{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T05:10:30Z","timestamp":1791263430565,"version":"4.1.0"},"reference-count":42,"publisher":"The Company of Biologists","license":[{"start":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T00:00:00Z","timestamp":1621296000000},"content-version":"am","delay-in-days":2694,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>Biogenesis of 40S pre-ribosomal subunits requires many trans-acting factors, among them several protein kinases. In this study we show that the human CK1 isoforms \u03b4 and \u03b5 are required for cytoplasmic maturation steps of 40S subunit precursors. We show that both CK1 \u03b4 and \u03b5 isoforms are components of pre-40S subunits, where they phosphorylate the ribosome biogenesis factors ENP1\/BYSL and LTV1. CK1 inhibition or co-depletion of CK1\u03b4 and \u03b5 result in failure to recycle a series of trans-acting factors including ENP1\/BYSL, LTV1, RRP12, DIM2\/PNO1, RIO2 and NOB1 from pre-40S particles after nuclear export. Further, CK1\u03b4\/\u03b5 co-depletion leads to defects in 18S-E pre-rRNA processing. Together, these data demonstrate that CK1\u03b4 and \u03b5 play a decisive role in triggering late steps of pre-40S maturation that are required for acquisition of functionality of 40S ribosomal subunits in protein translation.<\/jats:p>","DOI":"10.1242\/jcs.138719","type":"journal-article","created":{"date-parts":[[2014,1,15]],"date-time":"2014-01-15T06:23:57Z","timestamp":1389767037000},"source":"Crossref","is-referenced-by-count":36,"title":["CK1\u03b4 and CK1\u03b5 are components of human 40S subunit precursors required for cytoplasmic 40S maturation"],"prefix":"10.1242","author":[{"given":"Ivo","family":"Zemp","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Franziska","family":"Wandrey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sanjana","family":"Rao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Ashiono","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emanuel","family":"Wyler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian","family":"Montellese","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ulrike","family":"Kutay","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","published-online":{"date-parts":[[2014,1,1]]},"reference":[{"key":"2021042614260223600_b1","doi-asserted-by":"publisher","first-page":"730","DOI":"10.1124\/jpet.107.122846","article-title":"An inhibitor of casein kinase I epsilon induces phase delays in circadian rhythms under free-running and entrained conditions.","volume":"322","author":"Badura","year":"2007","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"2021042614260223600_b2","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1042\/BJ20070797","article-title":"The selectivity of protein kinase inhibitors: a further update.","volume":"408","author":"Bain","year":"2007","journal-title":"Biochem. J."},{"key":"2021042614260223600_b3","doi-asserted-by":"publisher","first-page":"1453","DOI":"10.1128\/MCB.21.5.1453-1462.2001","article-title":"The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis.","volume":"21","author":"Basu","year":"2001","journal-title":"Mol. Cell. Biol."},{"key":"2021042614260223600_b4","doi-asserted-by":"publisher","first-page":"162","DOI":"10.4161\/rna.18810","article-title":"Human RioK3 is a novel component of cytoplasmic pre-40S pre-ribosomal particles.","volume":"9","author":"Baumas","year":"2012","journal-title":"RNA Biol."},{"key":"2021042614260223600_b5","doi-asserted-by":"publisher","first-page":"5303","DOI":"10.1038\/sj.onc.1203939","article-title":"IC261, a specific inhibitor of the protein kinases casein kinase 1-delta and -epsilon, triggers the mitotic checkpoint and induces p53-dependent postmitotic effects.","volume":"19","author":"Behrend","year":"2000","journal-title":"Oncogene"},{"key":"2021042614260223600_b6","doi-asserted-by":"publisher","first-page":"3129","DOI":"10.1074\/jbc.M110.188565","article-title":"Opposing action of casein kinase 1 and calcineurin in nucleo-cytoplasmic shuttling of mammalian translation initiation factor eIF6.","volume":"286","author":"Biswas","year":"2011","journal-title":"J. Biol. Chem."},{"key":"2021042614260223600_b7","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1016\/j.cellsig.2006.08.011","article-title":"Wnt-3a utilizes a novel low dose and rapid pathway that does not require casein kinase 1-mediated phosphorylation of Dvl to activate beta-catenin.","volume":"19","author":"Bryja","year":"2007","journal-title":"Cell. Signal."},{"key":"2021042614260223600_b8","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1093\/nar\/gkq734","article-title":"Analysis of two human pre-ribosomal factors, bystin and hTsr1, highlights differences in evolution of ribosome biogenesis between yeast and mammals.","volume":"39","author":"Carron","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"2021042614260223600_b9","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1016\/j.biocel.2010.12.004","article-title":"Casein kinase 1: Complexity in the family.","volume":"43","author":"Cheong","year":"2011","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"2021042614260223600_b10","doi-asserted-by":"publisher","first-page":"3853","DOI":"10.1128\/MCB.00338-09","article-title":"Casein kinase 1 delta regulates the pace of the mammalian circadian clock.","volume":"29","author":"Etchegaray","year":"2009","journal-title":"Mol. Cell. Biol."},{"key":"2021042614260223600_b11","doi-asserted-by":"publisher","first-page":"1316","DOI":"10.1038\/nsmb.2403","article-title":"ATPase-dependent role of the atypical kinase Rio2 on the evolving pre-40S ribosomal subunit.","volume":"19","author":"Ferreira-Cerca","year":"2012","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2021042614260223600_b12","doi-asserted-by":"publisher","first-page":"14875","DOI":"10.1074\/jbc.270.25.14875","article-title":"Isolation and characterization of human casein kinase I epsilon (CKI), a novel member of the CKI gene family.","volume":"270","author":"Fish","year":"1995","journal-title":"J. Biol. Chem."},{"key":"2021042614260223600_b13","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/S0378-1119(03)00629-2","article-title":"Ribosome assembly in eukaryotes.","volume":"313","author":"Fromont-Racine","year":"2003","journal-title":"Gene"},{"key":"2021042614260223600_b14","doi-asserted-by":"publisher","first-page":"993","DOI":"10.1083\/jcb.201011111","article-title":"Casein kinase 1 delta functions at the centrosome to mediate Wnt-3a-dependent neurite outgrowth.","volume":"192","author":"Greer","year":"2011","journal-title":"J. Cell Biol."},{"key":"2021042614260223600_b15","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1016\/S0898-6568(98)00042-4","article-title":"Casein kinase I: spatial organization and positioning of a multifunctional protein kinase family.","volume":"10","author":"Gross","year":"1998","journal-title":"Cell. Signal."},{"key":"2021042614260223600_b16","doi-asserted-by":"publisher","first-page":"2334","DOI":"10.1007\/s00018-008-8027-0","article-title":"The post-transcriptional steps of eukaryotic ribosome biogenesis.","volume":"65","author":"Henras","year":"2008","journal-title":"Cell. Mol. Life Sci."},{"key":"2021042614260223600_b17","doi-asserted-by":"publisher","first-page":"e1001455","DOI":"10.1371\/journal.pbio.1001455","article-title":"The circadian clock coordinates ribosome biogenesis.","volume":"11","author":"Jouffe","year":"2013","journal-title":"PLoS Biol."},{"key":"2021042614260223600_b18","doi-asserted-by":"publisher","first-page":"1727","DOI":"10.1038\/sj.onc.1201541","article-title":"p53 is phosphorylated in vitro and in vivo by the delta and epsilon isoforms of casein kinase 1 and enhances the level of casein kinase 1 delta in response to topoisomerase-directed drugs.","volume":"15","author":"Knippschild","year":"1997","journal-title":"Oncogene"},{"key":"2021042614260223600_b19","doi-asserted-by":"publisher","first-page":"675","DOI":"10.1016\/j.cellsig.2004.12.011","article-title":"The casein kinase 1 family: participation in multiple cellular processes in eukaryotes.","volume":"17","author":"Knippschild","year":"2005","journal-title":"Cell. Signal."},{"key":"2021042614260223600_b20","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1016\/j.bbamcr.2009.10.009","article-title":"Driving ribosome assembly.","volume":"1803","author":"Kressler","year":"2010","journal-title":"Biochim. Biophys. Acta"},{"key":"2021042614260223600_b21","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.jmb.2010.09.064","article-title":"An RNA conformational switch regulates pre-18S rRNA cleavage.","volume":"405","author":"Lamanna","year":"2011","journal-title":"J. Mol. Biol."},{"key":"2021042614260223600_b22","doi-asserted-by":"publisher","first-page":"744","DOI":"10.1038\/nsmb.2308","article-title":"Proofreading of pre-40S ribosome maturation by a translation initiation factor and 60S subunits.","volume":"19","author":"Lebaron","year":"2012","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2021042614260223600_b23","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1016\/S0092-8674(01)00610-9","article-title":"Posttranslational mechanisms regulate the mammalian circadian clock.","volume":"107","author":"Lee","year":"2001","journal-title":"Cell"},{"key":"2021042614260223600_b24","doi-asserted-by":"publisher","first-page":"10608","DOI":"10.1002\/anie.201103915","article-title":"A small molecule modulates circadian rhythms through phosphorylation of the period protein.","volume":"50","author":"Lee","year":"2011","journal-title":"Angew. Chem. Int. Ed. Engl."},{"key":"2021042614260223600_b25","doi-asserted-by":"publisher","first-page":"20052","DOI":"10.1074\/jbc.M001713200","article-title":"Crystal structure of a conformation-selective casein kinase-1 inhibitor.","volume":"275","author":"Mashhoon","year":"2000","journal-title":"J. Biol. Chem."},{"key":"2021042614260223600_b26","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1006\/excr.2000.5100","article-title":"Catalytic activity of protein kinase CK1 delta (casein kinase 1delta) is essential for its normal subcellular localization.","volume":"263","author":"Milne","year":"2001","journal-title":"Exp. Cell Res."},{"key":"2021042614260223600_b27","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1016\/j.tibs.2010.01.001","article-title":"Maturation of eukaryotic ribosomes: acquisition of functionality.","volume":"35","author":"Panse","year":"2010","journal-title":"Trends Biochem. Sci."},{"key":"2021042614260223600_b28","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1038\/43830","article-title":"Casein kinase I transduces Wnt signals.","volume":"401","author":"Peters","year":"1999","journal-title":"Nature"},{"key":"2021042614260223600_b29","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1038\/sj.embor.7400048","article-title":"D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a.","volume":"5","author":"Rena","year":"2004","journal-title":"EMBO Rep."},{"key":"2021042614260223600_b30","doi-asserted-by":"publisher","first-page":"2862","DOI":"10.1038\/sj.emboj.7600752","article-title":"Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells.","volume":"24","author":"Rouquette","year":"2005","journal-title":"EMBO J."},{"key":"2021042614260223600_b31","doi-asserted-by":"publisher","first-page":"651","DOI":"10.1038\/nature04840","article-title":"Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit.","volume":"441","author":"Sch\u00e4fer","year":"2006","journal-title":"Nature"},{"key":"2021042614260223600_b32","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1083\/jcb.201207131","article-title":"Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing.","volume":"200","author":"Sloan","year":"2013","journal-title":"J. Cell Biol."},{"key":"2021042614260223600_b33","doi-asserted-by":"publisher","first-page":"1449","DOI":"10.1126\/science.1208245","article-title":"Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates.","volume":"333","author":"Strunk","year":"2011","journal-title":"Science"},{"key":"2021042614260223600_b34","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.cell.2012.04.044","article-title":"A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits.","volume":"150","author":"Strunk","year":"2012","journal-title":"Cell"},{"key":"2021042614260223600_b35","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/S0962-8924(03)00054-0","article-title":"Pre-ribosomes on the road from the nucleolus to the cytoplasm.","volume":"13","author":"Tschochner","year":"2003","journal-title":"Trends Cell Biol."},{"key":"2021042614260223600_b36","doi-asserted-by":"publisher","first-page":"430","DOI":"10.1124\/jpet.109.151415","article-title":"Selective inhibition of casein kinase 1 epsilon minimally alters circadian clock period.","volume":"330","author":"Walton","year":"2009","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"2021042614260223600_b37","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1016\/S0968-0004(99)01460-7","article-title":"The economics of ribosome biosynthesis in yeast.","volume":"24","author":"Warner","year":"1999","journal-title":"Trends Biochem. Sci."},{"key":"2021042614260223600_b38","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1091\/mbc.E11-07-0639","article-title":"The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits.","volume":"23","author":"Widmann","year":"2012","journal-title":"Mol. Biol. Cell"},{"key":"2021042614260223600_b39","doi-asserted-by":"publisher","first-page":"e1000522","DOI":"10.1371\/journal.pbio.1000522","article-title":"A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export.","volume":"8","author":"Wild","year":"2010","journal-title":"PLoS Biol."},{"key":"2021042614260223600_b40","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1261\/rna.2325911","article-title":"Tandem affinity purification combined with inducible shRNA expression as a tool to study the maturation of macromolecular assemblies.","volume":"17","author":"Wyler","year":"2011","journal-title":"RNA"},{"key":"2021042614260223600_b41","doi-asserted-by":"publisher","first-page":"2783","DOI":"10.1016\/j.febslet.2007.05.013","article-title":"Nuclear export and cytoplasmic maturation of ribosomal subunits.","volume":"581","author":"Zemp","year":"2007","journal-title":"FEBS Lett."},{"key":"2021042614260223600_b42","doi-asserted-by":"publisher","first-page":"1167","DOI":"10.1083\/jcb.200904048","article-title":"Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2.","volume":"185","author":"Zemp","year":"2009","journal-title":"J. Cell Biol."}],"container-title":["Journal of Cell Science"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/127\/6\/1242\/1984700\/jcs-127-06-1242.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.138719\/2045926\/jcs138719.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/jcs\/article-pdf\/doi\/10.1242\/jcs.138719\/2045926\/jcs138719.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T18:24:34Z","timestamp":1621362274000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/jcs\/article\/doi\/10.1242\/jcs.138719\/263850\/CK1-and-CK1-are-components-of-human-40S-subunit"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2014,1,1]]},"references-count":42,"URL":"https:\/\/doi.org\/10.1242\/jcs.138719","relation":{},"ISSN":["1477-9137","0021-9533"],"issn-type":[{"value":"1477-9137","type":"electronic"},{"value":"0021-9533","type":"print"}],"subject":[],"published":{"date-parts":[[2014,1,1]]},"article-number":"jcs.138719"}}