A Protein Inventory of Human Ribosome Biogenesis Reveals an Essential Function of Exportin 5 in 60S Subunit Export

A systematic search for human ribosome biogenesis factors shows conservation of many aspects of eukaryotic ribosome synthesis with the well-studied process in yeast and identifies an export route of 60S subunits that is specific for higher eukaryotes.

[1]  B. Sollner-Webb,et al.  Nucleotide sequence determining the first cleavage site in the processing of mouse precursor rRNA. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Sander Granneman,et al.  Ribosome biogenesis: of knobs and RNA processing. , 2004, Experimental cell research.

[3]  Arlen W. Johnson,et al.  Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast. , 2007, Molecular biology of the cell.

[4]  U. Kutay,et al.  Exportin‐5‐mediated nuclear export of eukaryotic elongation factor 1A and tRNA , 2002, The EMBO journal.

[5]  E. Petfalski,et al.  The path from nucleolar 90S to cytoplasmic 40S pre‐ribosomes , 2003, The EMBO journal.

[6]  Tom Misteli,et al.  Potential Roles for Ubiquitin and the Proteasome during Ribosome Biogenesis , 2006, Molecular and Cellular Biology.

[7]  Y. Iwakura,et al.  Crucial Role of Bysl in Mammalian Preimplantation Development as an Integral Factor for 40S Ribosome Biogenesis , 2007, Molecular and Cellular Biology.

[8]  P. Silver,et al.  Factors affecting nuclear export of the 60S ribosomal subunit in vivo. , 2000, Molecular biology of the cell.

[9]  Brendan J. Frey,et al.  A Panoramic View of Yeast Noncoding RNA Processing , 2003, Cell.

[10]  L. Duret,et al.  ISG20L2, a Novel Vertebrate Nucleolar Exoribonuclease Involved in Ribosome Biogenesis*S , 2008, Molecular & Cellular Proteomics.

[11]  J. Ladenson,et al.  The role of human ribosomal proteins in the maturation of rRNA and ribosome production. , 2008, RNA.

[12]  U. Kutay,et al.  Nuclear export and cytoplasmic maturation of ribosomal subunits , 2007, FEBS letters.

[13]  Yanping Zhang,et al.  Signaling to p53: ribosomal proteins find their way. , 2009, Cancer cell.

[14]  K. Miller,et al.  Transcription of mouse rRNA genes by RNA polymerase I: In vitro and in vivo initiation and processing sites , 1981, Cell.

[15]  K. Czaplinski,et al.  Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. , 2004, RNA.

[16]  R. Savkur,et al.  Preferential cleavage in pre-ribosomal RNA byprotein B23 endoribonuclease. , 1998, Nucleic acids research.

[17]  Arlen W. Johnson,et al.  Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates , 2003, The EMBO journal.

[18]  B. Ebert,et al.  Ribosomopathies: human disorders of ribosome dysfunction. , 2010, Blood.

[19]  B. McStay,et al.  A Novel Small-Subunit Processome Assembly Intermediate That Contains the U3 snoRNP, Nucleolin, RRP5, and DBP4 , 2009, Molecular and Cellular Biology.

[20]  U. Kutay,et al.  Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway , 2003, Journal of Cell Science.

[21]  L. Brill,et al.  The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries. , 2009, Molecular cell.

[22]  U. Kutay,et al.  Nuclear Export of MicroRNA Precursors , 2004, Science.

[23]  F. Bischoff,et al.  Identification of Two Novel RanGTP-binding Proteins Belonging to the Importin β Superfamily* , 2000, The Journal of Biological Chemistry.

[24]  David Tollervey,et al.  Ribosome synthesis meets the cell cycle. , 2004, Current opinion in microbiology.

[25]  B. McStay,et al.  Recruitment of factors linking transcription and processing of pre-rRNA to NOR chromatin is UBF-dependent and occurs independent of transcription in human cells. , 2007, Genes & development.

[26]  Ning Li,et al.  Human 1A6/DRIM, the homolog of yeast Utp20, functions in the 18S rRNA processing. , 2007, Biochimica et biophysica acta.

[27]  P. Pandolfi,et al.  Nucleophosmin Serves as a Rate-Limiting Nuclear Export Chaperone for the Mammalian Ribosome , 2008, Molecular and Cellular Biology.

[28]  E. Hurt,et al.  Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. , 2007, Molecular cell.

[29]  G. Culver,et al.  Deconstructing ribosome construction. , 2009, Trends in biochemical sciences.

[30]  Ulrike Kutay,et al.  Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2 , 2009, The Journal of cell biology.

[31]  D. Tollervey,et al.  A Novel In Vivo Assay Reveals Inhibition of Ribosomal Nuclear Export in Ran-Cycle and Nucleoporin Mutants , 1999, The Journal of cell biology.

[32]  Valérie Choesmel,et al.  Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells , 2005, The EMBO journal.

[33]  Anne E Carpenter,et al.  CellProfiler: image analysis software for identifying and quantifying cell phenotypes , 2006, Genome Biology.

[34]  J. Steitz,et al.  Sno Storm in the Nucleolus: New Roles for Myriad Small RNPs , 1997, Cell.

[35]  Insuk Lee,et al.  Rational Extension of the Ribosome Biogenesis Pathway Using Network-Guided Genetics , 2009, PLoS biology.

[36]  U. Kutay,et al.  Transport between the cell nucleus and the cytoplasm. , 1999, Annual review of cell and developmental biology.

[37]  E. Kremmer,et al.  Interdependence of Pes1, Bop1, and WDR12 Controls Nucleolar Localization and Assembly of the PeBoW Complex Required for Maturation of the 60S Ribosomal Subunit , 2007, Molecular and Cellular Biology.

[38]  M. Nomura,et al.  Assembly Mapping of 30S Ribosomal Proteins from E. coli , 1970, Nature.

[39]  E. Kremmer,et al.  The BRCT domain of mammalian Pes1 is crucial for nucleolar localization and rRNA processing , 2006, Nucleic acids research.

[40]  Blanche Schwappach,et al.  Exp5 exports eEF1A via tRNA from nuclei and synergizes with other transport pathways to confine translation to the cytoplasm , 2002, The EMBO journal.

[41]  Anthony K. L. Leung,et al.  Nucleolar proteome dynamics , 2005, Nature.

[42]  L. Terracciano,et al.  Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. , 2000, Science.

[43]  D. Tollervey,et al.  A Surfeit of Factors: Why is Ribosome Assembly So Much More Complicated in Eukaryotes than Bacteria? , 2004, RNA biology.

[44]  J. Steitz,et al.  Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte , 1993, Cell.

[45]  J. Shabanowitz,et al.  A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis , 2002, Nature.

[46]  A. Pasquinelli,et al.  Reverse 5' caps in RNAs made in vitro by phage RNA polymerases. , 1995, RNA.

[47]  M. Kaczanowska,et al.  Ribosome Biogenesis and the Translation Process in Escherichia coli , 2007, Microbiology and Molecular Biology Reviews.

[48]  T. Kiss,et al.  Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. , 2006, Cold Spring Harbor symposia on quantitative biology.

[49]  S. Baserga,et al.  M phase phosphoprotein 10 is a human U3 small nucleolar ribonucleoprotein component. , 1998, Molecular biology of the cell.

[50]  S. Baserga,et al.  When ribosomes go bad: diseases of ribosome biogenesis. , 2010, Molecular bioSystems.

[51]  I. Grummt Different epigenetic layers engage in complex crosstalk to define the epigenetic state of mammalian rRNA genes. , 2007, Human molecular genetics.

[52]  K. Mizuta,et al.  Ebp2p, the Yeast Homolog of Epstein-Barr Virus Nuclear Antigen 1-binding Protein 2, Interacts with Factors of Both the 60 S and the 40 S Ribosomal Subunit Assembly* , 2004, Journal of Biological Chemistry.

[53]  Z. Strezoska,et al.  Bop1 Is a Mouse WD40 Repeat Nucleolar Protein Involved in 28S and 5.8S rRNA Processing and 60S Ribosome Biogenesis , 2000, Molecular and Cellular Biology.

[54]  E. Hurt,et al.  A versatile interaction platform on the Mex67–Mtr2 receptor creates an overlap between mRNA and ribosome export , 2008, The EMBO journal.

[55]  D. Tollervey,et al.  Nuclear Export of 60S Ribosomal Subunits Depends on Xpo1p and Requires a Nuclear Export Sequence-Containing Factor, Nmd3p, That Associates with the Large Subunit Protein Rpl10p , 2001, Molecular and Cellular Biology.

[56]  Matthias Mann,et al.  Analysis of Nucleolar Protein Dynamics Reveals the Nuclear Degradation of Ribosomal Proteins , 2007, Current Biology.

[57]  Pierre-Emmanuel Gleizes,et al.  Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. , 2005, Molecular cell.

[58]  P. Silver,et al.  Nuclear export of the small ribosomal subunit requires the ran-GTPase cycle and certain nucleoporins. , 1999, Genes & development.

[59]  S. Napthine,et al.  Development of a tRNA-dependent in vitro translation system. , 2001, RNA.

[60]  B. Dujon,et al.  Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes , 2008, Microbiology and Molecular Biology Reviews.

[61]  David Tollervey,et al.  60S pre‐ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm , 2002, The EMBO journal.

[62]  B. Cullen,et al.  Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. , 2003, Genes & development.

[63]  Peter Gregor,et al.  NOPdb: Nucleolar Proteome Database—2008 update , 2008, Nucleic Acids Res..

[64]  J. Williamson,et al.  A complex assembly landscape for the 30S ribosomal subunit. , 2009, Annual review of biophysics.

[65]  R. Aebersold,et al.  An integrated workflow for charting the human interaction proteome: insights into the PP2A system , 2009, Molecular systems biology.

[66]  P. Bouvet,et al.  Nucleolin functions in the first step of ribosomal RNA processing , 1998, The EMBO journal.

[67]  J. Soudet,et al.  The post-transcriptional steps of eukaryotic ribosome biogenesis , 2008, Cellular and Molecular Life Sciences.

[68]  Ed Hurt,et al.  Pre-ribosomes on the road from the nucleolus to the cytoplasm. , 2003, Trends in cell biology.

[69]  Francesco Piazza,et al.  Dyskeratosis Congenita and Cancer in Mice Deficient in Ribosomal RNA Modification , 2003, Science.

[70]  Arlen W. Johnson,et al.  Nmd3p Is a Crm1p-Dependent Adapter Protein for Nuclear Export of the Large Ribosomal Subunit , 2000, The Journal of cell biology.

[71]  D. G. Pestov,et al.  Mammalian DEAD Box Protein Ddx51 Acts in 3′ End Maturation of 28S rRNA by Promoting the Release of U8 snoRNA , 2010, Molecular and Cellular Biology.

[72]  F. Bischoff,et al.  Identification of two novel RanGTP-binding proteins belonging to the importin beta superfamily. , 2000, The Journal of biological chemistry.

[73]  E. Kremmer,et al.  Mammalian WDR12 is a novel member of the Pes1–Bop1 complex and is required for ribosome biogenesis and cell proliferation , 2005, The Journal of cell biology.

[74]  Ed Hurt,et al.  Nuclear export of ribosomal 60S subunits by the general mRNA export receptor Mex67-Mtr2. , 2007, Molecular cell.

[75]  M. Dai,et al.  Nucleophosmin Is Essential for Ribosomal Protein L5 Nuclear Export , 2006, Molecular and Cellular Biology.

[76]  M. Dai,et al.  Crosstalk between c‐Myc and ribosome in ribosomal biogenesis and cancer , 2008, Journal of cellular biochemistry.

[77]  G. Lipowsky,et al.  Identification of a tRNA-specific nuclear export receptor. , 1998, Molecular cell.

[78]  Bernhard Kuster,et al.  90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. , 2002, Molecular cell.

[79]  Christopher H Wade,et al.  The budding yeast rRNA and ribosome biosynthesis (RRB) regulon contains over 200 genes , 2006, Yeast.

[80]  U. A. Ørom,et al.  MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. , 2008, Molecular cell.

[81]  F. Dohme,et al.  Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[82]  V. G. Panse,et al.  Maturation of eukaryotic ribosomes: acquisition of functionality. , 2010, Trends in biochemical sciences.