{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,23]],"date-time":"2026-07-23T09:57:00Z","timestamp":1784800620463,"version":"3.55.0"},"reference-count":41,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-017"},{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-012"},{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2023,4,1]],"date-time":"2023-04-01T00:00:00Z","timestamp":1680307200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-004"}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Reproductive Toxicology"],"published-print":{"date-parts":[[2023,4]]},"DOI":"10.1016\/j.reprotox.2023.108340","type":"journal-article","created":{"date-parts":[[2023,1,30]],"date-time":"2023-01-30T21:28:52Z","timestamp":1675114132000},"page":"108340","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":20,"special_numbering":"C","title":["Sertoli cells-derived exosomal miR-30a-5p regulates ubiquitin E3 ligase Zeb2 to affect the spermatogonial stem cells proliferation and differentiation"],"prefix":"10.1016","volume":"117","author":[{"given":"Bin","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chengxi","family":"Zhai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingzhong","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhu","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.reprotox.2023.108340_bib1","unstructured":"S.W. Leslie, L.E. Siref, T.L. Soon-Sutton, M.A.B. Khan, Male Infertility, StatPearls, Treasure Island (FL), 2022."},{"key":"10.1016\/j.reprotox.2023.108340_bib2","unstructured":"\u3008https:\/\/www.who.int\/health-topics\/infertility#tab=tab_1\u3009."},{"key":"10.1016\/j.reprotox.2023.108340_bib3","doi-asserted-by":"crossref","DOI":"10.12688\/f1000research.17076.1","article-title":"Recent advances in understanding and managing male infertility","volume":"8","author":"Fainberg","year":"2019","journal-title":"F1000Res"},{"issue":"18","key":"10.1016\/j.reprotox.2023.108340_bib4","doi-asserted-by":"crossref","first-page":"S35","DOI":"10.12968\/bjon.2016.25.18.S35","article-title":"Male infertility: an overview of causes and treatment options","volume":"25","author":"Leaver","year":"2016","journal-title":"Br. J. Nurs."},{"issue":"1","key":"10.1016\/j.reprotox.2023.108340_bib5","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.aju.2017.11.015","article-title":"Spermatogonial stem cell transplantation and male infertility: current status and future directions","volume":"16","author":"Forbes","year":"2018","journal-title":"Arab J. Urol."},{"issue":"4","key":"10.1016\/j.reprotox.2023.108340_bib6","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"},{"issue":"3","key":"10.1016\/j.reprotox.2023.108340_bib7","doi-asserted-by":"crossref","DOI":"10.3390\/cells9030745","article-title":"Spermatogonial stem cells for in vitro spermatogenesis and in vivo restoration of fertility","volume":"9","author":"Ibtisham","year":"2020","journal-title":"Cells"},{"issue":"1","key":"10.1016\/j.reprotox.2023.108340_bib8","doi-asserted-by":"crossref","DOI":"10.1111\/cpr.12933","article-title":"FGF9 promotes mouse spermatogonial stem cell proliferation mediated by p38 MAPK signalling","volume":"54","author":"Yang","year":"2021","journal-title":"Cell Prolif."},{"key":"10.1016\/j.reprotox.2023.108340_bib9","doi-asserted-by":"crossref","DOI":"10.1038\/cddis.2015.56","article-title":"Fgf9 inhibition of meiotic differentiation in spermatogonia is mediated by Erk-dependent activation of Nodal-Smad2\/3 signaling and is antagonized by Kit Ligand","volume":"6","author":"Tassinari","year":"2015","journal-title":"Cell Death Dis."},{"issue":"Pt 6","key":"10.1016\/j.reprotox.2023.108340_bib10","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1242\/jcs.057968","article-title":"Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells","volume":"123","author":"Barrios","year":"2010","journal-title":"J. Cell Sci."},{"issue":"8","key":"10.1016\/j.reprotox.2023.108340_bib11","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1038\/s41419-019-1782-z","article-title":"Multiple signaling pathways in Sertoli cells: recent findings in spermatogenesis","volume":"10","author":"Ni","year":"2019","journal-title":"Cell Death Dis."},{"issue":"2","key":"10.1016\/j.reprotox.2023.108340_bib12","doi-asserted-by":"crossref","DOI":"10.1016\/j.celrep.2020.03.077","article-title":"Distinct roles for Rac1 in sertoli cell function during testicular development and spermatogenesis","volume":"31","author":"Heinrich","year":"2020","journal-title":"Cell Rep."},{"issue":"8","key":"10.1016\/j.reprotox.2023.108340_bib13","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1002\/mrd.23402","article-title":"Characterization of rodent Sertoli cell primary cultures","volume":"87","author":"Zomer","year":"2020","journal-title":"Mol. Reprod. Dev."},{"issue":"16","key":"10.1016\/j.reprotox.2023.108340_bib14","doi-asserted-by":"crossref","first-page":"2968","DOI":"10.1038\/s41388-021-01753-1","article-title":"METTL3-mediated m(6)A methylation of SPHK2 promotes gastric cancer progression by targeting KLF2","volume":"40","author":"Huo","year":"2021","journal-title":"Oncogene"},{"issue":"1","key":"10.1016\/j.reprotox.2023.108340_bib15","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1093\/biolre\/ioy027","article-title":"50 years of spermatogenesis: Sertoli cells and their interactions with germ cells","volume":"99","author":"Griswold","year":"2018","journal-title":"Biol. Reprod."},{"issue":"8","key":"10.1016\/j.reprotox.2023.108340_bib16","doi-asserted-by":"crossref","first-page":"3950","DOI":"10.1111\/jcmm.16347","article-title":"Sertoli cell-derived exosomal MicroRNA-486-5p regulates differentiation of spermatogonial stem cell through PTEN in mice","volume":"25","author":"Li","year":"2021","journal-title":"J. Cell Mol. Med."},{"issue":"24","key":"10.1016\/j.reprotox.2023.108340_bib17","doi-asserted-by":"crossref","first-page":"25528","DOI":"10.18632\/aging.104158","article-title":"miRNA-122-5p stimulates the proliferation and DNA synthesis and inhibits the early apoptosis of human spermatogonial stem cells by targeting CBL and competing with lncRNA CASC7","volume":"12","author":"Zhou","year":"2020","journal-title":"Aging (Albany NY)"},{"issue":"3","key":"10.1016\/j.reprotox.2023.108340_bib18","doi-asserted-by":"crossref","first-page":"184","DOI":"10.1002\/cbf.3263","article-title":"MicroRNA-10b regulates the renewal of spermatogonial stem cells through Kruppel-like factor 4","volume":"35","author":"Li","year":"2017","journal-title":"Cell Biochem Funct."},{"issue":"8","key":"10.1016\/j.reprotox.2023.108340_bib19","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1002\/mrd.22843","article-title":"miR-100 promotes the proliferation of spermatogonial stem cells via regulating Stat3","volume":"84","author":"Huang","year":"2017","journal-title":"Mol. Reprod. Dev."},{"issue":"1","key":"10.1016\/j.reprotox.2023.108340_bib20","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1095\/biolreprod.112.103747","article-title":"MicroRNA 146 (Mir146) modulates spermatogonial differentiation by retinoic acid in mice","volume":"88","author":"Huszar","year":"2013","journal-title":"Biol. Reprod."},{"issue":"2","key":"10.1016\/j.reprotox.2023.108340_bib21","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1002\/jcb.24655","article-title":"miR-34c enhances mouse spermatogonial stem cells differentiation by targeting Nanos2","volume":"115","author":"Yu","year":"2014","journal-title":"J. Cell Biochem"},{"issue":"10","key":"10.1016\/j.reprotox.2023.108340_bib22","doi-asserted-by":"crossref","first-page":"1734","DOI":"10.1242\/dev.076539","article-title":"FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activation","volume":"139","author":"Ishii","year":"2012","journal-title":"Development"},{"issue":"6","key":"10.1016\/j.reprotox.2023.108340_bib23","doi-asserted-by":"crossref","first-page":"774","DOI":"10.1016\/j.stem.2013.04.001","article-title":"ROS are required for mouse spermatogonial stem cell self-renewal","volume":"12","author":"Morimoto","year":"2013","journal-title":"Cell Stem Cell"},{"issue":"7","key":"10.1016\/j.reprotox.2023.108340_bib24","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1016\/j.immuni.2021.04.015","article-title":"Differential usage of transcriptional repressor Zeb2 enhancers distinguishes adult and embryonic hematopoiesis","volume":"54","author":"Huang","year":"2021","journal-title":"Immunity"},{"issue":"9","key":"10.1016\/j.reprotox.2023.108340_bib25","doi-asserted-by":"crossref","first-page":"963","DOI":"10.2174\/15680096113136660102","article-title":"The role of snail in EMT and tumorigenesis","volume":"13","author":"Wang","year":"2013","journal-title":"Curr. Cancer Drug Targets"},{"issue":"19","key":"10.1016\/j.reprotox.2023.108340_bib26","doi-asserted-by":"crossref","DOI":"10.3390\/ijms21197315","article-title":"STAT3 mediated miR-30a-5p inhibition enhances proliferation and inhibits apoptosis in colorectal cancer cells","volume":"21","author":"Cheng","year":"2020","journal-title":"Int J. Mol. Sci."},{"issue":"12","key":"10.1016\/j.reprotox.2023.108340_bib27","doi-asserted-by":"crossref","first-page":"3604","DOI":"10.7150\/jca.41437","article-title":"MiR-30a-5p promotes cholangiocarcinoma cell proliferation through targeting SOCS3","volume":"11","author":"Zhang","year":"2020","journal-title":"J. Cancer"},{"issue":"3","key":"10.1016\/j.reprotox.2023.108340_bib28","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1038\/s41419-018-0444-x","article-title":"MicroRNA-30a-5p inhibits gallbladder cancer cell proliferation, migration and metastasis by targeting E2F7","volume":"9","author":"Ye","year":"2018","journal-title":"Cell Death Dis."},{"issue":"11","key":"10.1016\/j.reprotox.2023.108340_bib29","first-page":"5203","article-title":"MiR-30a-5p accelerates adipogenesis by negatively regulating Sirtuin 1","volume":"11","author":"Cui","year":"2018","journal-title":"Int J. Clin. Exp. Pathol."},{"issue":"1","key":"10.1016\/j.reprotox.2023.108340_bib30","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1186\/s10020-020-00219-6","article-title":"Long noncoding RNA HCG18 inhibits the differentiation of human bone marrow-derived mesenchymal stem cells in osteoporosis by targeting miR-30a-5p\/NOTCH1 axis","volume":"26","author":"Che","year":"2020","journal-title":"Mol. Med."},{"issue":"7","key":"10.1016\/j.reprotox.2023.108340_bib31","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1080\/15384101.2020.1731946","article-title":"The Lnc LINC00461\/miR-30a-5p facilitates progression and malignancy in non-small cell lung cancer via regulating ZEB2","volume":"19","author":"Li","year":"2020","journal-title":"Cell Cycle"},{"issue":"6","key":"10.1016\/j.reprotox.2023.108340_bib32","doi-asserted-by":"crossref","DOI":"10.1038\/cddis.2017.252","article-title":"The putative tumor suppressor microRNA-30a-5p modulates clear cell renal cell carcinoma aggressiveness through repression of ZEB2","volume":"8","author":"Chen","year":"2017","journal-title":"Cell Death Dis."},{"issue":"4","key":"10.1016\/j.reprotox.2023.108340_bib33","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.repbio.2020.07.002","article-title":"A review on the stem cell therapy and an introduction to exosomes as a new tool in reproductive medicine","volume":"20","author":"Kharazi","year":"2020","journal-title":"Reprod. Biol."},{"issue":"2","key":"10.1016\/j.reprotox.2023.108340_bib34","doi-asserted-by":"crossref","DOI":"10.3390\/biom11020249","article-title":"Control of gene expression by exosome-derived non-coding RNAs in cancer angiogenesis and lymphangiogenesis","volume":"11","author":"Arcucci","year":"2021","journal-title":"Biomolecules"},{"issue":"5","key":"10.1016\/j.reprotox.2023.108340_bib35","doi-asserted-by":"crossref","first-page":"1287","DOI":"10.1111\/brv.12608","article-title":"Exosome-mediated effects and applications in inflammatory bowel disease","volume":"95","author":"Ocansey","year":"2020","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"issue":"2","key":"10.1016\/j.reprotox.2023.108340_bib36","first-page":"182","article-title":"Extracellular vesicles: roles in gamete maturation, fertilization and embryo implantation","volume":"22","author":"Machtinger","year":"2016","journal-title":"Hum. Reprod. Update"},{"issue":"5","key":"10.1016\/j.reprotox.2023.108340_bib37","doi-asserted-by":"crossref","DOI":"10.3390\/cells9051157","article-title":"Mesenchymal stem\/stromal cell-derived exosomes for immunomodulatory therapeutics and skin regeneration","volume":"9","author":"Ha","year":"2020","journal-title":"Cells"},{"issue":"4","key":"10.1016\/j.reprotox.2023.108340_bib38","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1161\/CIRCRESAHA.118.313845","article-title":"Aggregation of child cardiac progenitor cells into spheres activates notch signaling and improves treatment of right ventricular heart failure","volume":"124","author":"Trac","year":"2019","journal-title":"Circ. Res."},{"issue":"7","key":"10.1016\/j.reprotox.2023.108340_bib39","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1038\/mt.2013.64","article-title":"Grape exosome-like nanoparticles induce intestinal stem cells and protect mice from DSS-induced colitis","volume":"21","author":"Ju","year":"2013","journal-title":"Mol. Ther."},{"issue":"5","key":"10.1016\/j.reprotox.2023.108340_bib40","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1161\/STROKEAHA.117.018292","article-title":"Exosome therapy for stroke","volume":"49","author":"Chen","year":"2018","journal-title":"Stroke"},{"issue":"10","key":"10.1016\/j.reprotox.2023.108340_bib41","doi-asserted-by":"crossref","first-page":"2910","DOI":"10.7150\/thno.30879","article-title":"M2 microglia-derived exosomes protect the mouse brain from ischemia-reperfusion injury via exosomal miR-124","volume":"9","author":"Song","year":"2019","journal-title":"Theranostics"}],"container-title":["Reproductive Toxicology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0890623823000138?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0890623823000138?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T14:00:31Z","timestamp":1760191231000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0890623823000138"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4]]},"references-count":41,"alternative-id":["S0890623823000138"],"URL":"https:\/\/doi.org\/10.1016\/j.reprotox.2023.108340","relation":{},"ISSN":["0890-6238"],"issn-type":[{"value":"0890-6238","type":"print"}],"subject":[],"published":{"date-parts":[[2023,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Sertoli cells-derived exosomal miR-30a-5p regulates ubiquitin E3 ligase Zeb2 to affect the spermatogonial stem cells proliferation and differentiation","name":"articletitle","label":"Article Title"},{"value":"Reproductive Toxicology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.reprotox.2023.108340","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 Published by Elsevier Inc.","name":"copyright","label":"Copyright"}],"article-number":"108340"}}