{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T13:28:57Z","timestamp":1790429337717,"version":"4.1.0"},"reference-count":32,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2019,1,17]],"date-time":"2019-01-17T00:00:00Z","timestamp":1547683200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100005301","name":"American College of Surgeons","doi-asserted-by":"crossref","award":["(George H.A. Clowes Memorial Research Career Development Award"],"award-info":[{"award-number":["(George H.A. Clowes Memorial Research Career Development Award"]}],"id":[{"id":"10.13039\/100005301","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Hackers for Hope"},{"name":"Matheson Fellowship"},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01HD038807"],"award-info":[{"award-number":["R01HD038807"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["P30 CA008748"],"award-info":[{"award-number":["P30 CA008748"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0209995","type":"journal-article","created":{"date-parts":[[2019,1,17]],"date-time":"2019-01-17T18:46:17Z","timestamp":1547750777000},"page":"e0209995","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":14,"title":["Mouse DCUN1D1 (SCCRO) is required for spermatogenetic individualization"],"prefix":"10.1371","volume":"14","author":[{"given":"Guochang","family":"Huang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew J.","family":"Kaufman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Russell J. H.","family":"Ryan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yevgeniy","family":"Romin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laryssa","family":"Huryn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarina","family":"Bains","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katia","family":"Manova-Todorova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia L.","family":"Morris","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7600-8947","authenticated-orcid":true,"given":"Gary R.","family":"Hunnicutt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carrie A.","family":"Adelman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John H. J.","family":"Petrini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Y.","family":"Ramanathan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1457-0066","authenticated-orcid":true,"given":"Bhuvanesh","family":"Singh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2019,1,17]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/1747-1028-3-7","article-title":"Cullin-RING ubiquitin ligases: global regulation and activation cycles","volume":"3","author":"DR Bosu","year":"2008","journal-title":"Cell Div"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1146\/annurev.biochem.78.101807.093809","article-title":"RING domain E3 ubiquitin ligases","volume":"78","author":"RJ Deshaies","year":"2009","journal-title":"Annu Rev Biochem"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1146\/annurev.arplant.58.032806.104011","article-title":"Regulation of Cullin RING Ligases","volume":"59","author":"SK Hotton","year":"2008","journal-title":"Annu Rev Plant Biol"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1146\/annurev.biophys.36.040306.132820","article-title":"Structural mechanisms underlying posttranslational modification by ubiquitin-like proteins","volume":"36","author":"BT Dye","year":"2007","journal-title":"Annu Rev Biophys Biomol Struct"},{"issue":"6","key":"ref5","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1016\/j.cell.2008.07.022","article-title":"Structural insights into NEDD8 activation of cullin-RING ligases: conformational control of conjugation","volume":"134","author":"DM Duda","year":"2008","journal-title":"Cell"},{"issue":"11","key":"ref6","doi-asserted-by":"crossref","first-page":"1985","DOI":"10.1038\/sj.onc.1207414","article-title":"Nedd8 on cullin: building an expressway to protein destruction","volume":"23","author":"ZQ Pan","year":"2004","journal-title":"Oncogene"},{"issue":"1","key":"ref7","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.molcel.2007.12.012","article-title":"Dcn1 functions as a scaffold-type E3 ligase for cullin neddylation","volume":"29","author":"T Kurz","year":"2008","journal-title":"Molecular cell"},{"issue":"7046","key":"ref8","doi-asserted-by":"crossref","first-page":"1257","DOI":"10.1038\/nature03662","article-title":"The conserved protein DCN-1\/Dcn1p is required for cullin neddylation in C. elegans and S. cerevisiae","volume":"435","author":"T Kurz","year":"2005","journal-title":"Nature"},{"issue":"5","key":"ref9","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1016\/j.molcel.2010.08.030","article-title":"A dual E3 mechanism for Rub1 ligation to Cdc53","volume":"39","author":"DC Scott","year":"2010","journal-title":"Molecular cell"},{"issue":"12","key":"ref10","doi-asserted-by":"crossref","first-page":"10297","DOI":"10.1074\/jbc.M110.203729","article-title":"SCCRO (DCUN1D1) promotes nuclear translocation and assembly of the neddylation E3 complex","volume":"286","author":"G Huang","year":"2011","journal-title":"J Biol Chem"},{"issue":"48","key":"ref11","doi-asserted-by":"crossref","first-page":"33211","DOI":"10.1074\/jbc.M804440200","article-title":"SCCRO (DCUN1D1) is an essential component of the E3 complex for neddylation","volume":"283","author":"AY Kim","year":"2008","journal-title":"J Biol Chem"},{"issue":"2","key":"ref12","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1038\/13886","article-title":"Loss of Cul1 results in early embryonic lethality and dysregulation of cyclin E","volume":"23","author":"MJ Dealy","year":"1999","journal-title":"Nat Genet"},{"issue":"14","key":"ref13","doi-asserted-by":"crossref","first-page":"4997","DOI":"10.1128\/MCB.22.14.4997-5005.2002","article-title":"CUL-4A is critical for early embryonic development","volume":"22","author":"B Li","year":"2002","journal-title":"Mol Cell Biol"},{"issue":"15","key":"ref14","doi-asserted-by":"crossref","first-page":"6203","DOI":"10.1073\/pnas.0812425106","article-title":"RBX1\/ROC1 disruption results in early embryonic lethality due to proliferation failure, partially rescued by simultaneous loss of p27","volume":"106","author":"M Tan","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"ref15","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1083\/jcb.200104035","article-title":"The NEDD8 system is essential for cell cycle progression and morphogenetic pathway in mice","volume":"155","author":"K Tateishi","year":"2001","journal-title":"J Cell Biol"},{"issue":"20","key":"ref16","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1016\/S0960-9822(00)80024-X","article-title":"Deletion of the Cul1 gene in mice causes arrest in early embryogenesis and accumulation of cyclin E","volume":"9","author":"Y Wang","year":"1999","journal-title":"Curr Biol"},{"issue":"12","key":"ref17","doi-asserted-by":"crossref","first-page":"6200","DOI":"10.1074\/jbc.M115.692756","article-title":"Squamous Cell Carcinoma-related Oncogene (SCCRO) Family Members Regulate Cell Growth and Proliferation through Their Cooperative and Antagonistic Effects on Cullin Neddylation","volume":"291","author":"W Fu","year":"2016","journal-title":"J Biol Chem"},{"issue":"1","key":"ref18","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1093\/nar\/gkg064","article-title":"BayGenomics: a resource of insertional mutations in mouse embryonic stem cells","volume":"31","author":"D Stryke","year":"2003","journal-title":"Nucleic Acids Res"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1186\/1751-0147-55-83","article-title":"Pup mortality in laboratory mice\u2014infanticide or not?","volume":"55","author":"EM Weber","year":"2013","journal-title":"Acta Vet Scand"},{"issue":"6","key":"ref20","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1038\/ng1367","article-title":"Essential role of Plzf in maintenance of spermatogonial stem cells","volume":"36","author":"JA Costoya","year":"2004","journal-title":"Nat Genet"},{"issue":"4","key":"ref21","doi-asserted-by":"crossref","first-page":"1883","DOI":"10.1210\/endo.139.4.5871","article-title":"Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells","volume":"139","author":"S Jenab","year":"1998","journal-title":"Endocrinology"},{"issue":"3","key":"ref22","doi-asserted-by":"crossref","first-page":"e1000042","DOI":"10.1371\/journal.pgen.1000042","article-title":"ZIP4H (TEX11) deficiency in the mouse impairs meiotic double strand break repair and the regulation of crossing over","volume":"4","author":"CA Adelman","year":"2008","journal-title":"PLoS genetics"},{"issue":"47","key":"ref23","doi-asserted-by":"crossref","first-page":"16501","DOI":"10.1073\/pnas.0407708101","article-title":"Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility","volume":"101","author":"K Miki","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"ref24","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1095\/biolreprod.109.079566","article-title":"The annulus of the mouse sperm tail is required to establish a membrane diffusion barrier that is engaged during the late steps of spermiogenesis","volume":"82","author":"S Kwitny","year":"2010","journal-title":"Biol Reprod"},{"key":"ref25","first-page":"286","article-title":"Histological and histopathological evaluation of the testis","volume":"xiv","author":"LD Russell","year":"1990"},{"issue":"37","key":"ref26","doi-asserted-by":"crossref","first-page":"15254","DOI":"10.1074\/jbc.M117.778530","article-title":"Squamous cell carcinoma-related oncogene (SCCRO) neddylates Cul3 protein to selectively promote midbody localization and activity of Cul3(KLHL21) protein complex during abscission","volume":"292","author":"G Huang","year":"2017","journal-title":"J Biol Chem"},{"issue":"2","key":"ref27","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.ydbio.2007.02.025","article-title":"Conversion of midbodies into germ cell intercellular bridges","volume":"305","author":"MP Greenbaum","year":"2007","journal-title":"Developmental biology"},{"issue":"8","key":"ref28","doi-asserted-by":"crossref","first-page":"a005850","DOI":"10.1101\/cshperspect.a005850","article-title":"Germ cell intercellular bridges","volume":"3","author":"MP Greenbaum","year":"2011","journal-title":"Cold Spring Harbor perspectives in biology"},{"issue":"10","key":"ref29","doi-asserted-by":"crossref","first-page":"e251","DOI":"10.1371\/journal.pbio.0050251","article-title":"A ubiquitin ligase complex regulates caspase activation during sperm differentiation in Drosophila","volume":"5","author":"E Arama","year":"2007","journal-title":"PLoS biology"},{"issue":"17","key":"ref30","doi-asserted-by":"crossref","first-page":"3855","DOI":"10.1242\/dev.127.17.3855","article-title":"A phospholipid kinase regulates actin organization and intercellular bridge formation during germline cytokinesis","volume":"127","author":"JA Brill","year":"2000","journal-title":"Development"},{"issue":"13","key":"ref31","doi-asserted-by":"crossref","first-page":"4982","DOI":"10.1073\/pnas.0505123103","article-title":"TEX14 is essential for intercellular bridges and fertility in male mice","volume":"103","author":"MP Greenbaum","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"3","key":"ref32","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1095\/biolreprod.108.070649","article-title":"Mouse TEX14 is required for embryonic germ cell intercellular bridges but not female fertility","volume":"80","author":"MP Greenbaum","year":"2009","journal-title":"Biol Reprod"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0209995","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,10]],"date-time":"2022-09-10T15:21:56Z","timestamp":1662823316000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0209995"}},"subtitle":[],"editor":[{"given":"Stefan","family":"Schlatt","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2019,1,17]]},"references-count":32,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,1,17]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0209995","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,1,17]]}}}