{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T23:14:49Z","timestamp":1787008489855,"version":"build-2736575974"},"reference-count":39,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2024,1,17]],"date-time":"2024-01-17T00:00:00Z","timestamp":1705449600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82371614"],"award-info":[{"award-number":["82371614"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82071696"],"award-info":[{"award-number":["82071696"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82301799"],"award-info":[{"award-number":["82301799"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Postgraduate Research & Practice Innovation Program of Jiangsu Province","award":["KYCX23_3618"],"award-info":[{"award-number":["KYCX23_3618"]}]},{"name":"Postgraduate Research & Practice Innovation Program of Jiangsu Province","award":["KYCX22_3561"],"award-info":[{"award-number":["KYCX22_3561"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,5,9]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The centrosome is critical for maintaining the sperm head\u2013tail connection and the formation of flagellar microtubules. In this study, we found that in mouse testes, CCDC159 (coiled-coil domain-containing protein 159) is specifically localized to the head\u2013tail coupling apparatus (HTCA) of spermatids, a structure that ensures sperm head\u2013tail tight conjunction. CCDC159 contains a C-terminal coiled-coil domain that functions as the centrosomal localization signal. Gene knockout (KO) of Ccdc159 in mice resulted in acephalic spermatozoa, abnormal flagella, and male infertility. To explore the mechanism behind CCDC159 regulating spermatogenesis, we identified CCDC159-binding proteins using a yeast two-hybrid screen and speculated that CCDC159 participates in HTCA assembly by regulating protein phosphatase PP1 activity. Further RNA-sequencing analyses of Ccdc159 KO testes revealed numerous genes involved in male gamete generation that were downregulated. Together, our results show that CCDC159 in spermatids is a novel centrosomal protein anchoring the sperm head to the tail. Considering the limitation of KO mouse model in clarifying the biological function of CCDC159 in spermatogenesis, a gene-rescue experiment will be performed in the future.<\/jats:p>","DOI":"10.1093\/biolre\/ioae012","type":"journal-article","created":{"date-parts":[[2024,1,15]],"date-time":"2024-01-15T16:33:24Z","timestamp":1705336404000},"page":"877-894","source":"Crossref","is-referenced-by-count":15,"title":["Coiled-coil domain containing 159 is required for spermatid head and tail assembly in mice"],"prefix":"10.1093","volume":"110","author":[{"given":"Tingting","family":"Ge","sequence":"first","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lu","family":"Yuan","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linwei","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fan","family":"Yang","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Department of Obstetrics and Gynecology, Affiliated Hospital, Yangzhou University , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenhua","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Changmin","family":"Niu","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guanghua","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Huiping","family":"Zhou","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Zheng","sequence":"additional","affiliation":[{"name":"Department of Histology and Embryology , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Yangzhou University , School of Medicine, , Yangzhou, Jiangsu , China"},{"name":"Department of Obstetrics and Gynecology, Affiliated Hospital, Yangzhou University , Yangzhou, Jiangsu , China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,1,17]]},"reference":[{"key":"2024051505405983000_ref1","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1016\/S2213-8587(16)30040-7","article-title":"Novel concepts in the aetiology of male reproductive impairment","volume":"5","author":"Tournaye","year":"2017","journal-title":"Lancet Diabetes Endocrinol"},{"key":"2024051505405983000_ref2","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":"2024051505405983000_ref3","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1007\/s00439-020-02202-x","article-title":"Disease gene discovery in male infertility: past, present and future","volume":"140","author":"Xavier","year":"2021","journal-title":"Hum Genet"},{"key":"2024051505405983000_ref4","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1016\/S0015-0282(16)50011-9","article-title":"Lack of a head in human spermatozoa from sterile patients: a syndrome associated with impaired fertilization","volume":"47","author":"Chemes","year":"1987","journal-title":"Fertil Steril"},{"key":"2024051505405983000_ref5","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1530\/jrf.0.0630543","article-title":"Ultrastructural study of the decapitated sperm defect in an infertile man","volume":"63","author":"Perotti","year":"1981","journal-title":"J Reprod Fertil"},{"key":"2024051505405983000_ref6","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1210\/rp.57.1.103","article-title":"Male germ cell gene expression","volume":"57","author":"Eddy","year":"2002","journal-title":"Recent Prog Horm Res"},{"key":"2024051505405983000_ref7","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1002\/ar.1091650204","article-title":"The fine structure and development of the neck region of the mammalian spermatozoon","volume":"165","author":"Fawcett","year":"1969","journal-title":"Anat Rec"},{"key":"2024051505405983000_ref8","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1093\/biolre\/iox096","article-title":"Formation and function of sperm tail structures in association with sperm motility defects","volume":"97","author":"Lehti","year":"2017","journal-title":"Biol Reprod"},{"key":"2024051505405983000_ref9","doi-asserted-by":"crossref","first-page":"231","DOI":"10.4103\/aja202198","article-title":"Genetic pathogenesis of acephalic spermatozoa syndrome: past, present, and future","volume":"24","author":"Wang","year":"2022","journal-title":"Asian J Androl"},{"key":"2024051505405983000_ref10","doi-asserted-by":"crossref","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":"2015","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2024051505405983000_ref11","doi-asserted-by":"crossref","first-page":"4926","DOI":"10.1038\/s41467-021-25227-w","article-title":"The missing linker between SUN5 and PMFBP1 in sperm head-tail coupling apparatus","volume":"12","author":"Zhang","year":"2021","journal-title":"Nat Commun"},{"key":"2024051505405983000_ref12","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.ajhg.2018.06.010","article-title":"Mutations in PMFBP1 cause acephalic spermatozoa syndrome","volume":"103","author":"Zhu","year":"2018","journal-title":"Am J Hum Genet"},{"key":"2024051505405983000_ref13","doi-asserted-by":"crossref","first-page":"e28199","DOI":"10.7554\/eLife.28199","article-title":"Essential role for SUN5 in anchoring sperm head to the tail","volume":"6","author":"Shang","year":"2017","journal-title":"Elife"},{"key":"2024051505405983000_ref14","doi-asserted-by":"crossref","first-page":"1673","DOI":"10.1093\/biolre\/ioz083","article-title":"Non-canonical RNA polyadenylation polymerase FAM46C is essential for fastening sperm head and flagellum in mice","volume":"100","author":"Zheng","year":"2019","journal-title":"Biol Reprod"},{"key":"2024051505405983000_ref15","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1111\/cge.13662","article-title":"Loss-of-function mutations in centrosomal protein 112 is associated with human acephalic spermatozoa phenotype","volume":"97","author":"Sha","year":"2020","journal-title":"Clin Genet"},{"key":"2024051505405983000_ref16","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1038\/s41467-022-29109-7","article-title":"CEP128 is involved in spermatogenesis in humans and mice","volume":"13","author":"Zhang","year":"2022","journal-title":"Nat Commun"},{"key":"2024051505405983000_ref17","doi-asserted-by":"crossref","first-page":"2725","DOI":"10.1007\/s43032-021-00595-2","article-title":"Coiled-coil domain-containing (CCDC) proteins: functional roles in general and male reproductive physiology","volume":"28","author":"Priyanka","year":"2021","journal-title":"Reprod Sci"},{"key":"2024051505405983000_ref18","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1002\/bies.201600062","article-title":"Coiled-coils: the long and short of it","volume":"38","author":"Truebestein","year":"2016","journal-title":"Bioessays"},{"key":"2024051505405983000_ref19","doi-asserted-by":"crossref","first-page":"dev200516","DOI":"10.1242\/dev.200516","article-title":"CCDC38 is required for sperm flagellum biogenesis and male fertility in mice","volume":"149","author":"Zhang","year":"2022","journal-title":"Development"},{"key":"2024051505405983000_ref20","doi-asserted-by":"crossref","first-page":"151","DOI":"10.3389\/fcell.2019.00151","article-title":"CCDC42 localizes to manchette, HTCA and tail and interacts with ODF1 and ODF2 in the formation of the male germ cell cytoskeleton","volume":"7","author":"Tapia Contreras","year":"2019","journal-title":"Front Cell Dev Biol"},{"key":"2024051505405983000_ref21","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1177\/1933719116641762","article-title":"A novel testis-specific gene, Ccdc136, is required for acrosome formation and fertilization in mice","volume":"23","author":"Geng","year":"2016","journal-title":"Reprod Sci"},{"key":"2024051505405983000_ref22","doi-asserted-by":"crossref","first-page":"1795","DOI":"10.1007\/s00439-022-02459-4","article-title":"Homozygous missense mutation in CCDC155 disrupts the transmembrane distribution of CCDC155 and SUN1, resulting in non-obstructive azoospermia and premature ovarian insufficiency in humans","volume":"141","author":"Wu","year":"2022","journal-title":"Hum Genet"},{"key":"2024051505405983000_ref23","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1091\/mbc.E19-07-0402","article-title":"Unraveling the mysteries of centriolar satellites: time to rewrite the textbooks about the centrosome\/cilium complex","volume":"31","author":"Odabasi","year":"2020","journal-title":"Mol Biol Cell"},{"key":"2024051505405983000_ref24","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1530\/REP-09-0243","article-title":"Disruption of the murine dynein light chain gene Tcte3-3 results in asthenozoospermia","volume":"139","author":"Rashid","year":"2010","journal-title":"Reproduction"},{"key":"2024051505405983000_ref25","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/gtc.12105","article-title":"Oligo-astheno-teratozoospermia in mice lacking ORP4, a sterol-binding protein in the OSBP-related protein family","volume":"19","author":"Udagawa","year":"2014","journal-title":"Genes Cells"},{"key":"2024051505405983000_ref26","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1016\/j.bbrc.2020.02.118","article-title":"GGNBP1 ensures proper spermiogenesis in response to stress in mice","volume":"525","author":"Han","year":"2020","journal-title":"Biochem Biophys Res Commun"},{"key":"2024051505405983000_ref27","doi-asserted-by":"crossref","first-page":"3724","DOI":"10.1091\/mbc.e08-04-0362","article-title":"Three members of the LC8\/DYNLL family are required for outer arm dynein motor function","volume":"19","author":"Tanner","year":"2008","journal-title":"Mol Biol Cell"},{"key":"2024051505405983000_ref28","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1038\/s41586-021-03662-5","article-title":"Phase separation drives aberrant chromatin looping and cancer development","volume":"595","author":"Ahn","year":"2021","journal-title":"Nature"},{"key":"2024051505405983000_ref29","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1016\/S0070-2153(99)49017-9","article-title":"Centrosome reduction during mammalian spermiogenesis","volume":"49","author":"Manandhar","year":"2000","journal-title":"Curr Top Dev Biol"},{"key":"2024051505405983000_ref30","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1006\/dbio.1998.8947","article-title":"Centrosome reduction during mouse spermiogenesis","volume":"203","author":"Manandhar","year":"1998","journal-title":"Dev Biol"},{"key":"2024051505405983000_ref31","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1002\/(SICI)1097-0169(1999)43:2<137::AID-CM5>3.0.CO;2-7","article-title":"Centriole and centrin degeneration during mouse spermiogenesis","volume":"43","author":"Manandhar","year":"1999","journal-title":"Cell Motil Cytoskeleton"},{"key":"2024051505405983000_ref32","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1186\/1477-7827-10-51","article-title":"Developmental expression and function of DKKL1\/Dkkl1 in humans and mice","volume":"10","author":"Yan","year":"2012","journal-title":"Reprod Biol Endocrinol"},{"key":"2024051505405983000_ref33","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1038\/s41420-021-00581-2","article-title":"Polyubiquitin gene Ubb is required for upregulation of Piwi protein level during mouse testis development","volume":"7","author":"Han","year":"2021","journal-title":"Cell Death Discov"},{"key":"2024051505405983000_ref34","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1016\/j.febslet.2004.10.112","article-title":"Yeast two-hybrid screens imply that GGNBP1, GGNBP2 and OAZ3 are potential interaction partners of testicular germ cell-specific protein GGN1","volume":"579","author":"Zhang","year":"2005","journal-title":"FEBS Lett"},{"key":"2024051505405983000_ref35","doi-asserted-by":"crossref","first-page":"2508","DOI":"10.1016\/j.ajpath.2017.07.016","article-title":"Ggnbp2-null mutation in mice leads to male infertility due to a defect at the spermiogenesis stage","volume":"187","author":"Liu","year":"2017","journal-title":"Am J Pathol"},{"key":"2024051505405983000_ref36","doi-asserted-by":"crossref","first-page":"2998","DOI":"10.1038\/s41598-017-03193-y","article-title":"GGNBP2 is necessary for testis morphology and sperm development","volume":"7","author":"Chen","year":"2017","journal-title":"Sci Rep"},{"key":"2024051505405983000_ref37","doi-asserted-by":"crossref","first-page":"e1000712","DOI":"10.1371\/journal.pgen.1000712","article-title":"OAZ-t\/OAZ3 is essential for rigid connection of sperm tails to heads in mouse","volume":"5","author":"Tokuhiro","year":"2009","journal-title":"PLoS Genet"},{"key":"2024051505405983000_ref38","doi-asserted-by":"crossref","first-page":"29417","DOI":"10.1074\/jbc.M111.274647","article-title":"Ornithine decarboxylase antizyme Oaz3 modulates protein phosphatase activity","volume":"286","author":"Ruan","year":"2011","journal-title":"J Biol Chem"},{"key":"2024051505405983000_ref39","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1002\/mrd.20313","article-title":"Germ-cell specific protein gametogenetin protein 2 (GGN2), expression in the testis, and association with intracellular membrane","volume":"72","author":"Zhao","year":"2005","journal-title":"Mol Reprod Dev"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioae012\/56612547\/ioae012.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/110\/5\/877\/57468452\/ioae012.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/110\/5\/877\/57468452\/ioae012.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,15]],"date-time":"2024-05-15T03:30:25Z","timestamp":1715743825000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/110\/5\/877\/7571407"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,17]]},"references-count":39,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2024,1,17]]},"published-print":{"date-parts":[[2024,5,9]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioae012","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,4]]},"published":{"date-parts":[[2024,1,17]]}}}