{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T11:26:30Z","timestamp":1790767590848,"version":"4.1.0"},"reference-count":48,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,1,1]],"date-time":"2021-01-01T00:00:00Z","timestamp":1609459200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,1,1]],"date-time":"2021-01-01T00:00:00Z","timestamp":1609459200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2020,12,2]],"date-time":"2020-12-02T00:00:00Z","timestamp":1606867200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31530014"],"award-info":[{"award-number":["31530014"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["2018YFC1003303"],"award-info":[{"award-number":["2018YFC1003303"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002855","name":"Ministry of Science and Technology of the People&apos;s Republic of China","doi-asserted-by":"publisher","award":["2019YFA0802100"],"award-info":[{"award-number":["2019YFA0802100"]}],"id":[{"id":"10.13039\/501100002855","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002855","name":"Ministry of Science and Technology of the People&apos;s Republic of China","doi-asserted-by":"publisher","award":["2018YFC1003303"],"award-info":[{"award-number":["2018YFC1003303"]}],"id":[{"id":"10.13039\/501100002855","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["jbc.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Journal of Biological Chemistry"],"published-print":{"date-parts":[[2021,1]]},"DOI":"10.1074\/jbc.ra120.016485","type":"journal-article","created":{"date-parts":[[2020,12,1]],"date-time":"2020-12-01T19:45:26Z","timestamp":1606851926000},"page":"100130","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":31,"special_numbering":"C","title":["Proteasome subunit \u03b14s is essential for formation of spermatoproteasomes and histone degradation during meiotic DNA repair in spermatocytes"],"prefix":"10.1016","volume":"296","author":[{"given":"Zi-Hui","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tian-Xia","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lian-Bin","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenhui","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yixun","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4029-6411","authenticated-orcid":false,"given":"Fei","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2608-9376","authenticated-orcid":false,"given":"Xiao-Bo","family":"Qiu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1074\/jbc.RA120.016485_bib1","doi-asserted-by":"crossref","first-page":"3518","DOI":"10.1200\/JCO.2008.18.3087","article-title":"Single-agent bortezomib in previously untreated multiple myeloma: efficacy, characterization of peripheral neuropathy, and molecular correlations with response and neuropathy","volume":"27","author":"Richardson","year":"2009","journal-title":"J.\u00a0Clin. Oncol."},{"key":"10.1074\/jbc.RA120.016485_bib2","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.molcel.2010.12.020","article-title":"Proteasome activators","volume":"41","author":"Stadtmueller","year":"2011","journal-title":"Mol. Cell"},{"key":"10.1074\/jbc.RA120.016485_bib3","doi-asserted-by":"crossref","first-page":"1765","DOI":"10.1111\/brv.12419","article-title":"Substrate receptors of proteasomes","volume":"93","author":"Jiang","year":"2018","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"10.1074\/jbc.RA120.016485_bib4","doi-asserted-by":"crossref","first-page":"1012","DOI":"10.1016\/j.cell.2013.04.032","article-title":"Acetylation-mediated proteasomal degradation of core histones during DNA repair and spermatogenesis","volume":"153","author":"Qian","year":"2013","journal-title":"Cell"},{"key":"10.1074\/jbc.RA120.016485_bib5","doi-asserted-by":"crossref","DOI":"10.15252\/embr.201745566","article-title":"DNA damage-induced replication stress results in PA200-proteasome-mediated degradation of acetylated histones","volume":"19","author":"Mandemaker","year":"2018","journal-title":"EMBO Rep."},{"key":"10.1074\/jbc.RA120.016485_bib6","doi-asserted-by":"crossref","first-page":"12365","DOI":"10.1074\/jbc.M114.558866","article-title":"Characterization of the testis-specific proteasome subunit alpha4s in mammals","volume":"289","author":"Uechi","year":"2014","journal-title":"J.\u00a0Biol. Chem."},{"key":"10.1074\/jbc.RA120.016485_bib7","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.ydbio.2011.05.661","article-title":"The E3 ubiquitin ligase cullin 4A regulates meiotic progression in mouse spermatogenesis","volume":"356","author":"Yin","year":"2011","journal-title":"Dev. Biol."},{"key":"10.1074\/jbc.RA120.016485_bib8","doi-asserted-by":"crossref","first-page":"R55","DOI":"10.1530\/REP-15-0562","article-title":"Epigenetic regulation of the histone-to-protamine transition during spermiogenesis","volume":"151","author":"Bao","year":"2016","journal-title":"Reproduction"},{"key":"10.1074\/jbc.RA120.016485_bib9","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.molcel.2017.02.025","article-title":"Histone variant H2A.L.2 guides transition protein-dependent protamine assembly in male germ cells","volume":"66","author":"Barral","year":"2017","journal-title":"Mol. Cell"},{"key":"10.1074\/jbc.RA120.016485_bib10","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/j.tig.2011.06.007","article-title":"New and old ways to control meiotic recombination","volume":"27","author":"Phadnis","year":"2011","journal-title":"Trends Genet."},{"key":"10.1074\/jbc.RA120.016485_bib11","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.cell.2016.09.035","article-title":"The landscape of mouse meiotic double-strand break formation, processing, and repair","volume":"167","author":"Lange","year":"2016","journal-title":"Cell"},{"key":"10.1074\/jbc.RA120.016485_bib12","article-title":"Meiotic recombination: the essence of heredity","volume":"7","author":"Hunter","year":"2015","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"10.1074\/jbc.RA120.016485_bib13","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1126\/science.1195774","article-title":"Distinct properties of the XY pseudoautosomal region crucial for male meiosis","volume":"331","author":"Kauppi","year":"2011","journal-title":"Science"},{"key":"10.1074\/jbc.RA120.016485_bib14","article-title":"The PSMA8 subunit of the spermatoproteasome is essential for proper meiotic exit and mouse fertility","volume":"15","author":"Go'mez-H","year":"2019","journal-title":"PLoS Genet."},{"key":"10.1074\/jbc.RA120.016485_bib15","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."},{"key":"10.1074\/jbc.RA120.016485_bib16","doi-asserted-by":"crossref","first-page":"5091","DOI":"10.1002\/j.1460-2075.1992.tb05616.x","article-title":"A\u00a0coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes","volume":"11","author":"Meuwissen","year":"1992","journal-title":"EMBO J."},{"issue":"Pt 10","key":"10.1074\/jbc.RA120.016485_bib17","doi-asserted-by":"crossref","first-page":"2749","DOI":"10.1242\/jcs.107.10.2749","article-title":"Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction","volume":"107","author":"Dobson","year":"1994","journal-title":"J.\u00a0Cell Sci."},{"key":"10.1074\/jbc.RA120.016485_bib18","doi-asserted-by":"crossref","first-page":"11987","DOI":"10.1073\/pnas.0600994103","article-title":"The Wilms tumor gene, Wt1, is required for Sox9 expression and maintenance of tubular architecture in the developing testis","volume":"103","author":"Gao","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1074\/jbc.RA120.016485_bib19","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1186\/gb-2007-8-9-227","article-title":"The protamine family of sperm nuclear proteins","volume":"8","author":"Balhorn","year":"2007","journal-title":"Genome Biol."},{"key":"10.1074\/jbc.RA120.016485_bib20","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1016\/j.bios.2008.07.040","article-title":"An annexin V-based biosensor for quantitatively detecting early apoptotic cells","volume":"24","author":"Tong","year":"2009","journal-title":"Biosens. Bioelectron."},{"key":"10.1074\/jbc.RA120.016485_bib21","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1003320","article-title":"Conditional inactivation of the DNA damage response gene Hus1 in mouse testis reveals separable roles for components of the RAD9-RAD1-HUS1 complex in meiotic chromosome maintenance","volume":"9","author":"Lyndaker","year":"2013","journal-title":"PLoS Genet."},{"key":"10.1074\/jbc.RA120.016485_bib22","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.molcel.2016.03.014","article-title":"Dynamic competing histone H4 K5K8 acetylation and butyrylation are hallmarks of highly active gene promoters","volume":"62","author":"Goudarzi","year":"2016","journal-title":"Mol. Cell"},{"key":"10.1074\/jbc.RA120.016485_bib23","doi-asserted-by":"crossref","first-page":"3233","DOI":"10.1242\/jcs.02466","article-title":"SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-\/- spermatocytes","volume":"118","author":"Bellani","year":"2005","journal-title":"J.\u00a0Cell Sci."},{"key":"10.1074\/jbc.RA120.016485_bib24","doi-asserted-by":"crossref","first-page":"7203","DOI":"10.1128\/MCB.25.16.7203-7215.2005","article-title":"Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage","volume":"25","author":"Barchi","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"10.1074\/jbc.RA120.016485_bib25","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":"10.1074\/jbc.RA120.016485_bib26","doi-asserted-by":"crossref","first-page":"1621","DOI":"10.1271\/bbb.120024","article-title":"Impairment of pachytene spermatogenesis in Dmrt7 deficient mice, possibly causing meiotic arrest","volume":"76","author":"Date","year":"2012","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"10.1074\/jbc.RA120.016485_bib27","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1038\/ng0796-336","article-title":"Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over","volume":"13","author":"Baker","year":"1996","journal-title":"Nat. Genet."},{"key":"10.1074\/jbc.RA120.016485_bib28","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1016\/S1097-2765(00)00097-6","article-title":"The mouse Spo11 gene is required for meiotic chromosome synapsis","volume":"6","author":"Romanienko","year":"2000","journal-title":"Mol. Cell"},{"key":"10.1074\/jbc.RA120.016485_bib29","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1101\/gad.329705","article-title":"Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation","volume":"19","author":"de Vries","year":"2005","journal-title":"Genes Dev."},{"key":"10.1074\/jbc.RA120.016485_bib30","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.cell.2009.07.035","article-title":"Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure","volume":"139","author":"Mets","year":"2009","journal-title":"Cell"},{"key":"10.1074\/jbc.RA120.016485_bib31","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1002\/mrd.1080310303","article-title":"Highly acetylated H4 is associated with histone displacement in rat spermatids","volume":"31","author":"Meistrich","year":"1992","journal-title":"Mol. Reprod. Dev."},{"key":"10.1074\/jbc.RA120.016485_bib32","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1002\/jemt.20730","article-title":"gammaH2AX marks the main events of the spermatogenic process","volume":"72","author":"Blanco-Rodriguez","year":"2009","journal-title":"Microsc. Res. Tech."},{"key":"10.1074\/jbc.RA120.016485_bib33","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1126\/science.8290959","article-title":"Meiosis-induced double-strand break sites determined by yeast chromatin structure","volume":"263","author":"Wu","year":"1994","journal-title":"Science"},{"key":"10.1074\/jbc.RA120.016485_bib34","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1007\/s003359900149","article-title":"Molecular analysis of a recombinational hotspot adjacent to Lmp2 gene in the mouse MHC: fine location and chromatin structure","volume":"7","author":"Mizuno","year":"1996","journal-title":"Mamm. Genome"},{"key":"10.1074\/jbc.RA120.016485_bib35","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1159\/000076812","article-title":"Specific arrests of spermatogenesis in genetically modified and mutant mice","volume":"103","author":"de Rooij","year":"2003","journal-title":"Cytogenet. Genome Res."},{"key":"10.1074\/jbc.RA120.016485_bib36","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.0030198","article-title":"Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein","volume":"3","author":"de la Fuente","year":"2007","journal-title":"PLoS Genet."},{"key":"10.1074\/jbc.RA120.016485_bib37","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/nsmb.3347","article-title":"Histone degradation in response to DNA damage enhances chromatin dynamics and recombination rates","volume":"24","author":"Hauer","year":"2017","journal-title":"Nat. Struct. Mol. Biol."},{"key":"10.1074\/jbc.RA120.016485_bib38","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.molcel.2019.07.014","article-title":"Characterization of fully recombinant human 20S and 20S-PA200 proteasome complexes","volume":"76","author":"R\u00eago","year":"2019","journal-title":"Mol. Cell"},{"key":"10.1074\/jbc.RA120.016485_bib39","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/978-3-540-48461-5_6","article-title":"An integration of old and new perspectives of mammalian meiotic sterility","volume":"28","author":"Ashley","year":"2000","journal-title":"Results Probl. Cell Differ."},{"key":"10.1074\/jbc.RA120.016485_bib40","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":"10.1074\/jbc.RA120.016485_bib41","doi-asserted-by":"crossref","first-page":"2001","DOI":"10.1242\/dev.00410","article-title":"Impaired meiotic DNA-damage repair and lack of crossing-over during spermatogenesis in BRCA1 full-length isoform deficient mice","volume":"130","author":"Xu","year":"2003","journal-title":"Development"},{"key":"10.1074\/jbc.RA120.016485_bib42","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1016\/j.cell.2012.06.045","article-title":"Small-molecule inhibition of BRDT for male contraception","volume":"150","author":"Matzuk","year":"2012","journal-title":"Cell"},{"key":"10.1074\/jbc.RA120.016485_bib43","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1007\/978-0-387-09597-4_9","article-title":"Antioxidant systems and oxidative stress in the testes","volume":"636","author":"Aitken","year":"2008","journal-title":"Adv. Exp. Med. Biol."},{"key":"10.1074\/jbc.RA120.016485_bib44","doi-asserted-by":"crossref","first-page":"3809","DOI":"10.1038\/emboj.2012.233","article-title":"Bromodomain-dependent stage-specific male genome programming by Brdt","volume":"31","author":"Gaucher","year":"2012","journal-title":"EMBO J."},{"key":"10.1074\/jbc.RA120.016485_bib45","doi-asserted-by":"crossref","first-page":"5742","DOI":"10.1038\/sj.emboj.7601450","article-title":"hRpn13\/ADRM1\/GP110 is a novel proteasome subunit that binds the deubiquitinating enzyme, UCH37","volume":"25","author":"Qiu","year":"2006","journal-title":"EMBO J."},{"key":"10.1074\/jbc.RA120.016485_bib46","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1002\/cyto.a.22463","article-title":"Optimized flow cytometry isolation of murine spermatocytes","volume":"85","author":"Gaysinskaya","year":"2014","journal-title":"Cytometry A"},{"key":"10.1074\/jbc.RA120.016485_bib47","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1001062","article-title":"Mouse TRIP13\/PCH2 is required for recombination and normal higher-order chromosome structure during meiosis","volume":"6","author":"Roig","year":"2010","journal-title":"PLoS Genet."},{"key":"10.1074\/jbc.RA120.016485_bib48","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/S0076-6879(05)98026-9","article-title":"Purification and assay of proteasome activator PA200","volume":"398","author":"Ustrell","year":"2005","journal-title":"Methods Enzymol."}],"container-title":["Journal of Biological Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0021925820001222?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0021925820001222?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1074\/jbc.RA120.016485","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,4,28]],"date-time":"2026-04-28T23:56:13Z","timestamp":1777420573000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0021925820001222"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,1]]},"references-count":48,"alternative-id":["S0021925820001222"],"URL":"https:\/\/doi.org\/10.1074\/jbc.ra120.016485","relation":{},"ISSN":["0021-9258"],"issn-type":[{"value":"0021-9258","type":"print"}],"subject":[],"published":{"date-parts":[[2021,1]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Proteasome subunit \u03b14s is essential for formation of spermatoproteasomes and histone degradation during meiotic DNA repair in spermatocytes","name":"articletitle","label":"Article Title"},{"value":"Journal of Biological Chemistry","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1074\/jbc.RA120.016485","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2020 The Authors. Published by Elsevier Inc on behalf of American Society for Biochemistry and Molecular Biology.","name":"copyright","label":"Copyright"}],"article-number":"100130"}}