105700_B19","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1038\/nrm2938","article-title":"Heat shock factors: integrators of cell stress, development and lifespan","volume":"11","author":"Akerfelt","year":"2010","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2024092307420105700_B20","doi-asserted-by":"crossref","first-page":"34469","DOI":"10.1074\/jbc.M110.157552","article-title":"Heat shock transcription factor 1 localizes to sex chromatin during meiotic repression","volume":"285","author":"Akerfelt","year":"2010","journal-title":"J. Biol. Chem."},{"key":"2024092307420105700_B21","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1002\/gene.20005","article-title":"Essential requirement for both hsf1 and hsf2 transcriptional activity in spermatogenesis and male fertility","volume":"38","author":"Wang","year":"2004","journal-title":"Genesis"},{"key":"2024092307420105700_B22","doi-asserted-by":"crossref","first-page":"3252","DOI":"10.1016\/j.celrep.2018.11.090","article-title":"Heat shock factor 5 is essential for spermatogenesis in zebrafish","volume":"25","author":"Saju","year":"2018","journal-title":"Cell Rep."},{"key":"2024092307420105700_B23","doi-asserted-by":"crossref","first-page":"e15194","DOI":"10.1016\/j.heliyon.2023.e15194","article-title":"Heat shock factor 5 establishes the male germ-line meiotic sex chromosome inactivation through regulation of Smarca4","volume":"9","author":"Barutc","year":"2023","journal-title":"Heliyon"},{"key":"2024092307420105700_B24","doi-asserted-by":"crossref","first-page":"3330","DOI":"10.1038\/s41467-024-47601-0","article-title":"Atypical heat shock transcription factor HSF5 is critical for male meiotic prophase under non-stress conditions","volume":"15","author":"Yoshimura","year":"2023","journal-title":"Nat. Commun."},{"key":"2024092307420105700_B25","doi-asserted-by":"crossref","first-page":"dev199573","DOI":"10.1242\/dev.199573","article-title":"Uncoupling transcription and translation through miRNA-dependent poly (A) length control in haploid male germ cells","volume":"149","author":"Guo","year":"2022","journal-title":"Development"},{"key":"2024092307420105700_B26","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/s41422-021-00539-0","article-title":"SDX on the X chromosome is required for male sex determination","volume":"32","author":"Zhan","year":"2022","journal-title":"Cell Res."},{"key":"2024092307420105700_B27","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1007\/978-1-62703-038-0_27","article-title":"Assessment of spermatogenesis through staging of seminiferous tubules","volume":"927","author":"Meistrich","year":"2013","journal-title":"Methods Mol. Biol."},{"key":"2024092307420105700_B28","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1007\/978-1-4939-8766-5_10","article-title":"Chromosome spread analyses of meiotic sex chromosome inactivation","volume":"1861","author":"Alavattam","year":"2018","journal-title":"Methods Mol. Biol."},{"key":"2024092307420105700_B29","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1007\/s00412-008-0167-3","article-title":"Regulation of the meiotic prophase I to metaphase I transition in mouse spermatocytes","volume":"117","author":"Sun","year":"2008","journal-title":"Chromosoma"},{"key":"2024092307420105700_B30","doi-asserted-by":"crossref","first-page":"1930","DOI":"10.1038\/s41467-019-09982-5","article-title":"CUT&Tag for efficient epigenomic profiling of small samples and single cells","volume":"10","author":"Kaya-Okur","year":"2019","journal-title":"Nat. Commun."},{"key":"2024092307420105700_B31","doi-asserted-by":"crossref","first-page":"jkac130","DOI":"10.1093\/g3journal\/jkac130","article-title":"Comparative analysis of the testes from wild-type and Alkbh5-knockout mice using single-cell RNA sequencing","volume":"12","author":"Hong","year":"2022","journal-title":"G3"},{"key":"2024092307420105700_B32","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"2024092307420105700_B33","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2024092307420105700_B34","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1016\/j.molcel.2010.05.004","article-title":"Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities","volume":"38","author":"Heinz","year":"2010","journal-title":"Mol. Cell"},{"key":"2024092307420105700_B35","doi-asserted-by":"crossref","first-page":"W160","DOI":"10.1093\/nar\/gkw257","article-title":"deepTools2: a next generation web server for deep-sequencing data analysis","volume":"44","author":"Ram\u00edrez","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"2024092307420105700_B36","doi-asserted-by":"crossref","first-page":"2382","DOI":"10.1093\/bioinformatics\/btv145","article-title":"ChIPseeker: an R\/Bioconductor package for ChIP peak annotation, comparison and visualization","volume":"31","author":"Yu","year":"2015","journal-title":"Bioinformatics"},{"key":"2024092307420105700_B37","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1038\/s41587-023-01767-y","article-title":"Dictionary learning for integrative, multimodal and scalable single-cell analysis","volume":"42","author":"Hao","year":"2024","journal-title":"Nat. Biotechnol."},{"key":"2024092307420105700_B38","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1038\/s41422-018-0074-y","article-title":"Single-cell RNA-seq uncovers dynamic processes and critical regulators in mouse spermatogenesis","volume":"28","author":"Chen","year":"2018","journal-title":"Cell Res."},{"key":"2024092307420105700_B39","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1186\/s13059-015-0844-5","article-title":"MAST: a flexible statistical framework for assessing transcriptional changes and characterizing heterogeneity in single-cell RNA sequencing data","volume":"16","author":"Finak","year":"2015","journal-title":"Genome Biol."},{"key":"2024092307420105700_B40","doi-asserted-by":"crossref","first-page":"W216","DOI":"10.1093\/nar\/gkac194","article-title":"DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update)","volume":"50","author":"Sherman","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"2024092307420105700_B41","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1038\/s41586-018-0414-6","article-title":"RNA velocity of single cells","volume":"560","author":"La\u00a0Manno","year":"2018","journal-title":"Nature"},{"key":"2024092307420105700_B42","doi-asserted-by":"crossref","first-page":"6586","DOI":"10.1038\/s41467-022-34188-7","article-title":"UniTVelo: temporally unified RNA velocity reinforces single-cell trajectory inference","volume":"13","author":"Gao","year":"2022","journal-title":"Nat. Commun."},{"key":"2024092307420105700_B43","doi-asserted-by":"crossref","first-page":"2788","DOI":"10.1038\/ncomms3788","article-title":"MEIOB exhibits single-stranded DNA-binding and exonuclease activities and is essential for meiotic recombination","volume":"4","author":"Luo","year":"2013","journal-title":"Nat. Commun."},{"key":"2024092307420105700_B44","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1038\/s41467-019-09182-1","article-title":"Staged developmental mapping and X chromosome transcriptional dynamics during mouse spermatogenesis","volume":"10","author":"Ernst","year":"2019","journal-title":"Nat. Commun."},{"key":"2024092307420105700_B45","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1016\/j.cub.2006.01.066","article-title":"Postmeiotic sex chromatin in the male germline of mice","volume":"16","author":"Namekawa","year":"2006","journal-title":"Curr. Biol."},{"key":"2024092307420105700_B46","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1159\/000076813","article-title":"Temporal expression of cell cycle-related proteins during spermatogenesis: establishing a timeline for onset of the meiotic divisions","volume":"103","author":"Inselman","year":"2003","journal-title":"Cytogenet. Genome Res."},{"key":"2024092307420105700_B47","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1007\/s00412-004-0293-5","article-title":"Correlation of meiotic events in testis sections and microspreads of mouse spermatocytes relative to the mid-pachytene checkpoint","volume":"113","author":"Ashley","year":"2004","journal-title":"Chromosoma"},{"key":"2024092307420105700_B48","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1038\/85830","article-title":"Recombinational DNA double-strand breaks in mice precede synapsis","volume":"27","author":"Mahadevaiah","year":"2001","journal-title":"Nat. Genet."},{"key":"2024092307420105700_B49","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.devcel.2018.10.004","article-title":"SETDB1 links the meiotic DNA damage response to sex chromosome silencing in mice","volume":"47","author":"Hirota","year":"2018","journal-title":"Dev. Cell"},{"key":"2024092307420105700_B50","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/s00412-012-0364-y","article-title":"Inactivation or non-reactivation: what accounts better for the silence of sex chromosomes during mammalian male meiosis?","volume":"121","author":"Page","year":"2012","journal-title":"Chromosoma"},{"key":"2024092307420105700_B51","doi-asserted-by":"crossref","first-page":"eaaz2129","DOI":"10.1126\/sciadv.aaz2129","article-title":"SKP1 drives the prophase I to metaphase I transition during male meiosis","volume":"6","author":"Guan","year":"2020","journal-title":"Sci. Adv."},{"key":"2024092307420105700_B52","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1093\/biolre\/ioz070","article-title":"Functions of cyclins and CDKs in mammalian gametogenesisdagger","volume":"101","author":"Chotiner","year":"2019","journal-title":"Biol. Reprod."},{"key":"2024092307420105700_B53","doi-asserted-by":"crossref","first-page":"3007","DOI":"10.1242\/dev.124.15.3007","article-title":"HSP70-2 is required for CDC2 kinase activity in meiosis I of mouse spermatocytes","volume":"124","author":"Zhu","year":"1997","journal-title":"Development"},{"key":"2024092307420105700_B54","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/978-3-319-51409-3_3","volume-title":"The Role of Heat Shock Proteins in Reproductive System Development and Function","author":"Widlak","year":"2017"},{"key":"2024092307420105700_B55","doi-asserted-by":"crossref","first-page":"651","DOI":"10.1016\/j.devcel.2018.07.025","article-title":"A comprehensive roadmap of murine spermatogenesis defined by single-cell RNA-Seq","volume":"46","author":"Green","year":"2018","journal-title":"Dev. Cell"},{"key":"2024092307420105700_B56","doi-asserted-by":"crossref","first-page":"1650","DOI":"10.1016\/j.celrep.2018.10.026","article-title":"The mammalian spermatogenesis single-cell transcriptome, from spermatogonial stem cells to spermatids","volume":"25","author":"Hermann","year":"2018","journal-title":"Cell Rep."},{"key":"2024092307420105700_B57","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1038\/s41592-023-01994-w","article-title":"Deep generative modeling of transcriptional dynamics for RNA velocity analysis in single cells","volume":"21","author":"Gayoso","year":"2024","journal-title":"Nat. Methods"},{"key":"2024092307420105700_B58","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/s13059-019-1663-x","article-title":"PAGA: graph abstraction reconciles clustering with trajectory inference through a topology preserving map of single cells","volume":"20","author":"Wolf","year":"2019","journal-title":"Genome Biol."},{"key":"2024092307420105700_B59","doi-asserted-by":"crossref","first-page":"2240","DOI":"10.1093\/hmg\/ddaa113","article-title":"Male sterility and reduced female fertility in SCAPER-deficient mice","volume":"29","author":"Tatour","year":"2020","journal-title":"Hum. Mol. Genet."},{"key":"2024092307420105700_B60","doi-asserted-by":"crossref","first-page":"e1003435","DOI":"10.1371\/journal.pgen.1003435","article-title":"Senataxin plays an essential role with DNA damage response proteins in meiotic recombination and gene silencing","volume":"9","author":"Becherel","year":"2013","journal-title":"PLoS Genet."},{"key":"2024092307420105700_B61","doi-asserted-by":"crossref","first-page":"e49307","DOI":"10.7554\/eLife.49307","article-title":"Dzip1 and Fam92 form a ciliary transition zone complex with cell type specific roles in Drosophila","volume":"8","author":"Lapart","year":"2019","journal-title":"eLife"},{"key":"2024092307420105700_B62","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1016\/j.cub.2009.02.047","article-title":"Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression","volume":"19","author":"Vasileva","year":"2009","journal-title":"Curr. Biol."},{"key":"2024092307420105700_B63","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1016\/S1097-2765(00)80430-X","article-title":"The ISWI chromatin-remodeling protein is required for gene expression and the maintenance of higher order chromatin structure in vivo","volume":"5","author":"Deuring","year":"2000","journal-title":"Mol. Cell"},{"key":"2024092307420105700_B64","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/S0168-9525(00)02060-6","article-title":"The Swi\/Snf family nucleosome-remodeling complexes and transcriptional control","volume":"16","author":"Sudarsanam","year":"2000","journal-title":"Trends Genet."},{"key":"2024092307420105700_B65","first-page":"S1097-2765(24)00536-7","article-title":"Swi\/Snf chromatin remodeling regulates transcriptional interference and gene repression","author":"Morse","year":"2023","journal-title":"Mol Cell"},{"key":"2024092307420105700_B66","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1101\/gad.331157.119","article-title":"The chromatin remodeler Snf2h is essential for oocyte meiotic cell cycle progression","volume":"34","author":"Zhang","year":"2020","journal-title":"Genes Dev."},{"key":"2024092307420105700_B67","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1242\/dev.073478","article-title":"An essential role for a mammalian SWI\/SNF chromatin-remodeling complex during male meiosis","volume":"139","author":"Kim","year":"2012","journal-title":"Development"},{"key":"2024092307420105700_B68","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1038\/cr.2015.16","article-title":"SMARCE1 suppresses EGFR expression and controls responses to MET and ALK inhibitors in lung cancer","volume":"25","author":"Papadakis","year":"2015","journal-title":"Cell Res."},{"key":"2024092307420105700_B69","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1242\/dev.000018","article-title":"Meiotic sex chromosome inactivation","volume":"134","author":"Turner","year":"2007","journal-title":"Development"},{"key":"2024092307420105700_B70","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1093\/biolre\/ioaa021","article-title":"The XY body: an attractive chromatin domain","volume":"102","author":"Handel","year":"2020","journal-title":"Biol. Reprod."},{"key":"2024092307420105700_B71","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1016\/j.devcel.2006.02.009","article-title":"Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids","volume":"10","author":"Turner","year":"2006","journal-title":"Dev. Cell"},{"key":"2024092307420105700_B72","doi-asserted-by":"crossref","first-page":"1125","DOI":"10.1016\/S0092-8674(00)81312-4","article-title":"Meiotic pachytene arrest in MLH1-deficient mice","volume":"85","author":"Edelmann","year":"1996","journal-title":"Cell"},{"key":"2024092307420105700_B73","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/S1534-5807(03)00093-5","article-title":"H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis","volume":"4","author":"Fernandez-Capetillo","year":"2003","journal-title":"Dev. Cell"},{"key":"2024092307420105700_B74","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1101\/gad.2030811","article-title":"MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cells","volume":"25","author":"Ichijima","year":"2011","journal-title":"Genes Dev."},{"key":"2024092307420105700_B75","doi-asserted-by":"crossref","first-page":"2003636","DOI":"10.1002\/advs.202003636","article-title":"The CNOT4 subunit of the CCR4-NOT complex is involved in mRNA degradation, efficient DNA damage repair, and XY chromosome crossover during male germ cell meiosis","volume":"8","author":"Dai","year":"2021","journal-title":"Adv. Sci."},{"key":"2024092307420105700_B76","doi-asserted-by":"crossref","first-page":"3387","DOI":"10.1038\/s41467-019-11346-y","article-title":"Meiosis I progression in spermatogenesis requires a type of testis-specific 20S core proteasome","volume":"10","author":"Zhang","year":"2019","journal-title":"Nat. Commun."}],"container-title":["Nucleic Acids Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/nar\/advance-article-pdf\/doi\/10.1093\/nar\/gkae701\/59209290\/gkae701.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/nar\/advance-article-pdf\/doi\/10.1093\/nar\/gkae701\/59209290\/gkae701.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,23]],"date-time":"2024-09-23T07:43:00Z","timestamp":1727077380000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/nar\/article\/52\/17\/10255\/7736810"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,20]]},"references-count":76,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2024,8,20]]},"published-print":{"date-parts":[[2024,9,23]]}},"URL":"https:\/\/doi.org\/10.1093\/nar\/gkae701","relation":{},"ISSN":["0305-1048","1362-4962"],"issn-type":[{"value":"0305-1048","type":"print"},{"value":"1362-4962","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,9,23]]},"published":{"date-parts":[[2024,8,20]]}}}