Maturation of eukaryotic ribosomes: acquisition of functionality

Trends in Biochemical Sciences

Volumn 35, Issue 5, 2010, Pages 260-266

  Panse, Vikram Govind ^a   Johnson, Arlen W ^b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; RIBOSOME RNA;

BACTERIAL CELL; CYTOPLASM; EUKARYOTIC CELL; FUNGAL CELL; LARGE RIBOSOMAL SUBUNIT; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; REVIEW; RIBOSOME; RNA PROCESSING; RNA TRANSCRIPTION; SMALL RIBOSOMAL SUBUNIT;

BIOLOGICAL TRANSPORT; CELL NUCLEUS; CYTOPLASM; EUKARYOTA; EUKARYOTIC CELLS; RIBOSOMAL PROTEINS; RIBOSOMES; TRANS-ACTIVATORS;

EUKARYOTA;

EID: 77952583684     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2010.01.001     Document Type: Review

References (69)

1. Bashan A., Yonath A. Correlating ribosome function with high-resolution structures. Trends Microbiol. 2008, 16:326-335.
2. Schmeing T.M., Ramakrishnan V. What recent ribosome structures have revealed about the mechanism of translation. Nature 2009, 461:1234-1242.
3. Steitz T.A. A structural understanding of the dynamic ribosome machine. Nat. Rev. Mol. Cell Biol. 2008, 9:242-253.
4. Trapman J., et al. Ribosomal precursor particles from yeast. Exp. Cell Res. 1975, 90:95-104.
5. Udem S.A., Warner J.R. The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J. Biol. Chem. 1973, 248:1412-1416.
6. Venema J., Tollervey D. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 1999, 33:261-311.
7. Kressler D., et al. Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol. Cell Biol. 1999, 19:7897-7912.
8. Tschochner H., Hurt E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 2003, 13:255-263.
9. Zemp I., Kutay U. Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 2007, 581:2783-2793.
10. Dragon F., et al. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 2002, 417:967-970.
11. Grandi P., et al. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 2002, 10:105-115.
12. Gleizes P.E., et al. Ultrastructural localization of rRNA shows defective nuclear export of preribosomes in mutants of the Nup82p complex. J. Cell Biol. 2001, 155:923-936.
13. Fromont-Racine M., et al. Ribosome assembly in eukaryotes. Gene 2003, 313:17-42.
14. Kressler D., et al. Driving Ribosome Assembly. Biochim. Biophys. Acta 2009, 10.1016/j.bbamcr.2009.10.009.
15. Strunk B.S., Karbstein K. Powering through ribosome assembly. RNA 2009, 15:2083-2104.
16. Ulbrich C., et al. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 2009, 138:911-922.
17. Henras A.K., et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol. Life Sci. 2008, 65:2334-2359.
18. Staley J.P., Woolford J.L. Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines. Curr. Opin. Cell Biol. 2009, 21:109-118.
19. Hurt E., et al. A novel in vivo assay reveals inhibition of ribosomal nuclear export in Ran-cycle and nucleoporin mutants. J. Cell Biol. 1999, 144:389-401.
20. Milkereit P., et al. A noc complex specifically involved in the formation and nuclear export of ribosomal 40 S subunits. J. Biol. Chem. 2003, 278:4072-4081.
21. Stage-Zimmermann T., et al. Factors affecting nuclear export of the 60S ribosomal subunit in vivo. Mol. Biol. Cell 2000, 11:3777-3789.
22. Moy T.I., Silver P.A. Nuclear export of the small ribosomal subunit requires the ran-GTPase cycle and certain nucleoporins. Genes Dev. 1999, 13:2118-2133.
23. Moy T.I., Silver P.A. Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci. 2002, 115:2985-2995.
24. Seiser R.M., et al. Ltv1 is required for efficient nuclear export of the ribosomal small subunit in Saccharomyces cerevisiae. Genetics 2006, 174:679-691.
25. Zemp I., et al. Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 2009, 185:1167-1180.
26. Ribbeck K., Gorlich D. The permeability barrier of nuclear pore complexes appears to operate via hydrophobic exclusion. EMBO J. 2002, 21:2664-2671.
27. Yao W., et al. Nuclear export of ribosomal 60S subunits by the general mRNA export receptor Mex67-Mtr2. Mol. Cell 2007, 26:51-62.
28. Bradatsch B., et al. Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. Mol. Cell 2007, 27:767-779.
29. Hung N.J., et al. Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast. Mol. Biol. Cell 2008, 19:735-744.
30. Pertschy B., et al. Cytoplasmic recycling of 60S preribosomal factors depends on the AAA protein Drg1. Mol. Cell Biol. 2007, 27:6581-6592.
31. Lupas A.N., Martin J. AAA proteins. Curr. Opin. Struct. Biol. 2002, 12:746-753.
32. Saveanu C., et al. Sequential protein association with nascent 60S ribosomal particles. Mol. Cell Biol. 2003, 23:4449-4460.
33. Lebreton A., et al. A functional network involved in the recycling of nucleocytoplasmic pre-60S factors. J. Cell Biol. 2006, 173:349-360.
34. Hung N.J., Johnson A.W. Nuclear recycling of the pre-60S ribosomal subunit-associated factor Arx1 depends on Rei1 in Saccharomyces cerevisiae. Mol. Cell Biol. 2006, 26:3718-3727.
35. Demoinet E., et al. The Hsp40 chaperone Jjj1 is required for the nucleo-cytoplasmic recycling of preribosomal factors in Saccharomyces cerevisiae. RNA 2007, 13:1570-1581.
36. Meyer A.E., et al. The specialized cytosolic J-protein, Jjj1, functions in 60S ribosomal subunit biogenesis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1558-1563.
37. Parnell K.M., Bass B.L. Functional redundancy of yeast proteins Reh1 and Rei1 in cytoplasmic 60S subunit maturation. Mol. Cell Biol. 2009, 29:4014-4023.
38. Bradshaw R.A., et al. N-terminal processing: the methionine aminopeptidase and N alpha-acetyl transferase families. Trends Biochem. Sci. 1998, 23:263-267.
39. Beckmann R., et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 2001, 107:361-372.
40. Russell D.W., Spremulli L.L. Purification and characterization of a ribosome dissociation factor (eukaryotic initiation factor 6) from wheat germ. J. Biol. Chem. 1979, 254:8796-8800.
41. Valenzuela D.M., et al. Eukaryotic ribosomal subunit anti-association activity of calf liver is contained in a single polypeptide chain protein of Mr = 25,500 (eukaryotic initiation factor 6). J. Biol. Chem. 1982, 257:7712-7719.
42. Benelli D., et al. Function and ribosomal localization of aIF6, a translational regulator shared by archaea and eukarya. Nucleic Acids Res. 2009, 37:256-267.
43. Becam A.M., et al. Ria1p (Ynl163c), a protein similar to elongation factors 2, is involved in the biogenesis of the 60S subunit of the ribosome in Saccharomyces cerevisiae. Mol. Genet. Genomics 2001, 266:454-462.
44. Senger B., et al. The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 2001, 8:1363-1373.
45. Menne T.F., et al. The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat. Genet. 2007, 39:486-495.
46. Hedges J., et al. Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J. 2005, 24:567-579.
47. Karl T., et al. GRC5 and NMD3 function in translational control of gene expression and interact genetically. Curr. Genet. 1999, 34:419-429.
48. Kemmler S., et al. Yvh1 is required for a late maturation step in the 60S biogenesis pathway. J. Cell Biol. 2009, 186:863-880.
49. Lo K.Y., et al. Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0. J. Cell Biol. 2009, 186:849-862.
50. Gonzalo P., Reboud J.P. The puzzling lateral flexible stalk of the ribosome. Biol. Cell 2003, 95:179-193.
51. Rodriguez-Mateos M., et al. Role and dynamics of the ribosomal protein P0 and its related trans-acting factor Mrt4 during ribosome assembly in Saccharomyces cerevisiae. Nucleic Acids Res. 2009, 37:7519-7532.
52. Pertschy B., et al. RNA helicase Prp43 and its co-factor Pfa1 promote 20S to 18S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem. 2009, 284:35079-35091.
53. Schafer T., et al. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J. 2003, 22:1370-1380.
54. Schafer T., et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 2006, 441:651-655.
55. Rouquette J., et al. Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J. 2005, 24:2862-2872.
56. Lamanna A.C., Karbstein K. Nob1 binds the single-stranded cleavage site D at the 3'-end of 18S rRNA with its PIN domain. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14259-14264.
57. Geerlings T.H., et al. Rio2p, an evolutionarily conserved, low abundant protein kinase essential for processing of 20 S Pre-rRNA in Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278:22537-22545.
58. Vanrobays E., et al. Processing of 20S pre-rRNA to 18S ribosomal RNA in yeast requires Rrp10p, an essential non-ribosomal cytoplasmic protein. EMBO J. 2001, 20:4204-4213.
59. Soudet J., et al. Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae. EMBO J. 2009, 10.1038/emboj.2009.307.
60. Xu Z., et al. A conserved rRNA methyltransferase regulates ribosome biogenesis. Nat. Struct. Mol. Biol. 2008, 15:534-536.
61. Johnson A.W., et al. Nuclear export of ribosomal subunits. Trends Biochem. Sci. 2002, 27:580-585.
62. Ho J.H.-N., et al. Nascent 60S subunits enter the free pool bound by Nmd3p. RNA 2000, 6:1625-1634.
63. Kallstrom G., et al. The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localied to the nucleus and cytoplasm, respectively. Mol. Cell Biol. 2003, 23:4344-4355.
64. Britton R.A. Role of GTPases in bacterial ribosome assembly. Annu. Rev. Microbiol. 2009, 63:155-176.
65. Hage A.E., Tollervey D. A surfeit of factors: why is ribosome assembly so much more complicated in eukaryotes than bacteria? RNA Biol. 2004, 1:10-15.
66. Connolly K., Culver G. Deconstructing ribosome construction. Trends Biochem. Sci. 2009, 34:256-263.
67. Ansel K.M., et al. Mouse Eri1 interacts with the ribosome and catalyzes 5.8S rRNA processing. Nat. Struct. Mol. Biol. 2008, 15:523-530.
68. Gabel H.W., Ruvkun G. The exonuclease ERI-1 has a conserved dual role in 5.8S rRNA processing and RNAi. Nat. Struct. Mol. Biol. 2008, 15:531-533.
69. Thomson E., Tollervey D. The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol. Cell Biol. 2009, 10.1128/MCB.01359-09.