{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T07:45:07Z","timestamp":1785829507569,"version":"3.56.0"},"reference-count":50,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2019,6,18]],"date-time":"2019-06-18T00:00:00Z","timestamp":1560816000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"DOI":"10.3389\/fphys.2019.00765","type":"journal-article","created":{"date-parts":[[2019,6,18]],"date-time":"2019-06-18T05:13:16Z","timestamp":1560834796000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":51,"title":["Overexpression of MicroRNA-10a in Germ Cells Causes Male Infertility by Targeting Rad51 in Mouse and Human"],"prefix":"10.3389","volume":"10","author":[{"given":"Huihui","family":"Gao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Wen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Congcong","family":"Cao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daqian","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chenhao","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shengsong","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xunbin","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xingxu","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuiqiao","family":"Yuan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wuzi","family":"Dong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2019,6,18]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1830","DOI":"10.1158\/1541-7786.MCR-08-0167","article-title":"Down-regulation of hsa-miR-10a in chronic myeloid leukemia CD34+ cells increases USF2-mediated cell growth.","volume":"6","author":"Agirre","year":"2008","journal-title":"Mol. Cancer Res."},{"key":"B2","doi-asserted-by":"publisher","first-page":"21686","DOI":"10.1074\/jbc.M111.328054","article-title":"MicroRNA-449 and microRNA-34b\/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway.","volume":"287","author":"Bao","year":"2012","journal-title":"J. Biol. Chem."},{"key":"B3","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1261\/rna.1963810","article-title":"Role of miR-34c microRNA in the late steps of spermatogenesis.","volume":"16","author":"Bouhallier","year":"2010","journal-title":"RNA"},{"key":"B4","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1126\/science.1085242","article-title":"Role of microRNAs in plant and animal development.","volume":"301","author":"Carrington","year":"2003","journal-title":"Science"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.2144\/000113764","article-title":"Isolation of Sertoli, Leydig, and spermatogenic cells from the mouse testis.","volume":"51","author":"Chang","year":"2011","journal-title":"Biotechniques"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gni178","article-title":"Real-time quantification of microRNAs by stem-loop RT-PCR.","volume":"33","author":"Chen","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"B7","doi-asserted-by":"publisher","first-page":"4142","DOI":"10.1093\/nar\/gkw1287","article-title":"MicroRNA-202 maintains spermatogonial stem cells by inhibiting cell cycle regulators and RNA binding proteins.","volume":"45","author":"Chen","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1004597","article-title":"Oligoasthenoteratozoospermia and infertility in mice deficient for miR-34b\/c and miR-449 loci.","volume":"10","author":"Comazzetto","year":"2014","journal-title":"PLoS Genet."},{"key":"B9","doi-asserted-by":"publisher","first-page":"64932","DOI":"10.18632\/oncotarget.10751","article-title":"miR-29 regulates Tet1 expression and contributes to early differentiation of mouse ESCs.","volume":"7","author":"Cui","year":"2016","journal-title":"Oncotarget"},{"key":"B10","doi-asserted-by":"publisher","first-page":"1383","DOI":"10.1016\/j.celrep.2017.01.024","article-title":"Meiotic knockdown and complementation reveals essential role of RAD51 in Mouse spermatogenesis.","volume":"18","author":"Dai","year":"2017","journal-title":"Cell. Rep."},{"key":"B11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/humrep\/13.suppl_1.1","article-title":"Spermatogenesis.","volume":"13","author":"de Kretser","year":"1998","journal-title":"Hum. Reprod."},{"key":"B12","doi-asserted-by":"publisher","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":"B13","doi-asserted-by":"publisher","first-page":"3560","DOI":"10.1073\/pnas.1016454108","article-title":"Molecular basis for enhancement of the meiotic DMC1 recombinase by RAD51 associated protein 1 (RAD51AP1).","volume":"108","author":"Dray","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B14","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1002\/dvg.20310","article-title":"Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre.","volume":"45","author":"Gallardo","year":"2007","journal-title":"Genesis"},{"key":"B15","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1016\/j.cell.2005.10.022","article-title":"Human RISC couples microRNA biogenesis and posttranscriptional gene silencing.","volume":"123","author":"Gregory","year":"2005","journal-title":"Cell"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0001738","article-title":"MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis.","volume":"3","author":"Hayashi","year":"2008","journal-title":"PLoS One"},{"key":"B17","doi-asserted-by":"publisher","first-page":"2205","DOI":"10.1002\/stem.1474","article-title":"MiRNA-20 and mirna-106a regulate spermatogonial stem cell renewal at the post-transcriptional level via targeting STAT3 and Ccnd1.","volume":"31","author":"He","year":"2013","journal-title":"Stem Cells"},{"key":"B18","doi-asserted-by":"publisher","first-page":"9383","DOI":"10.1074\/jbc.M109.095612","article-title":"miR-10a contributes to retinoid acid-induced smooth muscle cell differentiation.","volume":"285","author":"Huang","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B19","doi-asserted-by":"publisher","first-page":"309","DOI":"10.2164\/jandrol.111.014167","article-title":"Control of messenger RNA fate by RNA-binding proteins: an emphasis on mammalian spermatogenesis.","volume":"33","author":"Idler","year":"2012","journal-title":"J. Androl."},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1186\/s12885-015-1374-y","article-title":"MicroRNA-10a is reduced in breast cancer and regulated in part through retinoic acid.","volume":"15","author":"Khan","year":"2015","journal-title":"BMC Cancer"},{"key":"B21","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1007\/s00412-005-0334-8","article-title":"Mutant meiotic chromosome core components in mice can cause apparent sexual dimorphic endpoints at prophase or X-Y defective male-specific sterility.","volume":"114","author":"Kolas","year":"2005","journal-title":"Chromosoma"},{"key":"B22","doi-asserted-by":"publisher","first-page":"2474","DOI":"10.1073\/pnas.0510813103","article-title":"Retinoic acid regulates sex-specific timing of meiotic initiation in mice.","volume":"103","author":"Koubova","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B23","doi-asserted-by":"publisher","first-page":"380","DOI":"10.1016\/j.febslet.2014.12.024","article-title":"MiR-10a and miR-181c regulate collagen type I generation in hypertrophic scars by targeting PAI-1 and uPA.","volume":"589","author":"Li","year":"2015","journal-title":"FEBS Lett."},{"key":"B24","doi-asserted-by":"publisher","first-page":"R139","DOI":"10.1530\/REP-14-0431","article-title":"Mammalian gonocyte and spermatogonia differentiation: recent advances and remaining challenges.","volume":"149","author":"Manku","year":"2015","journal-title":"Reproduction"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.113.110502","article-title":"Toward a more precise and informative nomenclature describing fetal and neonatal male germ cells in rodents.","volume":"89","author":"McCarrey","year":"2013","journal-title":"Biol. Reprod."},{"key":"B26","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1089\/rej.2015.1719","article-title":"miR-204 regulates the proliferation of dairy goat spermatogonial stem cells via targeting to sirt1.","volume":"19","author":"Niu","year":"2016","journal-title":"Rejuvenation Res."},{"key":"B27","doi-asserted-by":"publisher","first-page":"12740","DOI":"10.1073\/pnas.1109987108","article-title":"MicroRNA-21 regulates the self-renewal of mouse spermatogonial stem cells.","volume":"108","author":"Niu","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B28","doi-asserted-by":"publisher","first-page":"5667","DOI":"10.1128\/mcb.21.16.5667-5677.2001","article-title":"A meiotic chromosomal core consisting of cohesin complex proteins recruits DNA recombination proteins and promotes synapsis in the absence of an axial element in mammalian meiotic cells.","volume":"21","author":"Pelttari","year":"2001","journal-title":"Mol. Cell Biol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1038\/nsmb923","article-title":"The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination.","volume":"12","author":"Petukhova","year":"2005","journal-title":"Nat. Struct. Mol. Biol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.taap.2016.06.010","article-title":"Epigenetic modification of miR-10a regulates renal damage by targeting CREB1 in type 2 diabetes mellitus.","volume":"306","author":"Shan","year":"2016","journal-title":"Toxicol. Appl. Pharmacol."},{"key":"B31","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1038\/ng0793-239","article-title":"Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA.","volume":"4","author":"Shinohara","year":"1993","journal-title":"Nat. Genet."},{"key":"B32","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1111\/boc.201200014","article-title":"MicroRNA signature in various cell types of mouse spermatogenesis: evidence for stage-specifically expressed miRNA-221, -203 and -34b-5p mediated spermatogenesis regulation.","volume":"104","author":"Smorag","year":"2012","journal-title":"Biol. Cell"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1111\/cpr.12297","article-title":"Reduced microRNA-188-3p expression contributes to apoptosis of spermatogenic cells in patients with azoospermia.","volume":"50","author":"Song","year":"2017","journal-title":"Cell. Prolif."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003913","article-title":"Loss of miR-10a activates lpo and collaborates with activated Wnt signaling in inducing intestinal neoplasia in female mice.","volume":"9","author":"Stadthagen","year":"2013","journal-title":"PLoS Genet."},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0076004","article-title":"Targeted gene deletion of miRNAs in mice by TALEN system.","volume":"8","author":"Takada","year":"2013","journal-title":"PLoS One"},{"key":"B36","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/bs.ctdb.2016.11.013","article-title":"Roles of retinoic acid in germ cell differentiation.","volume":"125","author":"Teletin","year":"2017","journal-title":"Curr. Top. Dev. Biol."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1038\/cddis.2013.138","article-title":"The targeting and functions of miRNA-383 are mediated by FMRP during spermatogenesis.","volume":"4","author":"Tian","year":"2013","journal-title":"Cell Death Dis."},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.111.096313","article-title":"Two miR NAclusters, Mir-17-92 (Mirc1) and Mir-106b-25 (Mirc3), are involved in the regulation of spermatogonial differentiation in mice.","volume":"86","author":"Tong","year":"2012","journal-title":"Biol. Reprod."},{"key":"B39","doi-asserted-by":"publisher","DOI":"10.1186\/1477-7827-12-85","article-title":"MicroRNA-34 family expression in bovine gametes and preimplantation embryos.","volume":"12","author":"Tscherner","year":"2014","journal-title":"Reprod. Biol. Endocrinol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1007\/s00246-014-0901-y","article-title":"miR-10a and miR-10b target the 3\u2032-untranslated region of TBX5 to repress its expression.","volume":"35","author":"Wang","year":"2014","journal-title":"Pediatr. Cardiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"3115","DOI":"10.12659\/msm.894554","article-title":"MiR-29 Induces K562 cell apoptosis by down-regulating FoxM1.","volume":"21","author":"Wang","year":"2015","journal-title":"Med. Sci. Monit."},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1038\/cddis.2013.184","article-title":"miR-29 targets Akt3 to reduce proliferation and facilitate differentiation of myoblasts in skeletal muscle development.","volume":"4","author":"Wei","year":"2013","journal-title":"Cell Death Dis."},{"key":"B43","doi-asserted-by":"publisher","first-page":"2136","DOI":"10.1053\/j.gastro.2009.08.065","article-title":"Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer.","volume":"137","author":"Weiss","year":"2009","journal-title":"Gastroenterology"},{"key":"B44","doi-asserted-by":"publisher","first-page":"E2851","DOI":"10.1073\/pnas.1407777111","article-title":"Two miRclusters, N. A., miR-34b\/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis.","volume":"111","author":"Wu","year":"2014","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.112.104034","article-title":"Lcn5 promoter directs the region-specific expression of cre recombinase in caput epididymidis of transgenic mice.","volume":"88","author":"Xie","year":"2013","journal-title":"Biol. Reprod."},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0016235","article-title":"Discovery of porcine microRNAs in multiple tissues by a Solexa deep sequencing approach.","volume":"6","author":"Xie","year":"2011","journal-title":"PLoS One"},{"key":"B47","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1242\/dev.087403","article-title":"MicroRNAs 221 and 222 regulate the undifferentiated state in mammalian male germ cells.","volume":"140","author":"Yang","year":"2013","journal-title":"Development"},{"key":"B48","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1530\/REP-14-0643","article-title":"MicroRNAs and DNA methylation as epigenetic regulators of mitosis, meiosis and spermiogenesis.","volume":"150","author":"Yao","year":"2015","journal-title":"Reproduction"},{"key":"B49","doi-asserted-by":"publisher","first-page":"E430","DOI":"10.1073\/pnas.1424648112","article-title":"Spata6 is required for normal assembly of the sperm connecting piece and tight head-tail conjunction.","volume":"112","author":"Yuan","year":"","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B50","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1242\/bio.201410959","article-title":"mir-34b\/c and mir-449a\/b\/c are required for spermatogenesis, but not for the first cleavage division in mice.","volume":"4","author":"Yuan","year":"","journal-title":"Biol. Open"}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fphys.2019.00765\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,6,18]],"date-time":"2019-06-18T05:13:19Z","timestamp":1560834799000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/article\/10.3389\/fphys.2019.00765\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,6,18]]},"references-count":50,"alternative-id":["10.3389\/fphys.2019.00765"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2019.00765","relation":{},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,6,18]]},"article-number":"765"}}