{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,6]],"date-time":"2026-05-06T00:53:11Z","timestamp":1778028791775,"version":"3.51.4"},"reference-count":83,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2023,7,3]],"date-time":"2023-07-03T00:00:00Z","timestamp":1688342400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/100011132","name":"Rutgers University","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100011132","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["HD088571"],"award-info":[{"award-number":["HD088571"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["HD038082"],"award-info":[{"award-number":["HD038082"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["R03 HD108418"],"award-info":[{"award-number":["R03 HD108418"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["K99\/R00 HD083521"],"award-info":[{"award-number":["K99\/R00 HD083521"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["F32 HD072628"],"award-info":[{"award-number":["F32 HD072628"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,9,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>ADAD1 is a testis-specific RNA-binding protein expressed in post-meiotic spermatids whose loss leads to defective sperm and male infertility. However, the drivers of the Adad1 phenotype remain unclear. Morphological and functional analysis of Adad1 mutant sperm showed defective DNA compaction, abnormal head shaping, and reduced motility. Mutant testes demonstrated minimal transcriptome changes; however, ribosome association of many transcripts was reduced, suggesting ADAD1 may be required for their translational activation. Further, immunofluorescence of proteins encoded by select transcripts showed delayed protein accumulation. Additional analyses demonstrated impaired subcellular localization of multiple proteins, suggesting protein transport is also abnormal in Adad1 mutants. To clarify the mechanism giving rise to this, the manchette, a protein transport microtubule network, and the LINC (linker of nucleoskeleton and cytoskeleton) complex, which connects the manchette to the nuclear lamin, were assessed across spermatid development. Proteins of both displayed delayed translation and\/or localization in mutant spermatids implicating ADAD1 in their regulation, even in the absence of altered ribosome association. Finally, ADAD1\u2019s impact on the NPC (nuclear pore complex), a regulator of both the manchette and the LINC complex, was examined. Reduced ribosome association of NPC encoding transcripts and reduced NPC protein abundance along with abnormal localization in Adad1 mutants confirmed ADAD1's impact on translation is required for a NPC in post-meiotic germ cells. Together, these studies lead to a model whereby ADAD1\u2019s influence on nuclear transport leads to deregulation of the LINC complex and the manchette, ultimately generating the range of physiological defects observed in the Adad1 phenotype.<\/jats:p>","DOI":"10.1093\/biolre\/ioad069","type":"journal-article","created":{"date-parts":[[2023,6,30]],"date-time":"2023-06-30T01:33:36Z","timestamp":1688088816000},"page":"340-355","source":"Crossref","is-referenced-by-count":6,"title":["ADAD1 is required for normal translation of nuclear pore and transport protein transcripts in spermatids of<i>Mus musculus<\/i>"],"prefix":"10.1093","volume":"109","author":[{"given":"Sarah","family":"Potgieter","sequence":"first","affiliation":[{"name":"The State University of New Jersey Department of Animal Sciences, Rutgers, , New Brunswick, NJ , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christopher","family":"Eddy","sequence":"additional","affiliation":[{"name":"The State University of New Jersey Department of Animal Sciences, Rutgers, , New Brunswick, NJ , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aditi","family":"Badrinath","sequence":"additional","affiliation":[{"name":"The State University of New Jersey Department of Animal Sciences, Rutgers, , New Brunswick, NJ , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lauren","family":"Chukrallah","sequence":"additional","affiliation":[{"name":"The State University of New Jersey Department of Animal Sciences, Rutgers, , New Brunswick, NJ , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Toby","family":"Lo","sequence":"additional","affiliation":[{"name":"The State University of New Jersey Department of Animal Sciences, Rutgers, , New Brunswick, NJ , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gayatri","family":"Mohanty","sequence":"additional","affiliation":[{"name":"University of Massachusetts Department of Veterinary and Animal Sciences, , Amherst, MA , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pablo E","family":"Visconti","sequence":"additional","affiliation":[{"name":"University of Massachusetts Department of Veterinary and Animal Sciences, , Amherst, MA , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elizabeth M","family":"Snyder","sequence":"additional","affiliation":[{"name":"The State University of New Jersey Department of Animal Sciences, Rutgers, , New Brunswick, NJ , USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2023,7,3]]},"reference":[{"key":"2023091508552439200_ref1","doi-asserted-by":"crossref","first-page":"1838","DOI":"10.1016\/j.bbadis.2012.02.008","article-title":"Molecular control of rodent spermatogenesis","volume":"1822","author":"Jan","year":"2012","journal-title":"Biochim Biophys Acta\u2014Mol Basis Dis"},{"key":"2023091508552439200_ref2","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.gene.2018.03.059","article-title":"The acroframosome-acroplaxome-manchette axis may function in sperm head shaping and male fertility","volume":"660","author":"Wei","year":"2018","journal-title":"Gene"},{"key":"2023091508552439200_ref3","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/0014-4827(65)90023-6","article-title":"Synthetic activities during spermatogenesis in the mouse","volume":"39","author":"Monesi","year":"1965","journal-title":"Exp Cell Res"},{"key":"2023091508552439200_ref4","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1007\/s004290050245","article-title":"Transcriptional and translational regulation of gene expression in haploid spermatids","volume":"199","author":"Steger","year":"1999","journal-title":"Anat Embryol"},{"key":"2023091508552439200_ref5","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/0012-1606(84)90262-8","article-title":"Translational regulation and deadenylation of a protamine mRNA during spermiogenesis in the mouse","volume":"105","author":"Kleene","year":"1984","journal-title":"Dev Biol"},{"key":"2023091508552439200_ref6","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1093\/molehr\/4.10.939","article-title":"Expression of mRNA and protein of nucleoproteins during human spermiogenesis","volume":"4","author":"Steger","year":"1998","journal-title":"Mol Hum Reprod"},{"key":"2023091508552439200_ref7","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/0014-4827(84)90572-X","article-title":"DNA packaging in mouse spermatids","volume":"150","author":"Balhorn","year":"1984","journal-title":"Exp Cell Res"},{"key":"2023091508552439200_ref8","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1002\/(SICI)1098-2795(199602)43:2<268::AID-MRD17>3.0.CO;2-#","article-title":"Patterns of translational regulation in the mammalian testis","volume":"43","author":"Kleene","year":"1996","journal-title":"Mol Reprod Dev"},{"key":"2023091508552439200_ref9","doi-asserted-by":"crossref","first-page":"12451","DOI":"10.1073\/pnas.92.26.12451","article-title":"Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice","volume":"92","author":"Lee","year":"1995","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2023091508552439200_ref10","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1038\/9684","article-title":"A double-stranded RNA binding protein required for activation of repressed messages in mammalian germ cells","volume":"22","author":"Zhong","year":"1999","journal-title":"Nat Genet"},{"key":"2023091508552439200_ref11","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1038\/ng0501-10","article-title":"Packaging paternal chromosomes with protamine","volume":"28","author":"Braun","year":"2001","journal-title":"Nat Genet"},{"key":"2023091508552439200_ref12","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1002\/(SICI)1098-2795(200006)56:2+<230::AID-MRD3>3.0.CO;2-V","article-title":"DNA condensation by protamine and arginine-rich peptides: analysis of toroid stability using single DNA molecules","volume":"56","author":"Balhorn","year":"2000","journal-title":"Mol Reprod Dev"},{"key":"2023091508552439200_ref13","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1095\/biolreprod.114.124255","article-title":"Sperm protamine-status correlates to the fertility of breeding bulls","volume":"92","author":"Dogan","year":"2015","journal-title":"Biol Reprod"},{"key":"2023091508552439200_ref14","doi-asserted-by":"crossref","first-page":"4683","DOI":"10.1073\/pnas.97.9.4683","article-title":"Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice","volume":"97","author":"Yu","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2023091508552439200_ref15","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1101\/gad.3.6.793","article-title":"Protamine 3\u2032-untranslated sequences regulate temporal translational control and subcellular localization of growth hormone in spermatids of transgenic mice","volume":"3","author":"Braun","year":"1989","journal-title":"Genes Dev"},{"key":"2023091508552439200_ref16","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1002\/(SICI)1521-1878(199807)20:7<555::AID-BIES6>3.0.CO;2-J","article-title":"Molecular mechanisms of male germ cell differentiation","volume":"20","author":"Hecht","year":"1998","journal-title":"Bioessays"},{"key":"2023091508552439200_ref17","doi-asserted-by":"crossref","first-page":"e1005690","DOI":"10.1371\/journal.pgen.1005690","article-title":"Compound heterozygosity for Y box proteins causes sterility due to loss of translational repression","volume":"11","author":"Snyder","year":"2015","journal-title":"PLoS Genet"},{"key":"2023091508552439200_ref18","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1172\/JCI43350","article-title":"The poly(a)-binding protein partner Paip2a controls translation during late spermiogenesis in mice","volume":"120","author":"Yanagiya","year":"2010","journal-title":"J Clin Invest"},{"key":"2023091508552439200_ref19","article-title":"Distribution of Tenr, an RNA-binding protein, in a lattice-like network within the spermatid nucleus in the Mousel","author":"Schumacher","year":".."},{"key":"2023091508552439200_ref20","doi-asserted-by":"crossref","first-page":"11536","DOI":"10.1038\/s41598-020-67834-5","article-title":"ADAD1 and ADAD2, testis-specific adenosine deaminase domain-containing proteins, are required for male fertility","volume":"10","author":"Snyder","year":"2020","journal-title":"Sci Rep"},{"key":"2023091508552439200_ref21","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.ydbio.2004.10.009","article-title":"Disruption of murine Tenr results in teratospermia and male infertility","volume":"278","author":"Connolly","year":"2005","journal-title":"Dev Biol"},{"key":"2023091508552439200_ref22","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/nrm.2015.4","article-title":"A-to-I editing of coding and non-coding RNAs by ADARs","volume":"17","author":"Nishikura","year":"2016","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2023091508552439200_ref23","doi-asserted-by":"crossref","first-page":"13939","DOI":"10.1073\/pnas.0907143106","article-title":"Cell-type-specific isolation of ribosome-associated mRNA from complex tissues","volume":"106","author":"Sanz","year":"2009","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2023091508552439200_ref24","article-title":"RiboTag immunoprecipitation in the germ cells of the male mouse","volume":"157","author":"Chukrallah","year":"2020","journal-title":"J Vis Exp"},{"key":"2023091508552439200_ref25","volume-title":"Cytometry"},{"key":"2023091508552439200_ref26","volume-title":"Histological and Histopathological Evaluation of the Testis","author":"Russell","year":"1990","edition":"1st"},{"key":"2023091508552439200_ref27","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1095\/biolreprod.103.026880","article-title":"The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis","volume":"71","author":"Shima","year":"2004","journal-title":"Biol Reprod"},{"key":"2023091508552439200_ref28","doi-asserted-by":"crossref","first-page":"3047","DOI":"10.1093\/bioinformatics\/btw354","article-title":"MultiQC: summarize analysis results for multiple tools and samples in a single report","volume":"32","author":"Ewels","year":"2016","journal-title":"Bioinformatics"},{"key":"2023091508552439200_ref29","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat Methods"},{"key":"2023091508552439200_ref30","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"2023091508552439200_ref31","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1186\/s12859-019-2879-1","article-title":"pcaExplorer: an R\/Bioconductor package for interacting with RNA-seq principal components","volume":"20","author":"Marini","year":"2019","journal-title":"BMC Bioinformatics"},{"key":"2023091508552439200_ref32","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1530\/REP-19-0092","article-title":"An expanded mouse testis transcriptome and mass spectrometry defines novel proteins","volume":"159","author":"Gamble","year":"2020","journal-title":"Reproduction"},{"key":"2023091508552439200_ref33","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1186\/1471-2105-12-323","article-title":"RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome","volume":"12","author":"Li","year":"2011","journal-title":"BMC Bioinformatics"},{"key":"2023091508552439200_ref34","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1093\/bioinformatics\/btt087","article-title":"EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments","volume":"29","author":"Leng","year":"2013","journal-title":"Bioinformatics"},{"key":"2023091508552439200_ref35","doi-asserted-by":"crossref","first-page":"1952","DOI":"10.1093\/bioinformatics\/btz834","article-title":"DiscoRhythm: an easy-to-use web application and R package for discovering rhythmicity","volume":"36","author":"Carlucci","year":"2020","journal-title":"Bioinformatics"},{"key":"2023091508552439200_ref36","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Huang","year":"2009","journal-title":"Nat Protoc"},{"key":"2023091508552439200_ref37","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1186\/gb-2007-8-9-227","article-title":"The protamine family of sperm nuclear proteins","volume":"8","author":"Balhorn","year":"2007","journal-title":"Genome Biol"},{"key":"2023091508552439200_ref38","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1002\/1097-0320(20010601)44:2<113::AID-CYTO1089>3.0.CO;2-A","article-title":"Relationship between chromatin compactness and dye uptake for in situ chromatin stained with DAPI","volume":"44","author":"Mascetti","year":"2001","journal-title":"Cytometry"},{"key":"2023091508552439200_ref39","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1038\/labinvest.2017.13","article-title":"Blue intensity matters for cell cycle profiling in fluorescence DAPI-stained images","volume":"97","author":"Ferro","year":"2017","journal-title":"Lab Invest"},{"key":"2023091508552439200_ref40","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1093\/molehr\/4.2.127","article-title":"In-situ competition between protamine and fluorochromes for sperm DNA","volume":"4","author":"Bizzaro","year":"1998","journal-title":"Mol Hum Reprod"},{"key":"2023091508552439200_ref41","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1111\/j.1365-2605.1996.tb00429.x","article-title":"Chromomycin A3-staining as an indicator of protamine deficiency and fertilization","volume":"19","author":"Lolis","year":"1996","journal-title":"Int J Androl"},{"key":"2023091508552439200_ref42","first-page":"2","article-title":"Signaling mechanisms in mammalian sperm motility","volume":"96","author":"Freitas","year":"2017","journal-title":"Biol Reprod"},{"key":"2023091508552439200_ref43","doi-asserted-by":"crossref","first-page":"244","DOI":"10.2164\/jandrol.110.012492","article-title":"Identification of potential regulatory elements in the 5\u2032 and 3\u2032 UTRs of 12 translationally regulated mRNAs in mammalian spermatids by comparative genomics","volume":"33","author":"Chowdhury","year":"2012","journal-title":"J Androl"},{"key":"2023091508552439200_ref44","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1006\/dbio.2002.0728","article-title":"Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility","volume":"248","author":"Miki","year":"2002","journal-title":"Dev Biol"},{"key":"2023091508552439200_ref45","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1261\/rna.043729.113","article-title":"An atlas of chromatoid body components","volume":"20","author":"Meikar","year":"2014","journal-title":"RNA"},{"key":"2023091508552439200_ref46","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1095\/biolreprod.104.028191","article-title":"Nucleoprotein transitions during spermiogenesis in mice with transition nuclear protein Tnp1 and Tnp2 mutations","volume":"71","author":"Zhao","year":"2004","journal-title":"Biol Reprod"},{"key":"2023091508552439200_ref47","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1095\/biolreprod.104.029363","article-title":"Abnormalities and reduced reproductive potential of sperm from Tnp1- and Tnp2-null double mutant mice","volume":"71","author":"Shirley","year":"2004","journal-title":"Biol Reprod"},{"key":"2023091508552439200_ref48","doi-asserted-by":"crossref","first-page":"37922","DOI":"10.1038\/srep37922","article-title":"A-kinase anchoring protein 4 (AKAP4) is an ERK1\/2 substrate and a switch molecule between cAMP\/PKA and PKC\/ERK1\/2 in human spermatozoa","volume":"6","author":"Rahamim Ben-Navi","year":"2016","journal-title":"Sci Rep"},{"key":"2023091508552439200_ref49","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/mrd.10179","article-title":"Intramanchette transport (IMT): managing the making of the spermatid head, centrosome, and tail","volume":"63","author":"Kierszenbaum","year":"2002","journal-title":"Mol Reprod Dev"},{"key":"2023091508552439200_ref50","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1095\/biolreprod38.2.385","article-title":"Nuclear and manchette development in spermatids of normal and azh\/azh mutant mice","volume":"38","author":"Cole","year":"1988","journal-title":"Biol Reprod"},{"key":"2023091508552439200_ref51","doi-asserted-by":"crossref","first-page":"e1005090","DOI":"10.1371\/journal.pgen.1005090","article-title":"LRGUK-1 is required for basal body and manchette function during spermatogenesis and male fertility","volume":"11","author":"Liu","year":"2015","journal-title":"PLoS Genet"},{"key":"2023091508552439200_ref52","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1242\/dev.030858","article-title":"RIM-BP3 is a manchette-associated protein essential for spermiogenesis","volume":"136","author":"Zhou","year":"2009","journal-title":"Development"},{"key":"2023091508552439200_ref53","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/0012-1606(71)90124-2","article-title":"Morphogenetic factors influencing the shape of the sperm head","volume":"26","author":"Fawcett","year":"1971","journal-title":"Dev Biol"},{"key":"2023091508552439200_ref54","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1051\/rnd:19810312","article-title":"The spermatid manchette of mammals\u00a0: formation and relations with the nuclear envelope and the chromatin","volume":"21","author":"Courtens","year":"1981","journal-title":"Reprod Nutr D\u00e9velop"},{"key":"2023091508552439200_ref55","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1006\/dbio.1998.8942","article-title":"Isolation of the rat spermatid manchette and its perinuclear ring","volume":"200","author":"Mochida","year":"1998","journal-title":"Dev Biol"},{"key":"2023091508552439200_ref56","doi-asserted-by":"crossref","first-page":"3702","DOI":"10.3390\/ijms21103702","article-title":"Sperm differentiation: the role of trafficking of proteins","volume":"21","author":"Teves","year":"2020","journal-title":"IJMS"},{"key":"2023091508552439200_ref57","first-page":"7","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":"11","author":"Tapia Contreras","year":"2019","journal-title":"Front Cell Dev Biol"},{"key":"2023091508552439200_ref58","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1038\/5673","article-title":"Snapin: a SNARE\u2013associated protein implicated in synaptic transmission","volume":"2","author":"Ilardi","year":"1999","journal-title":"Nat Neurosci"},{"key":"2023091508552439200_ref59","doi-asserted-by":"crossref","first-page":"9058","DOI":"10.3390\/ijms21239058","article-title":"The role of the LINC complex in sperm development and function","volume":"21","author":"Kmonickova","year":"2020","journal-title":"IJMS"},{"key":"2023091508552439200_ref60","doi-asserted-by":"crossref","first-page":"6289","DOI":"10.1074\/jbc.RA119.012375","article-title":"The testis-specific LINC component SUN3 is essential for sperm head shaping during mouse spermiogenesis","volume":"295","author":"Gao","year":"2020","journal-title":"J Biol Chem"},{"key":"2023091508552439200_ref61","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1186\/gb-2011-12-5-222","article-title":"The Lamin protein family","volume":"12","author":"Dittmer","year":"2011","journal-title":"Genome Biol"},{"key":"2023091508552439200_ref62","doi-asserted-by":"crossref","first-page":"e12072","DOI":"10.1371\/journal.pone.0012072","article-title":"Mammalian sperm head formation involves different polarization of two novel LINC complexes","volume":"5","author":"G\u00f6b","year":"2010","journal-title":"PloS One"},{"key":"2023091508552439200_ref63","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1242\/jcs.104.2.557","article-title":"Presence of a nuclear lamina in pachytene spermatocytes of the rat","volume":"104","author":"Vester","year":"1993","journal-title":"J Cell Sci"},{"key":"2023091508552439200_ref64","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/j.yexcr.2005.03.023","article-title":"Nuclear envelope remodeling during mouse spermiogenesis: postmeiotic expression and redistribution of germline Lamin B3","volume":"307","author":"Sch\u00fctz","year":"2005","journal-title":"Exp Cell Res"},{"key":"2023091508552439200_ref65","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1242\/jcs.083246","article-title":"The nuclear pore complex\u2014structure and function at a glance","volume":"128","author":"Kabachinski","year":"2015","journal-title":"J Cell Sci"},{"key":"2023091508552439200_ref66","doi-asserted-by":"crossref","first-page":"2382","DOI":"10.1091\/mbc.e04-10-0857","article-title":"Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex","volume":"16","author":"Hawryluk-Gara","year":"2005","journal-title":"Mol Biol Cell"},{"key":"2023091508552439200_ref67","doi-asserted-by":"crossref","first-page":"1911","DOI":"10.3390\/ijms17111911","article-title":"SEPT12-NDC1 complexes are required for mammalian spermiogenesis","volume":"17","author":"Lai","year":"2016","journal-title":"Int J Mol Sci"},{"key":"2023091508552439200_ref68","doi-asserted-by":"crossref","DOI":"10.3389\/fphys.2020.00239","article-title":"Role of nucleoporins and transport receptors in cell differentiation","volume":"11","author":"Khan","year":"2020","journal-title":"Front Physiol"},{"key":"2023091508552439200_ref69","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.molcel.2004.12.010","article-title":"The integral membrane nucleoporin pom121 functionally links nuclear pore complex assembly and nuclear envelope formation","volume":"17","author":"Antonin","year":"2005","journal-title":"Mol Cell"},{"key":"2023091508552439200_ref70","doi-asserted-by":"crossref","first-page":"4230","DOI":"10.1091\/mbc.e03-04-0260","article-title":"Nuclear pore protein gp210 is essential for viability in HeLa cells and Caenorhabditis elegans","volume":"14","author":"Cohen","year":"2003","journal-title":"Mol Biol Cell"},{"key":"2023091508552439200_ref71","doi-asserted-by":"crossref","first-page":"ddad012","DOI":"10.1093\/hmg\/ddad012","article-title":"Population-based genetic analysis in infertile men reveals novel mutations of ADAD family members in patients with impaired spermatogenesis","volume":"32","author":"Dai","year":"2023","journal-title":"Hum Mol Genet"},{"key":"2023091508552439200_ref72","first-page":"1","article-title":"The RNA-binding protein DAZL functions as repressor and activator of mRNA translation during oocyte maturation","volume":"11","author":"Yang","year":"2020","journal-title":"Nat Commun"},{"key":"2023091508552439200_ref73","doi-asserted-by":"crossref","first-page":"7851","DOI":"10.1073\/pnas.1916471117","article-title":"Pumilio proteins utilize distinct regulatory mechanisms to achieve complementary functions required for pluripotency and embryogenesis","volume":"117","author":"Uyhazi","year":"2020","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2023091508552439200_ref74","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1261\/rna.038042.112","article-title":"Global regulation of alternative splicing by adenosine deaminase acting on RNA (ADAR)","volume":"19","author":"Solomon","year":"2013","journal-title":"RNA"},{"key":"2023091508552439200_ref75","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1016\/j.celrep.2019.03.095","article-title":"Disruption in A-to-I editing levels affects C. elegans development more than a complete lack of editing","volume":"27","author":"Ganem","year":"2019","journal-title":"Cell Rep"},{"key":"2023091508552439200_ref76","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1038\/nsmb.3403","article-title":"ADAR1 controls apoptosis of stressed cells by inhibiting Staufen1-mediated mRNA decay","volume":"24","author":"Sakurai","year":"2017","journal-title":"Nat Struct Mol Biol"},{"key":"2023091508552439200_ref77","doi-asserted-by":"crossref","first-page":"3219","DOI":"10.1242\/jcs.184184","article-title":"The LINC and NPC relationship\u2014it\u2019s complicated!","volume":"129","author":"Jahed","year":"2016","journal-title":"J Cell Sci"},{"key":"2023091508552439200_ref78","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1042\/BST0380829","article-title":"Relationships at the nuclear envelope: lamins and nuclear pore complexes in animals and plants","volume":"38","author":"Fiserova","year":"2010","journal-title":"Biochem Soc Trans"},{"key":"2023091508552439200_ref79","doi-asserted-by":"crossref","first-page":"2417","DOI":"10.1016\/j.molcel.2021.03.030","article-title":"Co-translational assembly and localized translation of nucleoporins in nuclear pore complex biogenesis","volume":"81","author":"Lautier","year":"2021","journal-title":"Mol Cell"},{"key":"2023091508552439200_ref80","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1007\/978-1-62703-038-0_27","volume-title":"Spermatogenesis: Methods and Protocols","author":"Meistrich","year":"2013"},{"key":"2023091508552439200_ref81","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a000554","article-title":"Lamin-binding proteins","volume":"2","author":"Wilson","year":"2010","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"2023091508552439200_ref82","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1003261","article-title":"The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse","volume":"9","author":"Link","year":"2013","journal-title":"PLoS Genet"},{"key":"2023091508552439200_ref83","doi-asserted-by":"crossref","first-page":"1363","DOI":"10.1242\/jcs.111.10.1363","article-title":"Clustering of pericentromeres initiates in step 9 of spermiogenesis of the rat (Rattus norvegicus) and contributes to a well defined genome architecture in the sperm nucleus","volume":"111","author":"Meyer-Ficca","year":"1998","journal-title":"J Cell Sci"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioad069\/50907298\/ioad069.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/109\/3\/340\/51523547\/ioad069.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/article-pdf\/109\/3\/340\/51523547\/ioad069.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,23]],"date-time":"2024-10-23T10:38:54Z","timestamp":1729679934000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/109\/3\/340\/7218337"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,3]]},"references-count":83,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2023,7,3]]},"published-print":{"date-parts":[[2023,9,12]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioad069","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,9]]},"published":{"date-parts":[[2023,7,3]]}}}