{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T02:33:16Z","timestamp":1784687596147,"version":"3.55.0"},"reference-count":49,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2025,7,24]],"date-time":"2025-07-24T00:00:00Z","timestamp":1753315200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,9,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Tex30, a member of the \u201ctestis-expressed\u201d genes, has been implicated in spermatogenesis due to its high expression in the testes, localized in both the cytoplasmic and soluble nuclear fractions of testicular cells. However, its precise role in germ cell development remains unclear. In this study, we generated Tex30 knockout (KO) mice by utilizing the CRISPR\/Cas9-mediated gene KO approach and comprehensively investigated its function in reproduction. The results revealed that the male Tex30 KO mice exhibited increased apoptosis in metaphase I spermatocytes, premature dissociation of XY chromosomes in late spermatocytes, and spermiogenic defects, leading to a significant reduction in sperm production and motility, and thus final subfertility. The adult female Tex30 KO mice did not show significant differences in ovaries and fertility when compared with the control females. IP-MS-based identification of TEX30 interactomes in testis unveils its role in RNA metabolism and cytoskeletal regulation, whose dysregulation resulted from TEX30 ablation may account for the reproductive phenotype in male mice. Taken together, the data presented in this study suggest that TEX30 plays a role in spermatogenesis and male fertility.<\/jats:p>","DOI":"10.1093\/biolre\/ioaf163","type":"journal-article","created":{"date-parts":[[2025,7,24]],"date-time":"2025-07-24T12:06:09Z","timestamp":1753358769000},"page":"672-685","source":"Crossref","is-referenced-by-count":4,"title":["Loss of TEX30 leads to male subfertility in mice"],"prefix":"10.1093","volume":"113","author":[{"given":"Qi","family":"Sun","sequence":"first","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zejia","family":"Li","sequence":"additional","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Binyi","family":"Wang","sequence":"additional","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Muyang","family":"Cheng","sequence":"additional","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Shen","sequence":"additional","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengcheng","family":"Luo","sequence":"additional","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2561-348X","authenticated-orcid":false,"given":"Rong","family":"Liu","sequence":"additional","affiliation":[{"name":"Hubei Provincial Key Laboratory of Developmentally Originated Disease, Taikang Center for Life and Medical Sciences, Taikang Medical School (School of Basic Medical Sciences), Wuhan University , Wuhan, Hubei Province ,","place":["China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,7,24]]},"reference":[{"key":"2025091917113043900_ref1","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1016\/j.rbmo.2016.08.001","article-title":"Retraction notice to \u2018does ovarian stimulation for IVF increase gynaecological cancer risk? A systematic review and meta-analysis\u2019 [reproductive BioMedicine online 31 (2015) 20-29]","volume":"33","author":"Zhao","year":"2016","journal-title":"Reprod Biomed Online"},{"key":"2025091917113043900_ref2","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1038\/s41572-023-00459-w","volume":"9","author":"Eisenberg","year":"2023","journal-title":"Male infertility Nat Rev Dis Primers"},{"key":"2025091917113043900_ref3","doi-asserted-by":"crossref","first-page":"3659","DOI":"10.1242\/dev.152413","article-title":"Unraveling transcriptome dynamics in human spermatogenesis","volume":"144","author":"Jan","year":"2017","journal-title":"Development"},{"key":"2025091917113043900_ref4","first-page":"1","article-title":"Spermatogenesis and cycle of the seminiferous epithelium","volume":"636","author":"Hess","year":"2008","journal-title":"Adv Exp Med Biol"},{"key":"2025091917113043900_ref5","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1038\/s41585-018-0003-3","article-title":"Genetics of male infertility","volume":"15","author":"Krausz","year":"2018","journal-title":"Nat Rev Urol"},{"key":"2025091917113043900_ref6","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1038\/86927","article-title":"An abundance of X-linked genes expressed in spermatogonia","volume":"27","author":"Wang","year":"2001","journal-title":"Nat Genet"},{"key":"2025091917113043900_ref7","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/s12610-021-00127-7","article-title":"Human testis-expressed (TEX) genes: a review focused on spermatogenesis and male fertility","volume":"31","author":"Bellil","year":"2021","journal-title":"Basic Clin Androl"},{"key":"2025091917113043900_ref8","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/S0925-4773(02)00026-6","article-title":"Expression of a novel TGIF subclass homeobox gene, Tex1, in the spermatids of mouse testis during spermatogenesis","volume":"113","author":"Lai","year":"2002","journal-title":"Mech Dev"},{"key":"2025091917113043900_ref9","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1111\/andr.13511","article-title":"Scrutinizing the human TEX genes in the context of human male infertility","volume":"12","author":"Sieper","year":"2024","journal-title":"Andrology"},{"key":"2025091917113043900_ref10","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1101\/gad.1613608","article-title":"Meiotic failure in male mice lacking an X-linked factor","volume":"22","author":"Yang","year":"2008","journal-title":"Genes Dev"},{"key":"2025091917113043900_ref11","doi-asserted-by":"crossref","first-page":"e1000042","DOI":"10.1371\/journal.pgen.1000042","article-title":"ZIP4H (TEX11) deficiency in the mouse impairs meiotic double strand break repair and the regulation of crossing over","volume":"4","author":"Adelman","year":"2008","journal-title":"PLoS Genet"},{"key":"2025091917113043900_ref12","doi-asserted-by":"crossref","first-page":"9260","DOI":"10.1074\/jbc.RA119.008404","article-title":"A molecular model for self-assembly of the synaptonemal complex protein SYCE3","volume":"294","author":"Dunne","year":"2019","journal-title":"J Biol Chem"},{"key":"2025091917113043900_ref13","doi-asserted-by":"crossref","first-page":"4025","DOI":"10.1242\/jcs.03182","article-title":"Characterization of a novel meiosis-specific protein within the central element of the synaptonemal complex","volume":"119","author":"Hamer","year":"2006","journal-title":"J Cell Sci"},{"key":"2025091917113043900_ref14","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1159\/000468934","article-title":"Two novel TEX15 mutations in a family with nonobstructive azoospermia","volume":"82","author":"Colombo","year":"2017","journal-title":"Gynecol Obstet Invest"},{"key":"2025091917113043900_ref15","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1095\/biolreprod.108.070649","article-title":"Mouse TEX14 is required for embryonic germ cell intercellular bridges but not female fertility","volume":"80","author":"Greenbaum","year":"2009","journal-title":"Biol Reprod"},{"key":"2025091917113043900_ref16","doi-asserted-by":"crossref","first-page":"12201","DOI":"10.1073\/pnas.1635054100","article-title":"A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets","volume":"100","author":"Schultz","year":"2003","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025091917113043900_ref17","doi-asserted-by":"crossref","first-page":"3526","DOI":"10.1002\/1873-3468.12433","article-title":"TEX13 is a novel male germ cell-specific nuclear protein potentially involved in transcriptional repression","volume":"590","author":"Kwon","year":"2016","journal-title":"FEBS Lett"},{"key":"2025091917113043900_ref18","doi-asserted-by":"crossref","first-page":"3017","DOI":"10.1007\/s11033-021-06265-5","article-title":"Analysis of mouse male germ cell-specific or -predominant Tex13 family genes encoding proteins with transcriptional repressor activity","volume":"48","author":"Kim","year":"2021","journal-title":"Mol Biol Rep"},{"key":"2025091917113043900_ref19","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1093\/molehr\/gal107","article-title":"Asthenoteratozoospermia in mice lacking testis expressed gene 18 (Tex18)","volume":"13","author":"Jaroszynski","year":"2007","journal-title":"Mol Hum Reprod"},{"key":"2025091917113043900_ref20","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1093\/biolre\/ioaa084","article-title":"CRISPR\/Cas9-mediated genome-edited mice reveal 10 testis-enriched genes are dispensable for male fecundity","volume":"103","author":"Park","year":"2020","journal-title":"Biol Reprod"},{"key":"2025091917113043900_ref21","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1038\/nature13992","article-title":"A comparative encyclopedia of DNA elements in the mouse genome","volume":"515","author":"Yue","year":"2014","journal-title":"Nature"},{"key":"2025091917113043900_ref22","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":"2025091917113043900_ref23","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1159\/000129818","article-title":"An air-drying method for meiotic preparations from mammalian testes","volume":"3","author":"Evans","year":"1964","journal-title":"Cytogenetics"},{"key":"2025091917113043900_ref24","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1074\/mcp.M113.035600","article-title":"Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics","volume":"13","author":"Fagerberg","year":"2014","journal-title":"Mol Cell Proteomics"},{"key":"2025091917113043900_ref25","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":"2025091917113043900_ref26","doi-asserted-by":"crossref","first-page":"e1000702","DOI":"10.1371\/journal.pgen.1000702","article-title":"Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase","volume":"5","author":"Wojtasz","year":"2009","journal-title":"PLoS Genet"},{"key":"2025091917113043900_ref27","doi-asserted-by":"crossref","first-page":"eabk1789","DOI":"10.1126\/sciadv.abk1789","article-title":"RAD51AP2 is required for efficient meiotic recombination between X and Y chromosomes","volume":"8","author":"Ma","year":"2022","journal-title":"Sci Adv"},{"key":"2025091917113043900_ref28","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1038\/s41421-023-00577-5","article-title":"A novel recombination protein C12ORF40\/REDIC1 is required for meiotic crossover formation","volume":"9","author":"Fan","year":"2023","journal-title":"Cell Discov"},{"key":"2025091917113043900_ref29","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1083\/jcb.200603063","article-title":"Mouse SYCP2 is required for synaptonemal complex assembly and chromosomal synapsis during male meiosis","volume":"173","author":"Yang","year":"2006","journal-title":"J Cell Biol"},{"key":"2025091917113043900_ref30","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1038\/ng.2541","article-title":"RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis","volume":"45","author":"Reynolds","year":"2013","journal-title":"Nat Genet"},{"key":"2025091917113043900_ref31","doi-asserted-by":"crossref","first-page":"12219","DOI":"10.1093\/nar\/gkaa1016","article-title":"The ssDNA-binding protein MEIOB acts as a dosage-sensitive regulator of meiotic recombination","volume":"48","author":"Guo","year":"2020","journal-title":"Nucleic Acids Res"},{"key":"2025091917113043900_ref32","doi-asserted-by":"crossref","first-page":"2904","DOI":"10.1074\/jbc.M410397200","article-title":"Association of NASP with HSP90 in mouse spermatogenic cells: stimulation of ATPase activity and transport of linker histones into nuclei","volume":"280","author":"Alekseev","year":"2005","journal-title":"J Biol Chem"},{"key":"2025091917113043900_ref33","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/978-3-319-51409-3_4","article-title":"Heat shock protein A2 (HSPA2): regulatory roles in germ cell development and sperm function","volume":"222","author":"Nixon","year":"2017","journal-title":"Adv Anat Embryol Cell Biol"},{"key":"2025091917113043900_ref34","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1038\/sj.onc.1203442","article-title":"SPAF, a new AAA-protein specific to early spermatogenesis and malignant conversion","volume":"19","author":"Liu","year":"2000","journal-title":"Oncogene"},{"key":"2025091917113043900_ref35","doi-asserted-by":"crossref","DOI":"10.3390\/ijms23031284","article-title":"Role of eIF5A in mitochondrial function","volume":"23","author":"Barba-Aliaga","year":"2022","journal-title":"Int J Mol Sci"},{"key":"2025091917113043900_ref36","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1038\/s41594-022-00909-1","article-title":"Structural maturation of SYCP1-mediated meiotic chromosome synapsis by SYCE3","volume":"30","author":"Crichton","year":"2023","journal-title":"Nat Struct Mol Biol"},{"key":"2025091917113043900_ref37","doi-asserted-by":"crossref","first-page":"510","DOI":"10.4103\/aja.aja_8_21","article-title":"A new TEX11 mutation causes azoospermia and testicular meiotic arrest","volume":"23","author":"Yu","year":"2021","journal-title":"Asian J Androl"},{"key":"2025091917113043900_ref38","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.lfs.2018.12.016","article-title":"Proteomic analyses reveal lower expression of TEX40 and ATP6V0A2 proteins related to calcium ion entry and acrosomal acidification in asthenozoospermic males","volume":"218","author":"Sinha","year":"2019","journal-title":"Life Sci"},{"key":"2025091917113043900_ref39","doi-asserted-by":"crossref","DOI":"10.3390\/ijms21186628","article-title":"Role of the glycosylphosphatidylinositol-anchored protein TEX101 and its related molecules in spermatogenesis","volume":"21","author":"Yoshitake","year":"2020","journal-title":"Int J Mol Sci"},{"key":"2025091917113043900_ref40","doi-asserted-by":"crossref","first-page":"2897","DOI":"10.1016\/j.cell.2023.05.009","article-title":"Structures of sperm flagellar doublet microtubules expand the genetic spectrum of male infertility","volume":"186","author":"Zhou","year":"2023","journal-title":"Cell"},{"key":"2025091917113043900_ref41","doi-asserted-by":"crossref","first-page":"2420","DOI":"10.4103\/NRR.NRR-D-23-01725","article-title":"CNKSR2 interactome analysis indicates its association with the centrosome\/microtubule system","volume":"20","author":"Yin","year":"2025","journal-title":"Neural Regen Res"},{"key":"2025091917113043900_ref42","first-page":"694","article-title":"Differentially expressed genes in asthenospermia: a bioinformatics-based study","volume":"17","author":"Mao","year":"2011","journal-title":"Zhonghua Nan Ke Xue"},{"key":"2025091917113043900_ref43","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1002\/1878-0261.13024","article-title":"Targeting of lactate dehydrogenase C dysregulates the cell cycle and sensitizes breast cancer cells to DNA damage response targeted therapy","volume":"16","author":"Naik","year":"2022","journal-title":"Mol Oncol"},{"key":"2025091917113043900_ref44","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":"2025091917113043900_ref45","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1080\/15548627.2019.1668228","article-title":"The Paf1 complex transcriptionally regulates the mitochondrial-anchored protein Atg32 leading to activation of mitophagy","volume":"16","author":"Zheng","year":"2020","journal-title":"Autophagy"},{"key":"2025091917113043900_ref46","doi-asserted-by":"crossref","first-page":"1894","DOI":"10.1038\/s41375-024-02328-1","article-title":"Altered RNA export by SF3B1 mutants confers sensitivity to nuclear export inhibition","volume":"38","author":"Chaudhry","year":"2024","journal-title":"Leukemia"},{"key":"2025091917113043900_ref47","first-page":"523","article-title":"Nuclear UPF1 is associated with chromatin for transcription-coupled RNA surveillance","volume":"42","author":"Hong","year":"2019","journal-title":"Mol Cells"},{"key":"2025091917113043900_ref48","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1016\/j.stem.2018.08.007","article-title":"Single-cell RNA sequencing analysis reveals sequential cell fate transition during human spermatogenesis","volume":"23","author":"Wang","year":"2018","journal-title":"Cell Stem Cell"},{"key":"2025091917113043900_ref49","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"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioaf163\/63839306\/ioaf163.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/113\/3\/672\/63839306\/ioaf163.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/113\/3\/672\/63839306\/ioaf163.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,19]],"date-time":"2025-09-19T21:11:42Z","timestamp":1758316302000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/113\/3\/672\/8211703"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,24]]},"references-count":49,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2025,7,24]]},"published-print":{"date-parts":[[2025,9,15]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioaf163","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,9]]},"published":{"date-parts":[[2025,7,24]]}}}