{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T19:50:00Z","timestamp":1792093800769,"version":"4.4.0"},"reference-count":201,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2018,10,24]],"date-time":"2018-10-24T00:00:00Z","timestamp":1540339200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-15-CE12-0001"],"award-info":[{"award-number":["ANR-15-CE12-0001"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-16-CE11-0029"],"award-info":[{"award-number":["ANR-16-CE11-0029"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-15-RAR3-0007-04"],"award-info":[{"award-number":["ANR-15-RAR3-0007-04"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>Ribosomal RNAs, the most abundant cellular RNA species, have evolved as the structural scaffold and the catalytic center of protein synthesis in every living organism. In eukaryotes, they are produced from a long primary transcript through an intricate sequence of processing steps that include RNA cleavage and folding and nucleotide modification. The mechanisms underlying this process in human cells have long been investigated, but technological advances have accelerated their study in the past decade. In addition, the association of congenital diseases to defects in ribosome synthesis has highlighted the central place of ribosomal RNA maturation in cell physiology regulation and broadened the interest in these mechanisms. Here, we give an overview of the current knowledge of pre-ribosomal RNA processing in human cells in light of recent progress and discuss how dysfunction of this pathway may contribute to the physiopathology of congenital diseases.<\/jats:p>","DOI":"10.3390\/biom8040123","type":"journal-article","created":{"date-parts":[[2018,10,24]],"date-time":"2018-10-24T10:40:48Z","timestamp":1540377648000},"page":"123","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":131,"title":["Pre-Ribosomal RNA Processing in Human Cells: From Mechanisms to Congenital Diseases"],"prefix":"10.3390","volume":"8","author":[{"given":"Maxime","family":"Aubert","sequence":"first","affiliation":[{"name":"Laboratoire de Biologie Mol\u00e9culaire Eucaryote, Centre de Biologie Int\u00e9grative (CBI), Universit\u00e9 de Toulouse, CNRS, UPS, 31000 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1204-8285","authenticated-orcid":false,"given":"Marie-Fran\u00e7oise","family":"O\u2019Donohue","sequence":"additional","affiliation":[{"name":"Laboratoire de Biologie Mol\u00e9culaire Eucaryote, Centre de Biologie Int\u00e9grative (CBI), Universit\u00e9 de Toulouse, CNRS, UPS, 31000 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simon","family":"Lebaron","sequence":"additional","affiliation":[{"name":"Laboratoire de Biologie Mol\u00e9culaire Eucaryote, Centre de Biologie Int\u00e9grative (CBI), Universit\u00e9 de Toulouse, CNRS, UPS, 31000 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0830-7341","authenticated-orcid":false,"given":"Pierre-Emmanuel","family":"Gleizes","sequence":"additional","affiliation":[{"name":"Laboratoire de Biologie Mol\u00e9culaire Eucaryote, Centre de Biologie Int\u00e9grative (CBI), Universit\u00e9 de Toulouse, CNRS, UPS, 31000 Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2018,10,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1083\/jcb.1.1.59","article-title":"A small particulate component of the cytoplasm","volume":"1","author":"Palade","year":"1955","journal-title":"J. Biophys. Biochem. Cytol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1038\/23641","article-title":"Placement of protein and RNA structures into a 5 \u00c5-resolution map of the 50S ribosomal subunit","volume":"400","author":"Ban","year":"1999","journal-title":"Nature"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2095","DOI":"10.1126\/science.285.5436.2095","article-title":"X-ray crystal structures of 70S ribosome functional complexes","volume":"285","author":"Cate","year":"1999","journal-title":"Science"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1038\/23631","article-title":"Structure of a bacterial 30S ribosomal subunit at 5.5 \u00c5 resolution","volume":"400","author":"Clemons","year":"1999","journal-title":"Nature"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1524","DOI":"10.1126\/science.1212642","article-title":"The structure of the eukaryotic ribosome at 3.0 \u00c5 resolution","volume":"334","author":"Melnikov","year":"2011","journal-title":"Science"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1126\/science.1211204","article-title":"Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6","volume":"334","author":"Klinge","year":"2011","journal-title":"Science"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"730","DOI":"10.1126\/science.1198308","article-title":"Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1","volume":"331","author":"Rabl","year":"2011","journal-title":"Science"},{"key":"ref_8","doi-asserted-by":"crossref","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":"ref_9","doi-asserted-by":"crossref","first-page":"1228","DOI":"10.1038\/nsmb.2425","article-title":"Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit","volume":"19","author":"Greber","year":"2012","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3491","DOI":"10.1038\/ncomms4491","article-title":"60S ribosome biogenesis requires rotation of the 5S ribonucleoprotein particle","volume":"5","author":"Leidig","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"914","DOI":"10.1038\/nsmb.3112","article-title":"Mechanism of eIF6 release from the nascent 60S ribosomal subunit","volume":"22","author":"Weis","year":"2015","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1016\/j.cell.2016.06.014","article-title":"Architecture of the 90S Pre-ribosome: A Structural View on the Birth of the Eukaryotic Ribosome","volume":"166","author":"Kornprobst","year":"2016","journal-title":"Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1038\/nature17942","article-title":"Diverse roles of assembly factors revealed by structures of late nuclear pre-60S ribosomes","volume":"534","author":"Wu","year":"2016","journal-title":"Nature"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Sun, Q., Zhu, X., Qi, J., An, W., Lan, P., Tan, D., Chen, R., Wang, B., Zheng, S., and Zhang, C. (2017). Molecular architecture of the 90S small subunit pre-ribosome. eLife, 6.","DOI":"10.7554\/eLife.22086"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Chaker-Margot, M., Barandun, J., Hunziker, M., and Klinge, S. (2017). Architecture of the yeast small subunit processome. Science, 355.","DOI":"10.1126\/science.aal1880"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Heuer, A., Thomson, E., Schmidt, C., Berninghausen, O., Becker, T., Hurt, E., and Beckmann, R. (2017). Cryo-EM structure of a late pre-40S ribosomal subunit from Saccharomyces cerevisiae. eLife, 6.","DOI":"10.7554\/eLife.30189"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Scaiola, A., Pe\u00f1a, C., Weisser, M., B\u00f6hringer, D., Leibundgut, M., Klingauf-Nerurkar, P., Gerhardy, S., Panse, V.G., and Ban, N. (2018). Structure of a eukaryotic cytoplasmic pre-40S ribosomal subunit. EMBO J., 37.","DOI":"10.15252\/embj.201798499"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"8465","DOI":"10.1093\/nar\/gkw714","article-title":"Structure of a human pre-40S particle points to a role for RACK1 in the final steps of 18S rRNA processing","volume":"44","author":"Larburu","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1038\/nature14427","article-title":"Structure of the human 80S ribosome","volume":"520","author":"Khatter","year":"2015","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1038\/s41586-018-0193-0","article-title":"Visualizing late states of human 40S ribosomal subunit maturation","volume":"558","author":"Ameismeier","year":"2018","journal-title":"Nature"},{"key":"ref_21","doi-asserted-by":"crossref","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. CMLS"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1534\/genetics.113.153197","article-title":"Ribosome biogenesis in the yeast Saccharomyces cerevisiae","volume":"195","author":"Woolford","year":"2013","journal-title":"Genetics"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.molcel.2013.08.011","article-title":"The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of Pre-rRNA processing factors","volume":"51","author":"Tafforeau","year":"2013","journal-title":"Mol. Cell"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1038\/nature03207","article-title":"Nucleolar proteome dynamics","volume":"433","author":"Andersen","year":"2005","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1002\/mas.20067","article-title":"Deciphering the human nucleolar proteome","volume":"25","author":"Coute","year":"2006","journal-title":"Mass Spectrom. Rev."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Wild, T., Horvath, P., Wyler, E., Widmann, B., Badertscher, L., Zemp, I., Kozak, K., Csucs, G., Lund, E., and Kutay, U. (2010). A protein inventory of human ribosome biogenesis reveals an essential function of exportin 5 in 60S subunit export. PLoS Biol., 8.","DOI":"10.1371\/journal.pbio.1000522"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1923","DOI":"10.1016\/j.celrep.2018.01.056","article-title":"Diverse Regulators of Human Ribosome Biogenesis Discovered by Changes in Nucleolar Number","volume":"22","author":"McCann","year":"2018","journal-title":"Cell Rep."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1242\/dmm.020529","article-title":"Ribosomopathies: how a common root can cause a tree of pathologies","volume":"8","author":"Danilova","year":"2015","journal-title":"Dis. Model. Mech."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"e1025185","DOI":"10.1080\/21675511.2015.1025185","article-title":"Ribosomopathies: Global process, tissue specific defects","volume":"3","author":"Yelick","year":"2015","journal-title":"Rare Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1521","DOI":"10.1016\/j.biochi.2012.02.001","article-title":"Mapping the cleavage sites on mammalian pre-rRNAs: Where do we stand?","volume":"94","author":"Mullineux","year":"2012","journal-title":"Biochimie"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1002\/wrna.1269","article-title":"An overview of pre-ribosomal RNA processing in eukaryotes","volume":"6","author":"Henras","year":"2015","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1801","DOI":"10.1002\/1873-3468.12682","article-title":"Comparison of preribosomal RNA processing pathways in yeast, plant and human cells\u2013focus on coordinated action of endo- and exoribonucleases","volume":"591","author":"Tomecki","year":"2017","journal-title":"FEBS Lett."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1111\/j.1432-1033.1991.tb15743.x","article-title":"Secondary structure of the 5\u2032 external transcribed spacer of vertebrate pre-rRNA. Presence of phylogenetically conserved features","volume":"195","author":"Michot","year":"1991","journal-title":"Eur. J. Biochem. FEBS"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1002\/wrna.74","article-title":"Eukaryotic 5S rRNA biogenesis: Eukaryotic 5S rRNA biogenesis","volume":"2","author":"Ciganda","year":"2011","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1016\/j.celrep.2017.09.067","article-title":"The Conserved RNA Exonuclease Rexo5 Is Required for 3\u2032 End Maturation of 28S rRNA, 5S rRNA, and snoRNAs","volume":"21","author":"Gerstberger","year":"2017","journal-title":"Cell Rep."},{"key":"ref_36","doi-asserted-by":"crossref","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":"ref_37","doi-asserted-by":"crossref","first-page":"4709","DOI":"10.1093\/nar\/gkt160","article-title":"Gradual processing of the ITS1 from the nucleolus to the cytoplasm during synthesis of the human 18S rRNA","volume":"41","author":"Preti","year":"2013","journal-title":"Nucleic Acids Res."},{"key":"ref_38","doi-asserted-by":"crossref","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":"ref_39","doi-asserted-by":"crossref","first-page":"6822","DOI":"10.1093\/nar\/gkx253","article-title":"Poly(A)-specific ribonuclease is a nuclear ribosome biogenesis factor involved in human 18S rRNA maturation","volume":"45","author":"Montellese","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1083\/jcb.201005117","article-title":"Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits","volume":"190","author":"Choesmel","year":"2010","journal-title":"J. Cell Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1182\/blood-2006-07-038372","article-title":"Impaired ribosome biogenesis in Diamond\u2013Blackfan anemia","volume":"109","author":"Choesmel","year":"2007","journal-title":"Blood"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1182\/blood-2006-07-038232","article-title":"Human RPS19, the gene mutated in Diamond\u2013Blackfan anemia, encodes a ribosomal protein required for the maturation of 40S ribosomal subunits","volume":"109","author":"Flygare","year":"2007","journal-title":"Blood"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Belin, S., Beghin, A., Solano-Gonzalez, E., Bezin, L., Brunet-Manquat, S., Textoris, J., Prats, A.C., Mertani, H.C., Dumontet, C., and Diaz, J.J. (2009). Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0007147"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/bs.enz.2017.03.007","article-title":"Synthesis, Function, and Heterogeneity of snoRNA-Guided Posttranscriptional Nucleoside Modifications in Eukaryotic Ribosomal RNAs","volume":"41","author":"Henras","year":"2017","journal-title":"Enzymes"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1002\/wrna.117","article-title":"The box C\/D and H\/ACA snoRNPs: Key players in the modification, processing and the dynamic folding of ribosomal RNA","volume":"3","author":"Watkins","year":"2012","journal-title":"Wiley Interdiscip. Rev. RNA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1080\/15476286.2016.1259781","article-title":"Tuning the ribosome: The influence of rRNA modification on eukaryotic ribosome biogenesis and function","volume":"14","author":"Sloan","year":"2017","journal-title":"RNA Biol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Taoka, M., Nobe, Y., Yamaki, Y., Sato, K., Ishikawa, H., Izumikawa, K., Yamauchi, Y., Hirota, K., Nakayama, H., and Takahashi, N. (2018). Landscape of the complete RNA chemical modifications in the human 80S ribosome. Nucleic Acids Res.","DOI":"10.1093\/nar\/gky811"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1038\/nature24482","article-title":"Visualization of chemical modifications in the human 80S ribosome structure","volume":"551","author":"Natchiar","year":"2017","journal-title":"Nature"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1093\/nar\/gkr700","article-title":"Loss of ribosomal RNA modification causes developmental defects in zebrafish","volume":"40","author":"Suzuki","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1101\/gad.228825.113","article-title":"A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains","volume":"28","author":"Gamalinda","year":"2014","journal-title":"Genes Dev."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1016\/j.cell.2017.11.039","article-title":"Visualizing the Assembly Pathway of Nucleolar Pre-60S Ribosomes","volume":"171","author":"Kater","year":"2017","journal-title":"Cell"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"35079","DOI":"10.1074\/jbc.M109.040774","article-title":"RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1","volume":"284","author":"Pertschy","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_53","doi-asserted-by":"crossref","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":"ref_54","doi-asserted-by":"crossref","first-page":"144","DOI":"10.15698\/mic2017.05.572","article-title":"Placeholder factors in ribosome biogenesis: please, pave my way","volume":"4","author":"Babiano","year":"2017","journal-title":"Microb. Cell"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1370","DOI":"10.1093\/emboj\/cdg121","article-title":"The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes","volume":"22","author":"Schafer","year":"2003","journal-title":"EMBO J."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1038\/nature00769","article-title":"A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis","volume":"417","author":"Dragon","year":"2002","journal-title":"Nature"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3007","DOI":"10.1128\/MCB.00029-09","article-title":"A novel small-subunit processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5, and DBP4","volume":"29","author":"Turner","year":"2009","journal-title":"Mol. Cell. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1261\/rna.043471.113","article-title":"The roles of SSU processome components and surveillance factors in the initial processing of human ribosomal RNA","volume":"20","author":"Sloan","year":"2014","journal-title":"RNA"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1260","DOI":"10.1038\/emboj.2009.79","article-title":"18S rRNA processing requires base pairings of snR30 H\/ACA snoRNA to eukaryote-specific 18S sequences","volume":"28","author":"Atzorn","year":"2009","journal-title":"EMBO J."},{"key":"ref_60","first-page":"4796","article-title":"The ribosome biogenesis factor yUtp23\/hUTP23 coordinates key interactions in the yeast and human pre-40S particle and hUTP23 contains an essential PIN domain","volume":"45","author":"Wells","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1101\/gad.286963.116","article-title":"Targeted CRISPR disruption reveals a role for RNase MRP RNA in human preribosomal RNA processing","volume":"31","author":"Goldfarb","year":"2017","journal-title":"Genes Dev."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"11180","DOI":"10.1093\/nar\/gku787","article-title":"Two orthogonal cleavages separate subunit RNAs in mouse ribosome biogenesis","volume":"42","author":"Wang","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"12509","DOI":"10.1093\/nar\/gkx963","article-title":"Nol12 is a multifunctional RNA binding protein at the nexus of RNA and DNA metabolism","volume":"45","author":"Scott","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"942","DOI":"10.1261\/rna.5256704","article-title":"Xenopus U3 snoRNA docks on pre-rRNA through a novel base-pairing interaction","volume":"10","author":"Borovjagin","year":"2004","journal-title":"RNA"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"5399","DOI":"10.1093\/nar\/gkw213","article-title":"The PIN domain endonuclease Utp24 cleaves pre-ribosomal RNA at two coupled sites in yeast and humans","volume":"44","author":"Wells","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.1080\/15476286.2015.1073437","article-title":"hUTP24 is essential for processing of the human rRNA precursor at site A1, but not at site A0","volume":"12","author":"Tomecki","year":"2015","journal-title":"RNA Biol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Ishikawa, H., Yoshikawa, H., Izumikawa, K., Miura, Y., Taoka, M., Nobe, Y., Yamauchi, Y., Nakayama, H., Simpson, R.J., and Isobe, T. (2016). Poly(A)-specific ribonuclease regulates the processing of small-subunit rRNAs in human cells. Nucleic Acids Res., gkw1047.","DOI":"10.1093\/nar\/gkw1047"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1016\/j.celrep.2018.03.089","article-title":"PARN and TOE1 Constitute a 3\u2032 End Maturation Module for Nuclear Noncoding RNAs","volume":"23","author":"Son","year":"2018","journal-title":"Cell Rep."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1016\/j.molcel.2018.05.009","article-title":"PABP Cooperates with the CCR4-NOT Complex to Promote mRNA Deadenylation and Block Precocious Decay","volume":"70","author":"Yi","year":"2018","journal-title":"Mol. Cell"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1261\/rna.032292.112","article-title":"Maturation of mammalian H\/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming","volume":"18","author":"Berndt","year":"2012","journal-title":"RNA"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1016\/j.celrep.2013.09.029","article-title":"Poly(A)-specific ribonuclease mediates 3\u2032-end trimming of Argonaute2-cleaved precursor microRNAs","volume":"5","author":"Yoda","year":"2013","journal-title":"Cell Rep."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"7521","DOI":"10.1093\/nar\/gkv669","article-title":"Destabilization of microRNAs in human cells by 3\u2032 deadenylation mediated by PARN and CUGBP1","volume":"43","author":"Katoh","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1016\/j.cell.2016.01.008","article-title":"Identification and Functional Analysis of the Pre-piRNA 3\u2032 Trimmer in Silkworms","volume":"164","author":"Izumi","year":"2016","journal-title":"Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1482","DOI":"10.1038\/ng.3423","article-title":"Poly(A)-specific ribonuclease (PARN) mediates 3\u2032-end maturation of the telomerase RNA component","volume":"47","author":"Moon","year":"2015","journal-title":"Nat. Genet."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"2232","DOI":"10.1016\/j.celrep.2015.10.075","article-title":"Human Telomerase RNA Processing and Quality Control","volume":"13","author":"Tseng","year":"2015","journal-title":"Cell Rep."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2244","DOI":"10.1016\/j.celrep.2015.11.003","article-title":"A Polyadenylation-Dependent 3\u2032 End Maturation Pathway Is Required for the Synthesis of the Human Telomerase RNA","volume":"13","author":"Nguyen","year":"2015","journal-title":"Cell Rep."},{"key":"ref_77","doi-asserted-by":"crossref","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":"ref_78","doi-asserted-by":"crossref","first-page":"12310","DOI":"10.1038\/ncomms12310","article-title":"The ATPase hCINAP regulates 18S rRNA processing and is essential for embryogenesis and tumour growth","volume":"7","author":"Bai","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1038\/emboj.2013.136","article-title":"A DIStinctively novel exoribonuclease that really likes U","volume":"32","author":"Gallouzi","year":"2013","journal-title":"EMBO J."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1811","DOI":"10.1093\/nar\/gkq1050","article-title":"5\u2032-end surveillance by Xrn2 acts as a shared mechanism for mammalian pre-rRNA maturation and decay","volume":"39","author":"Wang","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1128\/MCB.06019-11","article-title":"The evolutionarily conserved protein Las1 is required for pre-rRNA processing at both ends of ITS2","volume":"32","author":"Schillewaert","year":"2012","journal-title":"Mol. Cell. Biol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2564","DOI":"10.1093\/nar\/gkm082","article-title":"C1D and hMtr4p associate with the human exosome subunit PM\/Scl-100 and are involved in pre-rRNA processing","volume":"35","author":"Schilders","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1074\/mcp.M700510-MCP200","article-title":"ISG20L2, a novel vertebrate nucleolar exoribonuclease involved in ribosome biogenesis","volume":"7","author":"Coute","year":"2008","journal-title":"Mol. Cell. Proteomics"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1016\/S0021-9258(18)33294-0","article-title":"The nucleotide sequence of 8 S RNA bound to preribosomal RNA of Novikoff hepatoma. The 5\u2032-end of 8 S RNA is 5.8 S RNA","volume":"258","author":"Reddy","year":"1983","journal-title":"J. Biol. Chem."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2271","DOI":"10.1093\/nar\/27.11.2271","article-title":"Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences","volume":"27","author":"Michot","year":"1999","journal-title":"Nucleic Acids Res."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1038\/nsmb.1417","article-title":"Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing","volume":"15","author":"Ansel","year":"2008","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Fedoriw, A.M., Starmer, J., Yee, D., and Magnuson, T. (2012). Nucleolar association and transcriptional inhibition through 5S rDNA in mammals. PLoS Genet., 8.","DOI":"10.1371\/journal.pgen.1002468"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/S0092-8674(80)80048-1","article-title":"Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes","volume":"19","author":"Engelke","year":"1980","journal-title":"Cell"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"20857","DOI":"10.1016\/S0021-9258(17)31901-4","article-title":"Purification and characterization of human transcription factor IIIA","volume":"269","author":"Moorefield","year":"1994","journal-title":"J. Biol. Chem."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1016\/j.tig.2007.09.001","article-title":"The expanding RNA polymerase III transcriptome","volume":"23","author":"Dieci","year":"2007","journal-title":"Trends Genet."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.bbagrm.2012.09.010","article-title":"Identification of RNA polymerase III-transcribed genes in eukaryotic genomes","volume":"1829","author":"Dieci","year":"2013","journal-title":"Biochim. Biophys. Acta BBA\u2013Gene Regul. Mech."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/0092-8674(82)90099-X","article-title":"Precursor molecules of both human 5S ribosomal RNA and transfer RNAs are bound by a cellular protein reactive with anti-La Lupus antibodies","volume":"29","author":"Rinke","year":"1982","journal-title":"Cell"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1261\/rna.060723.117","article-title":"Characterization of the mammalian RNA exonuclease 5\/NEF-sp as a testis-specific nuclear 3\u2032 \u2192 5\u2032 exoribonuclease","volume":"23","author":"Silva","year":"2017","journal-title":"RNA"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1083\/jcb.106.3.545","article-title":"A 5S rRNA\/L5 complex is a precursor to ribosome assembly in mammalian cells","volume":"106","author":"Steitz","year":"1988","journal-title":"J. Cell Biol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"2580","DOI":"10.1101\/gad.1569307","article-title":"Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes","volume":"21","author":"Zhang","year":"2007","journal-title":"Genes Dev."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1126\/science.1226960","article-title":"Synchronizing Nuclear Import of Ribosomal Proteins with Ribosome Assembly","volume":"338","author":"Kressler","year":"2012","journal-title":"Science"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1101\/gad.260349.115","article-title":"Chaperoning 5S RNA assembly","volume":"29","author":"Madru","year":"2015","journal-title":"Genes Dev."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"6510","DOI":"10.1038\/ncomms7510","article-title":"Symportin 1 chaperones 5S RNP assembly during ribosome biogenesis by occupying an essential rRNA-binding site","volume":"6","author":"Kharde","year":"2015","journal-title":"Nat. Commun."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.celrep.2013.08.049","article-title":"The 5S RNP Couples p53 Homeostasis to Ribosome Biogenesis and Nucleolar Stress","volume":"5","author":"Sloan","year":"2013","journal-title":"Cell Rep."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"11390","DOI":"10.1038\/ncomms11390","article-title":"Involvement of human ribosomal proteins in nucleolar structure and p53-dependent nucleolar stress","volume":"7","author":"Nicolas","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1016\/0022-2836(73)90166-6","article-title":"Unusual metabolism of 5 S RNA in HeLa cells","volume":"73","author":"Leibowitz","year":"1973","journal-title":"J. Mol. Biol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.celrep.2013.05.045","article-title":"5S Ribosomal RNA Is an Essential Component of a Nascent Ribosomal Precursor Complex that Regulates the Hdm2-p53 Checkpoint","volume":"4","author":"Donati","year":"2013","journal-title":"Cell Rep."},{"key":"ref_103","doi-asserted-by":"crossref","unstructured":"Da Costa, L., Narla, A., and Mohandas, N. (2018). An update on the pathogenesis and diagnosis of Diamond\u2013Blackfan anemia. F1000Research, 7.","DOI":"10.12688\/f1000research.15542.1"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1053\/j.seminhematol.2011.02.005","article-title":"Diamond Blackfan anemia: Ribosomal proteins going rogue","volume":"48","author":"Ellis","year":"2011","journal-title":"Semin. Hematol."},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Ulirsch, J.C., Verboon, J.M., Kazerounian, S., Guo, M.H., Yuan, D., Ludwig, L.S., Handsaker, R.E., Abdulhay, N.J., Fiorini, C., and Genovese, G. (2018). The Genetic Landscape of Diamond\u2013Blackfan Anemia. bioRxiv, 365890.","DOI":"10.1016\/j.ajhg.2018.10.027"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"5913","DOI":"10.1093\/nar\/gkm626","article-title":"Molecular basis of Diamond\u2013Blackfan anemia: Structure and function analysis of RPS19","volume":"35","author":"Gregory","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"1720","DOI":"10.1093\/hmg\/ddm120","article-title":"Missense mutations associated with Diamond\u2013Blackfan anemia affect the assembly of ribosomal protein S19 into the ribosome","volume":"16","author":"Angelini","year":"2007","journal-title":"Hum. Mol. Genet."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.molcel.2005.09.005","article-title":"Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function","volume":"20","author":"Poll","year":"2005","journal-title":"Mol. Cell"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1016\/j.ajhg.2008.11.004","article-title":"Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond\u2013Blackfan anemia patients","volume":"83","author":"Gazda","year":"2008","journal-title":"Am. J. Hum. Genet."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1093\/hmg\/ddn015","article-title":"Mutation of ribosomal protein RPS24 in Diamond\u2013Blackfan anemia results in a ribosome biogenesis disorder","volume":"17","author":"Choesmel","year":"2008","journal-title":"Hum. Mol. Genet."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1111\/bjh.13880","article-title":"Ribosomal RNA analysis in the diagnosis of Diamond\u2013Blackfan Anaemia","volume":"172","author":"Quarello","year":"2016","journal-title":"Br. J. Haematol."},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Da Costa, L., O\u2019Donohue, M.-F., van Dooijeweert, B., Albrecht, K., Unal, S., Ramenghi, U., Leblanc, T., Dianzani, I., Tamary, H., and Bartels, M. (2017). Molecular approaches to diagnose Diamond\u2013Blackfan anemia: The EuroDBA experience. Eur. J. Med. Genet.","DOI":"10.1016\/j.ejmg.2017.10.017"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1002\/ajh.23807","article-title":"Exploiting pre-rRNA processing in Diamond Blackfan anemia gene discovery and diagnosis","volume":"89","author":"Farrar","year":"2014","journal-title":"Am. J. Hematol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"2240","DOI":"10.1002\/ajmg.a.36633","article-title":"Diamond\u2013Blackfan anemia with mandibulofacial dystostosis is heterogeneous, including the novel DBA genes TSR2 and RPS28","volume":"164","author":"Gripp","year":"2014","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"2439","DOI":"10.1172\/JCI63597","article-title":"Exome sequencing identifies GATA1 mutations resulting in Diamond\u2013Blackfan anemia","volume":"122","author":"Sankaran","year":"2012","journal-title":"J. Clin. Investig."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1111\/bjh.12919","article-title":"Recurrent GATA1 mutations in Diamond\u2013Blackfan anaemia","volume":"166","author":"Klar","year":"2014","journal-title":"Br. J. Haematol."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.1002\/pbc.24944","article-title":"Loss of GATA-1 full length as a cause of Diamond\u2013Blackfan anemia phenotype","volume":"61","author":"Parrella","year":"2014","journal-title":"Pediatr. Blood Cancer"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1038\/nm.3557","article-title":"Altered translation of GATA1 in Diamond\u2013Blackfan anemia","volume":"20","author":"Ludwig","year":"2014","journal-title":"Nat. Med."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.cell.2018.02.036","article-title":"Ribosome Levels Selectively Regulate Translation and Lineage Commitment in Human Hematopoiesis","volume":"173","author":"Khajuria","year":"2018","journal-title":"Cell"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1111\/bjh.13229","article-title":"Loss of function mutations in RPL27 and RPS27 identified by whole-exome sequencing in Diamond\u2013Blackfan anaemia","volume":"168","author":"Wang","year":"2015","journal-title":"Br. J. Haematol."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"1597","DOI":"10.1002\/pbc.25534","article-title":"Clinical and genomic heterogeneity of Diamond Blackfan anemia in the Russian Federation","volume":"62","author":"Smetanina","year":"2015","journal-title":"Pediatr. Blood Cancer"},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"515","DOI":"10.1007\/s12185-016-2151-7","article-title":"Diagnostic challenge of Diamond\u2013Blackfan anemia in mothers and children by whole-exome sequencing","volume":"105","author":"Ichimura","year":"2017","journal-title":"Int. J. Hematol."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1016\/j.ajhg.2009.12.015","article-title":"Ribosomal protein genes RPS10 and RPS26 are commonly mutated in Diamond\u2013Blackfan anemia","volume":"86","author":"Doherty","year":"2010","journal-title":"Am. J. Hum. Genet."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"e93","DOI":"10.3324\/haematol.2016.153932","article-title":"Exome sequencing identified RPS15A as a novel causative gene for Diamond\u2013Blackfan anemia","volume":"102","author":"Ikeda","year":"2017","journal-title":"Haematologica"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"1178","DOI":"10.1002\/humu.20608","article-title":"Ribosomal protein S17 gene (RPS17) is mutated in Diamond\u2013Blackfan anemia","volume":"28","author":"Cmejla","year":"2007","journal-title":"Hum. Mutat."},{"key":"ref_126","doi-asserted-by":"crossref","unstructured":"Song, M.-J., Yoo, E.-H., Lee, K.-O., Kim, G.-N., Kim, H.-J., Kim, S.-Y., and Kim, S.-H. (2009). A novel initiation codon mutation in the ribosomal protein S17 gene (RPS17) in a patient with Diamond\u2013Blackfan anemia. Pediatr. Blood Cancer, 54.","DOI":"10.1002\/pbc.22316"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"1293","DOI":"10.3324\/haematol.2009.020826","article-title":"Mutations in the ribosomal protein genes in Japanese patients with Diamond\u2013Blackfan anemia","volume":"95","author":"Konno","year":"2010","journal-title":"Haematologica"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"6943","DOI":"10.1182\/blood-2011-08-375170","article-title":"Ribosomal protein gene deletions in Diamond\u2013Blackfan anemia","volume":"118","author":"Farrar","year":"2011","journal-title":"Blood"},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1038\/5951","article-title":"The gene encoding ribosomal protein S19 is mutated in Diamond- Blackfan anaemia","volume":"21","author":"Draptchinskaia","year":"1999","journal-title":"Nat. Genet."},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"1110","DOI":"10.1086\/510020","article-title":"Ribosomal protein S24 gene is mutated in Diamond\u2013Blackfan anemia","volume":"79","author":"Gazda","year":"2006","journal-title":"Am. J. Hum. Genet."},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1182\/blood-2013-11-540278","article-title":"Whole-exome sequencing and functional studies identifyRPS29 as a novel gene mutated in multi-case Diamond\u2013Blackfan anemia families","volume":"124","author":"Mirabello","year":"2014","journal-title":"Blood"},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"1265","DOI":"10.1007\/s00439-013-1326-z","article-title":"Novel deletion of RPL15 identified by array-comparative genomic hybridization in Diamond\u2013Blackfan anemia","volume":"132","author":"Landowski","year":"2013","journal-title":"Hum. Genet."},{"key":"ref_133","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1136\/jmedgenet-2016-104346","article-title":"Novel and known ribosomal causes of Diamond\u2013Blackfan anaemia identified through comprehensive genomic characterisation","volume":"54","author":"Mirabello","year":"2017","journal-title":"J. Med. Genet."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1002\/humu.22081","article-title":"Frameshift mutation in p53 regulator RPL26 is associated with multiple physical abnormalities and a specific pre-ribosomal RNA processing defect in Diamond\u2013Blackfan anemia","volume":"33","author":"Gazda","year":"2012","journal-title":"Hum. Mutat."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"1582","DOI":"10.1182\/blood-2008-02-140012","article-title":"Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond\u2013Blackfan anemia","volume":"112","author":"Farrar","year":"2008","journal-title":"Blood"},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1038\/nature06494","article-title":"Identification of RPS14 as a 5q-syndrome gene by RNA interference screen","volume":"451","author":"Ebert","year":"2008","journal-title":"Nature"},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"976","DOI":"10.1126\/science.1234864","article-title":"Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia","volume":"340","author":"Bolze","year":"2013","journal-title":"Science"},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1016\/j.ajhg.2017.01.034","article-title":"A Ribosomopathy Reveals Decoding Defective Ribosomes Driving Human Dysmorphism","volume":"100","author":"Paolini","year":"2017","journal-title":"Am. J. Hum. Genet."},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1534\/genetics.114.168211","article-title":"A novel ribosomopathy caused by dysfunction of RPL10 disrupts neurodevelopment and causes X-linked microcephaly in humans","volume":"198","author":"Brooks","year":"2014","journal-title":"Genetics"},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"1908","DOI":"10.1002\/ajmg.a.37094","article-title":"RPL10 mutation segregating in a family with X-linked syndromic Intellectual Disability","volume":"167","author":"Thevenon","year":"2015","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.1002\/humu.22860","article-title":"A Novel Mutation in RPL10 (Ribosomal Protein L10) Causes X-Linked Intellectual Disability, Cerebellar Hypoplasia, and Spondylo-Epiphyseal Dysplasia","volume":"36","author":"Zanni","year":"2015","journal-title":"Hum. Mutat."},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1038\/sj.mp.4001883","article-title":"Mutations in the ribosomal protein gene RPL10 suggest a novel modulating disease mechanism for autism","volume":"11","author":"Klauck","year":"2006","journal-title":"Mol. Psychiatry"},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"1472","DOI":"10.1002\/ajmg.a.33977","article-title":"Mutation and expression analyses of the ribosomal protein gene RPL10 in an extended German sample of patients with autism spectrum disorder","volume":"155","author":"Chiocchetti","year":"2011","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.ejmg.2017.10.011","article-title":"A de novo mutation in RPL10 causes a rare X-linked ribosomopathy characterized by syndromic intellectual disability and epilepsy: A new case and review of the literature","volume":"61","author":"Bourque","year":"2018","journal-title":"Eur. J. Med. Genet."},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1038\/ng1062","article-title":"Mutations in SBDS are associated with Shwachman-Diamond syndrome","volume":"33","author":"Boocock","year":"2003","journal-title":"Nat. Genet."},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"4305","DOI":"10.1182\/blood-2011-06-353938","article-title":"Defective ribosome assembly in Shwachman-Diamond syndrome","volume":"118","author":"Wong","year":"2011","journal-title":"Blood"},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.ajhg.2016.05.002","article-title":"DNAJC21 Mutations Link a Cancer-Prone Bone Marrow Failure Syndrome to Corruption in 60S Ribosome Subunit Maturation","volume":"99","author":"Tummala","year":"2016","journal-title":"Am. J. Hum. Genet."},{"key":"ref_148","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1182\/blood-2016-08-735431","article-title":"Biallelic mutations in DNAJC21 cause Shwachman-Diamond syndrome","volume":"129","author":"Dhanraj","year":"2017","journal-title":"Blood"},{"key":"ref_149","doi-asserted-by":"crossref","unstructured":"Morini, J., Nacci, L., Babini, G., Cesaro, S., Valli, R., Ottolenghi, A., Nicolis, E., Pintani, E., Maserati, E., and Cipolli, M. (2018). Whole exome sequencing discloses heterozygous variants in the DNAJC21 and EFL1 genes but not in SRP54 in 6 out of 16 patients with Shwachman-Diamond Syndrome carrying biallelic SBDS mutations. Br. J. Haematol.","DOI":"10.1111\/bjh.15594"},{"key":"ref_150","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1136\/jmedgenet-2016-104366","article-title":"Mutations in EFL1, an SBDS partner, are associated with infantile pancytopenia, exocrine pancreatic insufficiency and skeletal anomalies in aShwachman-Diamond like syndrome","volume":"54","author":"Stepensky","year":"2017","journal-title":"J. Med. Genet."},{"key":"ref_151","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1016\/j.ajhg.2009.04.017","article-title":"Mutation of a Gene Essential for Ribosome Biogenesis, EMG1, Causes Bowen-Conradi Syndrome","volume":"84","author":"Armistead","year":"2009","journal-title":"Am. J. Hum. Genet."},{"key":"ref_152","doi-asserted-by":"crossref","first-page":"1526","DOI":"10.1093\/nar\/gkq931","article-title":"The Bowen-Conradi syndrome protein Nep1 (Emg1) has a dual role in eukaryotic ribosome biogenesis, as an essential assembly factor and in the methylation of \u03a81191 in yeast 18S rRNA","volume":"39","author":"Meyer","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_153","first-page":"5353","article-title":"Effects of the Bowen-Conradi syndrome mutation in EMG1 on its nuclear import, stability and nucleolar recruitment","volume":"25","author":"Warda","year":"2016","journal-title":"Hum. Mol. Genet."},{"key":"ref_154","doi-asserted-by":"crossref","first-page":"4798","DOI":"10.1093\/nar\/gkq185","article-title":"The C-terminus of Utp4, mutated in childhood cirrhosis, is essential for ribosome biogenesis","volume":"38","author":"Freed","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"ref_155","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1086\/344580","article-title":"A missense mutation (R565W) in cirhin (FLJ14728) in North American Indian childhood cirrhosis","volume":"71","author":"Chagnon","year":"2002","journal-title":"Am. J. Hum. Genet."},{"key":"ref_156","doi-asserted-by":"crossref","unstructured":"Marneros, A.G. (2013). BMS1 is mutated in aplasia cutis congenita. PLoS Genet., 9.","DOI":"10.1371\/journal.pgen.1003573"},{"key":"ref_157","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0092-8674(01)00205-7","article-title":"Mutations in the RNA component of RNase MRP cause a pleiotropic human disease, cartilage-hair hypoplasia","volume":"104","author":"Pelin","year":"2001","journal-title":"Cell"},{"key":"ref_158","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1038\/ng0598-32","article-title":"X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions","volume":"19","author":"Heiss","year":"1998","journal-title":"Nat. Genet."},{"key":"ref_159","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1086\/302446","article-title":"X-Linked Dyskeratosis Congenita Is Predominantly Caused by Missense Mutations in the DKC1 Gene","volume":"65","author":"Knight","year":"1999","journal-title":"Am. J. Hum. Genet."},{"key":"ref_160","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1093\/hmg\/ddm111","article-title":"Genetic heterogeneity in autosomal recessive dyskeratosis congenita with one subtype due to mutations in the telomerase-associated protein NOP10","volume":"16","author":"Walne","year":"2007","journal-title":"Hum. Mol. Genet."},{"key":"ref_161","doi-asserted-by":"crossref","first-page":"8073","DOI":"10.1073\/pnas.0800042105","article-title":"Mutations in the telomerase component NHP2 cause the premature ageing syndrome dyskeratosis congenita","volume":"105","author":"Vulliamy","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_162","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1136\/jmedgenet-2015-103292","article-title":"Bone marrow failure and developmental delay caused by mutations in poly(A)-specific ribonuclease (PARN)","volume":"52","author":"Dhanraj","year":"2015","journal-title":"J. Med. Genet."},{"key":"ref_163","doi-asserted-by":"crossref","first-page":"2151","DOI":"10.1172\/JCI78963","article-title":"Poly(A)-specific ribonuclease deficiency impacts telomere biology and causes dyskeratosis congenita","volume":"125","author":"Tummala","year":"2015","journal-title":"J. Clin. Investig."},{"key":"ref_164","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1038\/ejhg.2012.2","article-title":"Gross deletions in TCOF1 are a cause of Treacher\u2013Collins\u2013Franceschetti syndrome","volume":"20","author":"Bowman","year":"2012","journal-title":"Eur. J. Hum. Genet."},{"key":"ref_165","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1038\/ng.724","article-title":"Mutations in genes encoding subunits of RNA polymerases I and III cause Treacher Collins syndrome","volume":"43","author":"Dauwerse","year":"2011","journal-title":"Nat. Genet."},{"key":"ref_166","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/j.ijporl.2014.03.006","article-title":"Treacher Collins Syndrome: The genetics of a craniofacial disease","volume":"78","author":"Kadakia","year":"2014","journal-title":"Int. J. Pediatr. Otorhinolaryngol."},{"key":"ref_167","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1038\/gim.2014.12","article-title":"Autosomal recessive POLR1D mutation with decrease of TCOF1 mRNA is responsible for Treacher Collins syndrome","volume":"16","author":"Schaefer","year":"2014","journal-title":"Genet. Med."},{"key":"ref_168","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1016\/j.ajhg.2015.03.011","article-title":"Acrofacial Dysostosis, Cincinnati Type, a Mandibulofacial Dysostosis Syndrome with Limb Anomalies, Is Caused by POLR1A Dysfunction","volume":"96","author":"Weaver","year":"2015","journal-title":"Am. J. Hum. Genet."},{"key":"ref_169","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1038\/ejhg.2016.183","article-title":"Severe neurodegenerative disease in brothers with homozygous mutation in POLR1A","volume":"25","author":"Kara","year":"2017","journal-title":"Eur. J. Hum. Genet. EJHG"},{"key":"ref_170","doi-asserted-by":"crossref","unstructured":"Sinturel, F., and Gachon, F. (2017). Diurnal liver mass is associated with ribosome biogenesis. Oncotarget, 8.","DOI":"10.18632\/oncotarget.22255"},{"key":"ref_171","doi-asserted-by":"crossref","unstructured":"Robson, A., Owens, N.D.L., Baserga, S.J., Khokha, M.K., and Griffin, J.N. (2016). Expression of ribosomopathy genes during Xenopus tropicalis embryogenesis. BMC Dev. Biol., 16.","DOI":"10.1186\/s12861-016-0138-5"},{"key":"ref_172","doi-asserted-by":"crossref","first-page":"eaan2755","DOI":"10.1126\/science.aan2755","article-title":"Ribosomopathies: There\u2019s strength in numbers","volume":"358","author":"Mills","year":"2017","journal-title":"Science"},{"key":"ref_173","doi-asserted-by":"crossref","first-page":"3420","DOI":"10.1016\/S0021-9258(19)43961-6","article-title":"Regulation of synthesis of non-globin proteins in cell-free extracts of rabbit reticulocytes","volume":"248","author":"Lodish","year":"1973","journal-title":"J. Biol. Chem."},{"key":"ref_174","doi-asserted-by":"crossref","unstructured":"Van de Waterbeemd, M., Tamara, S., Fort, K.L., Damoc, E., Franc, V., Bieri, P., Itten, M., Makarov, A., Ban, N., and Heck, A.J.R. (2018). Dissecting ribosomal particles throughout the kingdoms of life using advanced hybrid mass spectrometry methods. Nat. Commun., 9.","DOI":"10.1038\/s41467-018-04853-x"},{"key":"ref_175","doi-asserted-by":"crossref","first-page":"eaao0665","DOI":"10.1126\/sciadv.aao0665","article-title":"Variant ribosomal RNA alleles are conserved and exhibit tissue-specific expression","volume":"4","author":"Parks","year":"2018","journal-title":"Sci. Adv."},{"key":"ref_176","doi-asserted-by":"crossref","first-page":"1588","DOI":"10.1093\/molbev\/msy021","article-title":"Revising the Structural Diversity of Ribosomal Proteins across the Three Domains of Life","volume":"35","author":"Melnikov","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_177","doi-asserted-by":"crossref","unstructured":"Sharma, S., Marchand, V., Motorin, Y., and Lafontaine, D.L.J. (2017). Identification of sites of 2\u2032-O-methylation vulnerability in human ribosomal RNAs by systematic mapping. Sci. Rep., 7.","DOI":"10.1038\/s41598-017-09734-9"},{"key":"ref_178","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.cell.2011.03.028","article-title":"Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning","volume":"145","author":"Kondrashov","year":"2011","journal-title":"Cell"},{"key":"ref_179","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/j.molcel.2018.07.018","article-title":"The Discovery of Ribosome Heterogeneity and Its Implications for Gene Regulation and Organismal Life","volume":"71","author":"Genuth","year":"2018","journal-title":"Mol. Cell"},{"key":"ref_180","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1016\/j.tibs.2017.05.005","article-title":"A Puzzle of Life: Crafting Ribosomal Subunits","volume":"42","author":"Kressler","year":"2017","journal-title":"Trends Biochem. Sci."},{"key":"ref_181","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1038\/nsmb.3454","article-title":"Eukaryotic ribosome assembly, transport and quality control","volume":"24","author":"Hurt","year":"2017","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_182","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1016\/j.tibs.2009.12.006","article-title":"A \u2018garbage can\u2019 for ribosomes: how eukaryotes degrade their ribosomes","volume":"35","author":"Lafontaine","year":"2010","journal-title":"Trends Biochem. Sci."},{"key":"ref_183","doi-asserted-by":"crossref","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":"ref_184","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1016\/j.molcel.2009.04.017","article-title":"A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay","volume":"34","author":"Cole","year":"2009","journal-title":"Mol. Cell"},{"key":"ref_185","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1083\/jcb.201311103","article-title":"Protecting the proteome: Eukaryotic cotranslational quality control pathways","volume":"204","author":"Bennett","year":"2014","journal-title":"J. Cell Biol."},{"key":"ref_186","doi-asserted-by":"crossref","first-page":"2579","DOI":"10.1038\/emboj.2012.85","article-title":"40S subunit dissociation and proteasome-dependent RNA degradation in nonfunctional 25S rRNA decay","volume":"31","author":"Fujii","year":"2012","journal-title":"EMBO J."},{"key":"ref_187","doi-asserted-by":"crossref","first-page":"1107","DOI":"10.1038\/nsmb.3495","article-title":"Preribosomes escaping from the nucleus are caught during translation by cytoplasmic quality control","volume":"24","author":"Sarkar","year":"2017","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_188","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1038\/emboj.2009.307","article-title":"Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae","volume":"29","author":"Soudet","year":"2010","journal-title":"EMBO J."},{"key":"ref_189","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1080\/15476286.2015.1058477","article-title":"Immature large ribosomal subunits containing the 7S pre-rRNA can engage in translation in Saccharomyces cerevisiae","volume":"12","author":"Kressler","year":"2015","journal-title":"RNA Biol."},{"key":"ref_190","doi-asserted-by":"crossref","first-page":"10824","DOI":"10.1093\/nar\/gkx734","article-title":"The Rio1p ATPase hinders premature entry into translation of late pre-40S pre-ribosomal particles","volume":"45","author":"Joret","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_191","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1038\/nsmb.3442","article-title":"Rps26 directs mRNA-specific translation by recognition of Kozak sequence elements","volume":"24","author":"Ferretti","year":"2017","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_192","doi-asserted-by":"crossref","first-page":"7884","DOI":"10.1093\/nar\/gkw482","article-title":"Profiling of 2\u2032-O-Me in human rRNA reveals a subset of fractionally modified positions and provides evidence for ribosome heterogeneity","volume":"44","author":"Krogh","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"ref_193","doi-asserted-by":"crossref","first-page":"12934","DOI":"10.1073\/pnas.1707674114","article-title":"Evidence for rRNA 2\u2032-O-methylation plasticity: Control of intrinsic translational capabilities of human ribosomes","volume":"114","author":"Erales","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_194","doi-asserted-by":"crossref","unstructured":"Bundred, J.R., Hendrix, E., and Coleman, M.L. (2018). The emerging roles of ribosomal histidyl hydroxylases in cell biology, physiology and disease. Cell. Mol. Life Sci.","DOI":"10.1007\/s00018-018-2903-z"},{"key":"ref_195","doi-asserted-by":"crossref","first-page":"12770","DOI":"10.1074\/jbc.RA118.002890","article-title":"Identification of Rpl29 as a major substrate of the lysine methyltransferase Set7\/9","volume":"293","author":"Hamidi","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_196","doi-asserted-by":"crossref","unstructured":"Loenarz, C., Sekirnik, R., Thalhammer, A., Ge, W., Spivakovsky, E., Mackeen, M.M., McDonough, M., Cockman, M.E., Kessler, B., and Ratcliffe, P. (2014). Hydroxylation of the eukaryotic ribosomal decoding center affects translational accuracy. Proc. Natl. Acad. Sci. USA, 111.","DOI":"10.1073\/pnas.1311750111"},{"key":"ref_197","doi-asserted-by":"crossref","first-page":"2567","DOI":"10.1182\/blood-2010-07-295238","article-title":"Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells","volume":"117","author":"Dutt","year":"2011","journal-title":"Blood"},{"key":"ref_198","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1038\/nm1725","article-title":"Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function","volume":"14","author":"Jones","year":"2008","journal-title":"Nat. Med."},{"key":"ref_199","doi-asserted-by":"crossref","first-page":"20467","DOI":"10.1073\/pnas.1218535109","article-title":"Mutual protection of ribosomal proteins L5 and L11 from degradation is essential for p53 activation upon ribosomal biogenesis stress","volume":"109","author":"Bursac","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_200","doi-asserted-by":"crossref","first-page":"3332","DOI":"10.1038\/sj.emboj.7601776","article-title":"Inhibition of c-Myc activity by ribosomal protein L11","volume":"26","author":"Dai","year":"2007","journal-title":"EMBO J."},{"key":"ref_201","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1261\/rna.064626.117","article-title":"The RNA exosome and RNA exosome-linked disease","volume":"24","author":"Morton","year":"2018","journal-title":"RNA"}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/8\/4\/123\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:26:01Z","timestamp":1760196361000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/8\/4\/123"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,10,24]]},"references-count":201,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2018,12]]}},"alternative-id":["biom8040123"],"URL":"https:\/\/doi.org\/10.3390\/biom8040123","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,10,24]]}}}