{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T19:01:02Z","timestamp":1790190062649,"version":"4.1.0"},"reference-count":69,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2024,8,19]],"date-time":"2024-08-19T00:00:00Z","timestamp":1724025600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Natural Young Science Foundation of Fujian Province","award":["2022J05149"],"award-info":[{"award-number":["2022J05149"]}]},{"name":"Natural Young Science Foundation of Fujian Province","award":["32273127"],"award-info":[{"award-number":["32273127"]}]},{"name":"Natural Young Science Foundation of Fujian Province","award":["31771648"],"award-info":[{"award-number":["31771648"]}]},{"name":"Natural Young Science Foundation of Fujian Province","award":["31672653"],"award-info":[{"award-number":["31672653"]}]},{"name":"Natural Young Science Foundation of Fujian Province","award":["JAT210233"],"award-info":[{"award-number":["JAT210233"]}]},{"name":"Natural Young Science Foundation of Fujian Province","award":["ZQ2020003"],"award-info":[{"award-number":["ZQ2020003"]}]},{"name":"Natural Young Science Foundation of Fujian Province","award":["ZQ2022001"],"award-info":[{"award-number":["ZQ2022001"]}]},{"name":"National Natural Science Foundation of China","award":["2022J05149"],"award-info":[{"award-number":["2022J05149"]}]},{"name":"National Natural Science Foundation of China","award":["32273127"],"award-info":[{"award-number":["32273127"]}]},{"name":"National Natural Science Foundation of China","award":["31771648"],"award-info":[{"award-number":["31771648"]}]},{"name":"National Natural Science Foundation of China","award":["31672653"],"award-info":[{"award-number":["31672653"]}]},{"name":"National Natural Science Foundation of China","award":["JAT210233"],"award-info":[{"award-number":["JAT210233"]}]},{"name":"National Natural Science Foundation of China","award":["ZQ2020003"],"award-info":[{"award-number":["ZQ2020003"]}]},{"name":"National Natural Science Foundation of China","award":["ZQ2022001"],"award-info":[{"award-number":["ZQ2022001"]}]},{"name":"Fujian Provincial Department of Education","award":["2022J05149"],"award-info":[{"award-number":["2022J05149"]}]},{"name":"Fujian Provincial Department of Education","award":["32273127"],"award-info":[{"award-number":["32273127"]}]},{"name":"Fujian Provincial Department of Education","award":["31771648"],"award-info":[{"award-number":["31771648"]}]},{"name":"Fujian Provincial Department of Education","award":["31672653"],"award-info":[{"award-number":["31672653"]}]},{"name":"Fujian Provincial Department of Education","award":["JAT210233"],"award-info":[{"award-number":["JAT210233"]}]},{"name":"Fujian Provincial Department of Education","award":["ZQ2020003"],"award-info":[{"award-number":["ZQ2020003"]}]},{"name":"Fujian Provincial Department of Education","award":["ZQ2022001"],"award-info":[{"award-number":["ZQ2022001"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["2022J05149"],"award-info":[{"award-number":["2022J05149"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["32273127"],"award-info":[{"award-number":["32273127"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["31771648"],"award-info":[{"award-number":["31771648"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["31672653"],"award-info":[{"award-number":["31672653"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["JAT210233"],"award-info":[{"award-number":["JAT210233"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["ZQ2020003"],"award-info":[{"award-number":["ZQ2020003"]}]},{"name":"Scientific Research Foundation of Jimei University","award":["ZQ2022001"],"award-info":[{"award-number":["ZQ2022001"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Research across various species has demonstrated that the doublesex and mab-3-related transcription factor 3 (dmrt3) plays pivotal roles in testis development. However, the precise molecular mechanisms of dmrt3 remain unclear. In this study, we investigated the role of dmrt3 (dmrt3a) in testis development using the model organism medaka (Oryzias latipes). SqRT-PCR and ISH analyses revealed that dmrt3a is predominantly expressed in the testis, especially in the spermatid and spermatozoon. Using CRISPR\/Cas9, we generated two dmrt3a homozygous mutants (-8 bp and -11 bp), which exhibited significantly reduced fertilization rates and embryo production. Additionally, the number of germ cells and sperm motility were markedly decreased in the dmrt3a mutants, manifesting as the symptoms of asthenozoospermia and oligozoospermia. Interestingly, RNA-Seq analysis showed that the deficiency of dmrt3a could lead to a significant downregulation of numerous genes related to gonadal development and severe disruptions in mitochondrial function. These results suggested that dmrt3a is essential for spermatogenesis and spermatozoa energy production. This paper provides new insights and perspectives for further exploring the molecular mechanisms underlying spermatogenesis and addressing male reproductive issues.<\/jats:p>","DOI":"10.3390\/ani14162406","type":"journal-article","created":{"date-parts":[[2024,8,19]],"date-time":"2024-08-19T10:11:28Z","timestamp":1724062288000},"page":"2406","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Medaka (Oryzias latipes) Dmrt3a Is Involved in Male Fertility"],"prefix":"10.3390","volume":"14","author":[{"given":"Ju","family":"Deng","sequence":"first","affiliation":[{"name":"State Key Laboratory of Mariculture Breeding, Engineering Research Center of the Modern Technology for Eel Industry, Ministry of Education, Jimei University, Xiamen 361021, China"},{"name":"Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen 361021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-3492-274X","authenticated-orcid":false,"given":"Yan","family":"Huang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Mariculture Breeding, Engineering Research Center of the Modern Technology for Eel Industry, Ministry of Education, Jimei University, Xiamen 361021, China"},{"name":"Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen 361021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0000-2813-0948","authenticated-orcid":false,"given":"Jingjie","family":"Liang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Mariculture Breeding, Engineering Research Center of the Modern Technology for Eel Industry, Ministry of Education, Jimei University, Xiamen 361021, China"},{"name":"Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen 361021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-2156-696X","authenticated-orcid":false,"given":"Yuewen","family":"Jiang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Mariculture Breeding, Engineering Research Center of the Modern Technology for Eel Industry, Ministry of Education, Jimei University, Xiamen 361021, China"},{"name":"Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen 361021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4763-2307","authenticated-orcid":false,"given":"Tiansheng","family":"Chen","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Mariculture Breeding, Engineering Research Center of the Modern Technology for Eel Industry, Ministry of Education, Jimei University, Xiamen 361021, China"},{"name":"Key Laboratory of Healthy Mariculture for the East China Sea, Ministry of Agriculture and Rural Affairs, Fisheries College, Jimei University, Xiamen 361021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,8,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1146\/annurev-animal-020518-115239","article-title":"Spermatogonial Stem Cell Transplantation: Insights and Outlook for Domestic Animals","volume":"7","author":"Giassetti","year":"2019","journal-title":"Annu. Rev. Anim. Biosci."},{"key":"ref_2","unstructured":"Birkhead, T.R., Hosken, D.J., and Pitnick, S. (2009). 3\u2014Sperm morphological diversity. Sperm Biology, Academic Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.ygcen.2009.02.013","article-title":"Spermatogenesis in fish","volume":"165","author":"Schulz","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.semcdb.2016.04.009","article-title":"Spermatogenesis in humans and its affecting factors","volume":"59","author":"Neto","year":"2016","journal-title":"Semin. Cell. Dev. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1017\/S0967199419000558","article-title":"Function of leukaemia inhibitory factor in spermatogenesis of a teleost fish, the medaka Oryzias latipes","volume":"27","author":"Satoh","year":"2019","journal-title":"Zygote"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Matsuyama, S., and Defalco, T. (2024). Steroid hormone signaling: Multifaceted support of testicular function. Front. Cell. Dev. Biol., 11.","DOI":"10.3389\/fcell.2023.1339385"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.scr.2017.07.026","article-title":"DMRT proteins and coordination of mammalian spermatogenesis","volume":"24","author":"Zhang","year":"2017","journal-title":"Stem Cell Res."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Zhang, Q., Huang, J., Fu, Y., Chen, J., and Wang, W. (2024). Genome-wide identification and expression profiles of sex-related gene families in the Pacific abalone Haliotis discus hannai. Comp. Biochem. Physiol. Part D Genom. Proteomics, 50.","DOI":"10.1016\/j.cbd.2024.101205"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Zhao, H.X., Xiao, Y.S., Xiao, Z.Z., Wu, Y.D., Ma, Y.T., and Li, J. (2024). Genome-wide investigation of the DMRT gene family sheds new insight into the regulation of sex differentiation in spotted knifejaw (Oplegnathus punctatus) with fusion chromosomes (Y). Int. J. Biol. Macromol., 257.","DOI":"10.1016\/j.ijbiomac.2023.128638"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1016\/j.jconrel.2023.09.027","article-title":"Exosome delivery to the testes for dmrt1 suppression: A powerful tool for sex-determining gene studies","volume":"363","author":"Zhu","year":"2023","journal-title":"J. Control. Release"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Xu, S.Q., Zhang, S.Y., Zhang, W.P., Liu, H.Y., Wang, M.H., Zhong, L.Q., Bian, W.J., and Chen, X.H. (2022). Genome-Wide Identification, Phylogeny, and Expression Profile of the Dmrt (Doublesex and Mab-3 Related Transcription Factor) Gene Family in Channel Catfish (Ictalurus punctatus). Front. Genet., 13.","DOI":"10.3389\/fgene.2022.891204"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1038\/nature10239","article-title":"DMRT1 prevents female reprogramming in the postnatal mammalian testis","volume":"476","author":"Matson","year":"2011","journal-title":"Nature"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.fertnstert.2022.10.032","article-title":"Functional assessment of DMRT1 variants and their pathogenicity for isolated male infertility","volume":"119","author":"Emich","year":"2023","journal-title":"Fertil. Steril."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2587","DOI":"10.1101\/gad.834100","article-title":"Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation","volume":"14","author":"Raymond","year":"2000","journal-title":"Genes. Dev."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Agbor, V.A., Tao, S., Lei, N., and Heckert, L.L. (2013). A Wt1-Dmrt1 transgene restores DMRT1 to sertoli cells of Dmrt1(-\/-) testes: A novel model of DMRT1-deficient germ cells. Biol. Reprod., 88.","DOI":"10.1095\/biolreprod.112.103135"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1007\/s11033-009-9619-y","article-title":"Exogenous cMHM regulates the expression of DMRT1 and ER alpha in avian testes","volume":"37","author":"Yang","year":"2010","journal-title":"Mol. Biol. Rep."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"11778","DOI":"10.1073\/pnas.182314699","article-title":"A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes","volume":"99","author":"Nanda","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1002\/2211-5463.12035","article-title":"Sexually dimorphic expression of Dmrt1 and \u03b3H2AX in germ stem cells during gonadal development in Xenopus laevis","volume":"6","author":"Fujitani","year":"2016","journal-title":"FEBS. Open. Bio"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.diff.2018.02.004","article-title":"Transcriptome analysis identifies genes involved in sex determination and development of Xenopus laevis gonads","volume":"100","author":"Piprek","year":"2018","journal-title":"Differentiation"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Dong, J., Li, J., Hu, J., Sun, C., Tian, Y., Li, W., Yan, N., Sun, C., Sheng, X., and Yang, S. (2020). Comparative Genomics Studies on the dmrt Gene Family in Fish. Front. Genet., 11.","DOI":"10.3389\/fgene.2020.563947"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.gene.2012.06.021","article-title":"Sex dimorphic expression of five dmrt genes identified in the Atlantic cod genome. The fish-specific dmrt2b diverged from dmrt2a before the fish whole-genome duplication","volume":"505","author":"Johnsen","year":"2012","journal-title":"Gene"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.fertnstert.2020.03.041","article-title":"New findings in disorders of sex development: Role of DMRT3 and OAS3","volume":"114","author":"Rojas","year":"2020","journal-title":"Fertil. Steril."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.ygeno.2006.07.017","article-title":"DMRT gene cluster analysis in the platypus: New insights into genomic organization and regulatory regions","volume":"89","author":"Wakefield","year":"2007","journal-title":"Genomics"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Ahituv, N., Zhu, Y., Visel, A., Holt, A., Afzal, V., Pennacchio, L.A., and Rubin, E.M. (2007). Deletion of ultraconserved elements yields viable mice. PLoS. Biol., 5.","DOI":"10.1371\/journal.pbio.0050234"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Bai, D.P., Chen, Y., Hu, Y.Q., He, W.F., Shi, Y.Z., Fan, Q.M., Luo, R.T., and Li, A. (2020). Transcriptome analysis of genes related to gonad differentiation and development in Muscovy ducks. Bmc. Genom., 21.","DOI":"10.1186\/s12864-020-06852-z"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.cbd.2005.08.003","article-title":"Expression of the DMRT gene and its roles in early gonadal development of the Japanese pufferfish Takifugu rubripes","volume":"1","author":"Yamaguchi","year":"2006","journal-title":"Comp. Biochem. Physiol. Part D Genom. Proteomics"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1002\/dvdy.20158","article-title":"Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes","volume":"231","author":"Kobayashi","year":"2004","journal-title":"Dev. Dyn."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1111\/j.1742-4658.2011.08030.x","article-title":"Dmrt1 genes at the crossroads: A widespread and central class of sexual development factors in fish","volume":"278","author":"Herpin","year":"2011","journal-title":"Febs. J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1038\/nature751","article-title":"DMY is a Y-specific DM-domain gene required for male development in the medaka fish","volume":"417","author":"Matsuda","year":"2002","journal-title":"Nature"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.ygcen.2015.10.004","article-title":"Evolution of the sex-determining gene in the teleostean genus Oryzias","volume":"239","author":"Matsuda","year":"2016","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1534\/genetics.114.173849","article-title":"The genomic and genetic toolbox of the teleost medaka (Oryzias latipes)","volume":"199","author":"Kirchmaier","year":"2015","journal-title":"Genetics"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.mce.2019.01.017","article-title":"Japanese medaka as a model for studying the relaxin family genes involved in neuroendocrine regulation: Insights from the expression of fish-specific rln3 and insl5 and rxfp3\/4-type receptor paralogues","volume":"487","author":"Alnafea","year":"2019","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Chen, L., Huang, Y., Pan, Q.-H., Wang, M.-Y., Liang, J.-J., and Chen, T.-S. (2024). The Chinese medaka (Oryzias sinensis) dmrt1 gene converts females to males in medaka (Oryzias latipes). Biochim. Biophys. Acta (BBA)-Gen. Subj., 1868.","DOI":"10.1016\/j.bbagen.2024.130664"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1007\/s10142-023-01090-4","article-title":"Japanese medaka Olpax6.1 mutant as a potential model for spondylo-ocular syndrome","volume":"23","author":"Pan","year":"2023","journal-title":"Funct. Integr. Genom."},{"key":"ref_35","unstructured":"(2011). National Committee for the Update of the Guide for the Care and Use of Laboratory. Guide for the Care and Use of Laboratory Animals, Eighth Edition, The National Academies Press."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1002\/jez.b.22760","article-title":"Maternal inheritance of Nanog ortholog in blunt-snout bream","volume":"328","author":"Yu","year":"2017","journal-title":"J. Exp. Zool. Part B Mol. Dev. Evol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1631\/jzus.B2100343","article-title":"Efficient gene editing in a medaka (Oryzias latipes) cell line and embryos by SpCas9\/tRNA-gRNA","volume":"23","author":"Pan","year":"2022","journal-title":"J. Zhejiang Univ. Sci. B"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1002\/jez.b.22808","article-title":"Generation of albino medaka (Oryzias latipes) by CRISPR\/Cas9","volume":"330","author":"Fang","year":"2018","journal-title":"J. Exp. Zool. Part B Mol. Dev. Evol."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Huang, Y., Wang, W.F., Huang, C.X., Li, X.H., Liu, H., and Wang, H.L. (2022). miR-731 modulates the zebrafish heart morphogenesis via targeting Calcineurin\/Nfatc3a pathway. Biochim. Biophys. Acta. Gen. Subj., 1866.","DOI":"10.1016\/j.bbagen.2022.130133"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1016\/j.mod.2004.03.012","article-title":"Stages of normal development in the medaka Oryzias latipes","volume":"121","author":"Iwamatsu","year":"2004","journal-title":"Mech. Dev."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/s00427-017-0583-6","article-title":"Black carp vasa identifies embryonic and gonadal germ cells","volume":"227","author":"Xue","year":"2017","journal-title":"Dev. Genes. Evol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1038\/nmeth.1226","article-title":"Mapping and quantifying mammalian transcriptomes by RNA-Seq","volume":"5","author":"Mortazavi","year":"2008","journal-title":"Nat. Methods"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1111\/and.12423","article-title":"Seminal cyclooxygenase relationship with oxidative stress in infertile oligoasthenoteratozoospermic men with varicocele","volume":"48","author":"Mostafa","year":"2016","journal-title":"Andrologia"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.theriogenology.2017.02.015","article-title":"The relationship. between mitochondrial DNA copy number and stallion sperm function","volume":"94","author":"Darr","year":"2017","journal-title":"Theriogenology"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.fertnstert.2020.03.008","article-title":"Genetic analysis of a Taiwanese family identifies a DMRT3-OAS3 interaction that is involved in human sexual differentiation through the regulation of ESR1 expression","volume":"114","author":"Tsai","year":"2020","journal-title":"Fertil. Steril."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1042\/BC20070114","article-title":"Nuclear localization, DNA binding and restricted expression in neural and germ cells of zebrafish Dmrt3","volume":"100","author":"Li","year":"2008","journal-title":"Biol. Cell."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Zeng, Y.T., Zheng, H.Q., He, C., Zhang, C.X., Zhang, H.K., and Zheng, H.P. (2024). Genome-wide identification and expression analysis of Dmrt gene family and their role in gonad development of Pacific oyster (Crassostrea gigas). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 269.","DOI":"10.1016\/j.cbpb.2023.110904"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3829","DOI":"10.1007\/s00018-013-1288-2","article-title":"Expanding roles for the evolutionarily conserved Dmrt sex transcriptional regulators during embryogenesis","volume":"70","author":"Bellefroid","year":"2013","journal-title":"Cell. Mol. Life. Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.tig.2012.02.002","article-title":"Dmrt genes in the development and evolution of sexual dimorphism","volume":"28","author":"Kopp","year":"2012","journal-title":"Trends. Genet."},{"key":"ref_50","first-page":"1406","article-title":"Genomic organization and phylogenetic and temporal-spatial expres sion analysis of Msdmrt3 in largemouth bass","volume":"28","author":"Sheng","year":"2021","journal-title":"JFSC"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/j.gene.2015.07.044","article-title":"Transcriptional variants of Dmrt1 and expression of four Dmrt genes in the blunt snout bream, Megalobrama amblycephala","volume":"573","author":"Su","year":"2015","journal-title":"Gene"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1016\/j.mod.2004.03.018","article-title":"Developmentally regulated and non-sex-specific expression of autosomal dmrt genes in embryos of the Medaka fish (Oryzias latipes)","volume":"121","author":"Winkler","year":"2004","journal-title":"Mech. Dev."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"8536","DOI":"10.1038\/sj.onc.1206907","article-title":"Gadd45a contributes to p53 stabilization in response to DNA damage","volume":"22","author":"Jin","year":"2003","journal-title":"Oncogene"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-3-030-94804-7_1","article-title":"GADD45 in Stress Signaling, Cell Cycle Control, and Apoptosis","volume":"1360","author":"Humayun","year":"2022","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s00441-019-03084-w","article-title":"Immune-associated renal disease found in caspase 3-deficient mice","volume":"379","author":"Suzuki","year":"2020","journal-title":"Cell. Tissue Res."},{"key":"ref_56","first-page":"493","article-title":"Role of sperm apoptosis and oxidative stress in male infertility: A narrative review","volume":"19","author":"Asadi","year":"2021","journal-title":"Int. J. Reprod. Biomed."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"R189","DOI":"10.1530\/REP-19-0452","article-title":"Impact of oxidative stress on male and female germ cells: Implications for fertility","volume":"159","author":"Aitken","year":"2020","journal-title":"Reproduction"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1093\/humupd\/dmaa034","article-title":"Molecular genetics of infertility: Loss-of-function mutations in humans and corresponding knockout\/mutated mice","volume":"27","author":"Jiao","year":"2021","journal-title":"Hum. Reprod. Update"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1002\/j.1939-4640.2000.tb03409.x","article-title":"Phenotypes of sperm pathology: Genetic and acquired forms in infertile men","volume":"21","author":"Chemes","year":"2000","journal-title":"J. Androl."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1080\/01485010390219656","article-title":"Asthenozoospermia: Analysis of a large population","volume":"49","author":"Curi","year":"2003","journal-title":"Arch. Androl."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1093\/humrep\/dey335","article-title":"Mitochondrial functionality modifies human sperm acrosin activity, acrosome reaction capability and chromatin integrity","volume":"34","author":"Zhang","year":"2019","journal-title":"Hum. Reprod."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"e13666","DOI":"10.1111\/and.13666","article-title":"Causes and consequences of sperm mitochondrial dysfunction","volume":"53","author":"Durairajanayagam","year":"2021","journal-title":"Andrologia"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.freeradbiomed.2019.06.018","article-title":"Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria","volume":"141","author":"Zhu","year":"2019","journal-title":"Free. Radic. Biol. Med."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.2164\/jandrol.112.016535","article-title":"Reactive oxygen species and sperm function-in sickness and in health","volume":"33","author":"Aitken","year":"2012","journal-title":"J. Androl."},{"key":"ref_65","first-page":"848","article-title":"Sperm mitochondrial DNA and male infertility: An update","volume":"23","author":"Li","year":"2017","journal-title":"Zhonghua Nan Ke Xue Natl. J. Androl."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Costa, J., Braga, P.C., Rebelo, I., Oliveira, P.F., and Alves, M.G. (2023). Mitochondria Quality Control and Male Fertility. Biology, 12.","DOI":"10.3390\/biology12060827"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.3109\/19401736.2014.947582","article-title":"Mitochondrial DNA mutations may not be frequent in asthenospermic infertile men","volume":"27","author":"Wang","year":"2016","journal-title":"Mitochondrial DNA. Part A DNA Mapp. Seq. Anal."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1016\/j.cmet.2017.07.003","article-title":"Increased Total mtDNA Copy Number Cures Male Infertility Despite Unaltered mtDNA Mutation Load","volume":"26","author":"Jiang","year":"2017","journal-title":"Cell. Metab."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1083\/jcb.201010024","article-title":"Mitochondrial DNA mutations in disease and aging","volume":"193","author":"Park","year":"2011","journal-title":"J. Cell. Biol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/14\/16\/2406\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T15:39:08Z","timestamp":1760110748000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/14\/16\/2406"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,8,19]]},"references-count":69,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2024,8]]}},"alternative-id":["ani14162406"],"URL":"https:\/\/doi.org\/10.3390\/ani14162406","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,8,19]]}}}