{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T17:44:54Z","timestamp":1791999894018,"version":"4.4.0"},"reference-count":49,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,6,25]],"date-time":"2021-06-25T00:00:00Z","timestamp":1624579200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31625015, 31521003, 81971441 and 81901541"],"award-info":[{"award-number":["31625015, 31521003, 81971441 and 81901541"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Male infertility is a multifactorial disease with a strong genetic background. Abnormal sperm morphologies have been found to be closely related to male infertility. Here, we conducted whole-exome sequencing in a cohort of 150 Han Chinese men with asthenoteratozoospermia. Two novel hemizygous mutations were identified in USP26, an X-linked gene preferentially expressed in the testis and encoding a deubiquitinating enzyme. These USP26 variants are extremely rare in human population genome databases and have been predicted to be deleterious by multiple bioinformatics tools. Hematoxylin-eosin staining and electron microscopy analyses of the spermatozoa from men harboring hemizygous USP26 variants showed a highly aberrant morphology and ultrastructure of the sperm heads and flagella. Real-time quantitative PCR and immunoblotting assays revealed obviously reduced levels of USP26 mRNA and protein in the spermatozoa from men harboring hemizygous deleterious variants of USP26. Furthermore, intracytoplasmic sperm injections performed on infertile men harboring hemizygous USP26 variants achieved satisfactory outcomes. Overall, our study demonstrates that USP26 is essential for normal sperm morphogenesis, and hemizygous USP26 mutations can induce X-linked asthenoteratozoospermia. These findings will provide effective guidance for the genetic and reproductive counseling of infertile men with asthenoteratozoospermia.<\/jats:p>","DOI":"10.3390\/cells10071594","type":"journal-article","created":{"date-parts":[[2021,6,25]],"date-time":"2021-06-25T11:07:40Z","timestamp":1624619260000},"page":"1594","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Novel Mutations in X-Linked, USP26-Induced Asthenoteratozoospermia and Male Infertility"],"prefix":"10.3390","volume":"10","author":[{"given":"Chunyu","family":"Liu","sequence":"first","affiliation":[{"name":"Obstetrics and Gynecology Hospital, NHC Key Laboratory of Reproduction Regulation (Shanghai Institute for Biomedical and Pharmaceutical Technologies), Fudan University, Shanghai 200011, China"},{"name":"Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Shen","sequence":"additional","affiliation":[{"name":"Department of Obstetrics\/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu 610041, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qunshan","family":"Shen","sequence":"additional","affiliation":[{"name":"Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei 230022, China"},{"name":"NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, Hefei 230032, China"},{"name":"Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People\u2019s Republic of China, Hefei 230032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen","family":"Zhang","sequence":"additional","affiliation":[{"name":"Fudan University Pudong Medical Center, Shanghai Key Laboratory of Medical Epigenetics, Institutes of Biomedical Sciences, Department of Systems Biology for Medicine, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2819-165X","authenticated-orcid":false,"given":"Jiaxiong","family":"Wang","sequence":"additional","affiliation":[{"name":"Center for Reproduction and Genetics, The Affiliated Suzhou Hospital of Nanjing Medical University, Suzhou Municipal Hospital, Suzhou 215002, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2701-1976","authenticated-orcid":false,"given":"Shuyan","family":"Tang","sequence":"additional","affiliation":[{"name":"Obstetrics and Gynecology Hospital, NHC Key Laboratory of Reproduction Regulation (Shanghai Institute for Biomedical and Pharmaceutical Technologies), Fudan University, Shanghai 200011, China"},{"name":"Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0009-3839","authenticated-orcid":false,"given":"Huan","family":"Wu","sequence":"additional","affiliation":[{"name":"Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei 230022, China"},{"name":"NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, Hefei 230032, China"},{"name":"Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People\u2019s Republic of China, Hefei 230032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shixiong","family":"Tian","sequence":"additional","affiliation":[{"name":"Obstetrics and Gynecology Hospital, NHC Key Laboratory of Reproduction Regulation (Shanghai Institute for Biomedical and Pharmaceutical Technologies), Fudan University, Shanghai 200011, China"},{"name":"Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiangshan","family":"Cong","sequence":"additional","affiliation":[{"name":"Obstetrics and Gynecology Hospital, NHC Key Laboratory of Reproduction Regulation (Shanghai Institute for Biomedical and Pharmaceutical Technologies), Fudan University, Shanghai 200011, China"},{"name":"Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaojin","family":"He","sequence":"additional","affiliation":[{"name":"Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei 230022, China"},{"name":"NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, Hefei 230032, China"},{"name":"Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People\u2019s Republic of China, Hefei 230032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li","family":"Jin","sequence":"additional","affiliation":[{"name":"Obstetrics and Gynecology Hospital, NHC Key Laboratory of Reproduction Regulation (Shanghai Institute for Biomedical and Pharmaceutical Technologies), Fudan University, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4556-8276","authenticated-orcid":false,"given":"Feng","family":"Zhang","sequence":"additional","affiliation":[{"name":"Obstetrics and Gynecology Hospital, NHC Key Laboratory of Reproduction Regulation (Shanghai Institute for Biomedical and Pharmaceutical Technologies), Fudan University, Shanghai 200011, China"},{"name":"Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai 200011, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaohui","family":"Jiang","sequence":"additional","affiliation":[{"name":"Department of Obstetrics\/Gynecology, Key Laboratory of Obstetric, Gynecologic and Pediatric Diseases and Birth Defects of Ministry of Education, West China Second University Hospital, Sichuan University, Chengdu 610041, China"},{"name":"Reproductive Andrology\/Human Sperm Bank, West China Second University Hospital, Sichuan University, Chengdu 610041, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunxia","family":"Cao","sequence":"additional","affiliation":[{"name":"Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, Hefei 230022, China"},{"name":"NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, Hefei 230032, China"},{"name":"Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People\u2019s Republic of China, Hefei 230032, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,25]]},"reference":[{"key":"ref_1","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_2","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1038\/ng2027","article-title":"Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility","volume":"39","author":"Dieterich","year":"2007","journal-title":"Nat. Genet."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1086\/521314","article-title":"Homozygous mutation in SPATA16 is associated with male infertility in human globozoospermia","volume":"81","author":"Dam","year":"2007","journal-title":"Am. J. Hum. Genet."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.ajhg.2011.01.018","article-title":"DPY19L2 deletion as a major cause of globozoospermia","volume":"88","author":"Koscinski","year":"2011","journal-title":"Am. J. Hum. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.ajhg.2013.11.017","article-title":"Mutations in DNAH1, which encodes an inner arm heavy chain dynein, lead to male infertility from multiple morphological abnormalities of the sperm flagella","volume":"94","author":"Coutton","year":"2014","journal-title":"Am. J. Hum. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1016\/j.ajhg.2020.06.004","article-title":"Bi-allelic DNAH8 Variants Lead to Multiple Morphological Abnormalities of the Sperm Flagella and Primary Male Infertility","volume":"107","author":"Liu","year":"2020","journal-title":"Am. J. Hum. Genet."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1016\/j.ajhg.2020.07.010","article-title":"Bi-allelic Loss-of-function Variants in CFAP58 Cause Flagellar Axoneme and Mitochondrial Sheath Defects and Asthenoteratozoospermia in Humans and Mice","volume":"107","author":"He","year":"2020","journal-title":"Am. J. Hum. Genet."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1136\/jmedgenet-2019-106775","article-title":"Biallelic variants in MAATS1 encoding CFAP91, a calmodulin-associated and spoke-associated complex protein, cause severe astheno-teratozoospermia and male infertility","volume":"57","author":"Martinez","year":"2020","journal-title":"J. Med. Genet."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/s00439-020-02113-x","article-title":"The genetic architecture of morphological abnormalities of the sperm tail","volume":"140","author":"Toure","year":"2020","journal-title":"Hum. Genet."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.ajhg.2021.01.002","article-title":"Deleterious variants in X-linked CFAP47 induce asthenoteratozoospermia and primary male infertility","volume":"108","author":"Liu","year":"2021","journal-title":"Am. J. Hum. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1016\/j.tibs.2017.09.002","article-title":"The Ubiquitin Code in the Ubiquitin-Proteasome System and Autophagy","volume":"42","author":"Kwon","year":"2017","journal-title":"Trends Biochem. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1016\/j.cell.2005.11.007","article-title":"A genomic and functional inventory of deubiquitinating enzymes","volume":"123","author":"Nijman","year":"2005","journal-title":"Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1186\/s13578-016-0127-1","article-title":"The emerging role of deubiquitinating enzymes in genomic integrity, diseases, and therapeutics","volume":"6","author":"He","year":"2016","journal-title":"Cell Biosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1016\/j.semcdb.2014.03.001","article-title":"The role of E3 ligases in the ubiquitin-dependent regulation of spermatogenesis","volume":"30","author":"Richburg","year":"2014","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"4711","DOI":"10.1007\/s00018-015-2030-z","article-title":"The role of deubiquitinating enzymes in spermatogenesis","volume":"72","author":"Suresh","year":"2015","journal-title":"Cell Mol. Life Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1038\/sj.ejhg.5201335","article-title":"Possible role of USP26 in patients with severely impaired spermatogenesis","volume":"13","author":"Stouffs","year":"2005","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1111\/j.1365-2605.2006.00708.x","article-title":"Alterations of the USP26 gene in Caucasian men","volume":"29","author":"Stouffs","year":"2006","journal-title":"Int. J. Androl."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1111\/j.1745-7262.2007.00305.x","article-title":"Novel mutations in ubiquitin-specific protease 26 gene might cause spermatogenesis impairment and male infertility","volume":"9","author":"Zhang","year":"2007","journal-title":"Asian J. Androl."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1080\/19396368.2016.1238116","article-title":"Single nucleotide polymorphisms of USP26 in azoospermic men","volume":"62","author":"Luddi","year":"2016","journal-title":"Syst. Biol. Reprod. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1016\/j.ccm.2016.04.008","article-title":"Primary Ciliary Dyskinesia","volume":"37","author":"Knowles","year":"2016","journal-title":"Clin. Chest Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1177\/0022034520970459","article-title":"Lrp6 Dynamic Expression in Tooth Development and Mutations in Oligodontia","volume":"100","author":"Yu","year":"2021","journal-title":"J. Dent. Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1093\/bioinformatics\/btp698","article-title":"Fast and accurate long-read alignment with Burrows-Wheeler transform","volume":"26","author":"Li","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e164","DOI":"10.1093\/nar\/gkq603","article-title":"ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data","volume":"38","author":"Wang","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1093\/humrep\/dew083","article-title":"Patients with multiple morphological abnormalities of the sperm flagella due to DNAH1 mutations have a good prognosis following intracytoplasmic sperm injection","volume":"31","author":"Wambergue","year":"2016","journal-title":"Hum. Reprod."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/S0303-7207(99)00060-X","article-title":"The ubiquitin system in gametogenesis","volume":"151","author":"Baarends","year":"1999","journal-title":"Mol. Cell Endocrinol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1007\/BF03343782","article-title":"Specific aspects of the ubiquitin system in spermatogenesis","volume":"23","author":"Baarends","year":"2000","journal-title":"J. Endocrinol. Invest."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1093\/humupd\/7.1.102","article-title":"The possible biological and reproductive functions of ubiquitin","volume":"7","author":"Bebington","year":"2001","journal-title":"Hum. Reprod. Update"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1002\/mrd.20364","article-title":"Overexpression of ubiquitin carboxyl-terminal hydrolase L1 arrests spermatogenesis in transgenic mice","volume":"73","author":"Wang","year":"2006","journal-title":"Mol. Reprod. Dev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"705","DOI":"10.1016\/j.devcel.2007.09.007","article-title":"Regulation of early wave of germ cell apoptosis and spermatogenesis by deubiquitinating enzyme CYLD","volume":"13","author":"Wright","year":"2007","journal-title":"Dev. Cell"},{"key":"ref_30","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":"ref_31","doi-asserted-by":"crossref","first-page":"e368","DOI":"10.1111\/j.1365-2605.2010.01130.x","article-title":"Localization of ubiquitin specific protease 26 at blood-testis barrier and near Sertoli cell-germ cell interface in mouse testes","volume":"34","author":"Lin","year":"2011","journal-title":"Int. J. Androl."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2911","DOI":"10.1093\/hmg\/ddi322","article-title":"Differential expression of sex-linked and autosomal germ-cell-specific genes during spermatogenesis in the mouse","volume":"14","author":"Wang","year":"2005","journal-title":"Hum. Mol. Genet."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1007\/s10815-013-0027-9","article-title":"Ubiquitin-specific protease (USP26) gene alterations associated with male infertility and recurrent pregnancy loss (RPL) in Iranian infertile patients","volume":"30","author":"Asadpor","year":"2013","journal-title":"J. Assist Reprod. Genet."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1111\/j.1745-7262.2008.00439.x","article-title":"Association of USP26 haplotypes in men in Taiwan, China with severe spermatogenic defect","volume":"10","author":"Lee","year":"2008","journal-title":"Asian. J. Androl."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"8785","DOI":"10.1038\/srep08785","article-title":"Excess of rare variants in genes that are key epigenetic regulators of spermatogenesis in the patients with non-obstructive azoospermia","volume":"5","author":"Li","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1177\/1933719116641758","article-title":"A Novel Missense Mutation in USP26 Gene Is Associated With Nonobstructive Azoospermia","volume":"23","author":"Ma","year":"2016","journal-title":"Reprod. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/S1472-6483(10)61119-4","article-title":"Novel mutations in testis-specific ubiquitin protease 26 gene may cause male infertility and hypogonadism","volume":"10","author":"Paduch","year":"2005","journal-title":"Reprod. Biomed. Online"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"720","DOI":"10.4103\/1008-682X.129134","article-title":"Association of 370-371insACA, 494T>C, and 1423C>T haplotype in ubiquitin-specific protease 26 gene and male infertility: A meta-analysis","volume":"16","author":"Xia","year":"2014","journal-title":"Asian J. Androl."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1158\/1541-7786.MCR-09-0424","article-title":"The deubiquitinating enzyme USP26 is a regulator of androgen receptor signaling","volume":"8","author":"Dirac","year":"2010","journal-title":"Mol. Cancer Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"797","DOI":"10.15252\/embr.201643270","article-title":"USP26 regulates TGF-beta signaling by deubiquitinating and stabilizing SMAD7","volume":"18","author":"Iyengar","year":"2017","journal-title":"EMBO. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.bbrc.2016.10.135","article-title":"The testis-specific USP26 is a deubiquitinating enzyme of the ubiquitin ligase Mdm2","volume":"482","author":"Golan","year":"2017","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1038\/s41467-017-00301-4","article-title":"USP26 functions as a negative regulator of cellular reprogramming by stabilising PRC1 complex components","volume":"8","author":"Ning","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"6919","DOI":"10.1093\/nar\/gkv613","article-title":"The de-ubiquitylating enzymes USP26 and USP37 regulate homologous recombination by counteracting RAP80","volume":"43","author":"Typas","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"13757","DOI":"10.1038\/s41598-019-50318-6","article-title":"Usp26 mutation in mice leads to defective spermatogenesis depending on genetic background","volume":"9","author":"Sakai","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1016\/S1472-6483(10)60531-7","article-title":"Gene polymorphisms and male infertility\u2014A meta-analysis and literature review","volume":"15","author":"Tuttelmann","year":"2007","journal-title":"Reprod. Biomed. Online"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1111\/andr.295","article-title":"Evidence from enzymatic and meta-analyses does not support a direct association between USP26 gene variants and male infertility","volume":"3","author":"Zhang","year":"2015","journal-title":"Andrology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1016\/j.ajhg.2019.10.010","article-title":"Bi-allelic Mutations in TTC29 Cause Male Subfertility with Asthenoteratospermia in Humans and Mice","volume":"105","author":"Liu","year":"2019","journal-title":"Am. J. Hum. Genet."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.gene.2017.08.033","article-title":"A homozygous CEP135 mutation is associated with multiple morphological abnormalities of the sperm flagella (MMAF)","volume":"633","author":"Sha","year":"2017","journal-title":"Gene"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.ajhg.2019.04.015","article-title":"Mutations in DNAH17, Encoding a Sperm-Specific Axonemal Outer Dynein Arm Heavy Chain, Cause Isolated Male Infertility Due to Asthenozoospermia","volume":"105","author":"Whitfield","year":"2019","journal-title":"Am. J. Hum. Genet."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/10\/7\/1594\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:23:57Z","timestamp":1760163837000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/10\/7\/1594"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,25]]},"references-count":49,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["cells10071594"],"URL":"https:\/\/doi.org\/10.3390\/cells10071594","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,25]]}}}