A 'garbage can' for ribosomes: how eukaryotes degrade their ribosomes

Trends in Biochemical Sciences

Volumn 35, Issue 5, 2010, Pages 267-277

  Lafontaine, Denis L J ^a,b  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b Academie Wallonie Bruxelles   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME RNA; TRANS ACTING FACTOR; VIRUS RNA;

AUTOPHAGY; BACTERIAL GENETICS; CELL ORGANELLE; EXOSOME; GENE MUTATION; HUMAN; LARGE RIBOSOMAL SUBUNIT; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NUCLEOLUS; PRIORITY JOURNAL; REVIEW; RIBOSOME; RNA DEGRADATION; RNA SEQUENCE; SMALL RIBOSOMAL SUBUNIT; UBIQUITINATION;

BASE SEQUENCE; EUKARYOTA; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, RIBOSOMAL;

EUKARYOTA;

EID: 77952580619     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2009.12.006     Document Type: Review

References (81)

1. Steitz T.A. A structural understanding of the dynamic ribosome machine. Nat. Rev. Mol. Cell Biol. 2008, 9:242-253.
2. Henras A.K., et al. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 2008, 65:2334-2359.
3. Strunk B.S., Karbstein K. Powering through ribosome assembly. RNA 2009, 15:2083-2104.
4. Warner J.R., McIntosh K.B. How common are extraribosomal functions of ribosomal proteins? Mol. Cell 2009, 34:3-11.
5. Lafontaine D., et al. The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 1995, 9:2470-2481.
6. 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.
7. Gadal O., et al. Rlp7p is associated with 60S preribosomes, restricted to the granular component of the nucleolus, and required for pre-rRNA processing. J. Cell Biol. 2002, 157:941-951.
8. Nunomura A., et al. RNA oxidation in Alzheimer disease and related neurodegenerative disorders. Acta Neuropathol. 2009, 118:151-166.
9. Doma M.K., Parker R. RNA quality control in eukaryotes. Cell 2007, 131:660-668.
10. Doma M.K., Parker R. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 2006, 440:561-564.
11. LaRiviere F.J., et al. A late-acting quality control process for mature eukaryotic rRNAs. Mol. Cell 2006, 24:619-626.
12. Schmid M., Jensen T.H. The exosome: a multipurpose RNA-decay machine. Trends Biochem. Sci. 2008, 33:501-510.
13. Cole S.E., et al. A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol. Cell 2009, 34:440-450.
14. Graille M., et al. Structure of yeast Dom34: a protein related to translation termination factor Erf1 and involved in No-Go decay. J. Biol. Chem. 2008, 283:7145-7154.
15. Carr-Schmid A., et al. Novel G-protein complex whose requirement is linked to the translational status of the cell. Mol. Cell. Biol. 2002, 22:2564-2574.
16. Balagopal V., Parker R. Polysomes, P bodies and stress granules: states and fates of eukaryotic mRNAs. Curr. Opin. Cell Biol. 2009, 21:403-408.
17. Fujii K., et al. A role for ubiquitin in the clearance of nonfunctional rRNAs. Genes Dev. 2009, 23:963-974.
18. Beau I., et al. Lost to translation: when autophagy targets mature ribosomes. Trends Cell Biol. 2008, 18:311-314.
19. Suter B., et al. Examining protein protein interactions using endogenously tagged yeast arrays: the cross-and-capture system. Genome Res. 2007, 17:1774-1782.
20. Krogan N.J., et al. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440:637-643.
21. Kaganovich D., et al. Misfolded proteins partition between two distinct quality control compartments. Nature 2008, 454:1088-1095.
22. Houseley J., et al. RNA-quality control by the exosome. Nat. Rev. Mol. Cell Biol. 2006, 7:529-539.
23. LaCava J., et al. RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 2005, 121:713-724.
24. Wyers F., et al. Cryptic pol II transcripts are degraded by a nuclear quality control pathway involving a new poly(A) polymerase. Cell 2005, 121:725-737.
25. Vanacova S., et al. A new yeast poly(A) polymerase complex involved in RNA quality control. PLoS Biology 2005, 3:e189.
26. Andersen K.R., et al. Take the "A" tail - quality control of ribosomal and transfer RNA. Biochim. Biophys. Acta 2008, 1779:532-537.
27. Dragon F., et al. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 2002, 417:967-970.
28. Gallagher J.E., et al. RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 2004, 18:2506-2517.
29. Turner A.J., et al. A novel small-subunit processome assembly intermediate that contains the U3 snoRNP, nucleolin, RRP5, and DBP4. Mol. Cell. Biol. 2009, 29:3007-3017.
30. Prieto J.L., McStay B. Recruitment of factors linking transcription and processing of pre-rRNA to NOR chromatin is UBF-dependent and occurs independent of transcription in human cells. Genes Dev. 2007, 21:2041-2054.
31. Wery M., et al. The nuclear poly(A) polymerase and Exosome cofactor Trf5 is recruited cotranscriptionally to nucleolar surveillance. RNA 2009, 15:406-419.
32. Dez C., et al. Roles of the HEAT repeat proteins Utp10 and Utp20 in 40S ribosome maturation. RNA 2007, 13:1516-1527.
33. Kuai L., et al. Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:8581-8586.
34. Fang F., et al. 5-fluorouracil enhances exosome-dependent accumulation of polyadenylated rRNAs. Mol. Cell. Biol. 2004, 24:10766-10776.
35. Schneider D.A., et al. Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly. Mol. Cell 2007, 26:217-229.
36. Dez C., et al. Surveillance of nuclear-restricted pre-ribosomes within a subnucleolar region of Saccharomyces cerevisiae. EMBO J. 2006, 25:1534-1546.
37. Nakatogawa H., et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat. Rev. Mol. Cell Biol. 2009, 10:458-467.
38. Kraft C., et al. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat. Cell Biol. 2008, 10:602-610.
39. Kraft C., Peter M. Is the Rsp5 ubiquitin ligase involved in the regulation of ribophagy? Autophagy 2008, 4:838-840.
40. Pan X., et al. Nucleus-vacuole junctions in Saccharomyces cerevisiae are formed through the direct interaction of Vac8p with Nvj1p. Mol. Biol. Cell 2000, 11:2445-2457.
41. Roberts P., et al. Piecemeal microautophagy of nucleus in Saccharomyces cerevisiae. Mol. Biol. Cell 2003, 14:129-141.
42. Wurtmann E.J., Wolin S.L. RNA under attack: cellular handling of RNA damage. Crit. Rev. Biochem. Mol. Biol. 2009, 44:34-49.
43. Mroczek S., Kufel J. Apoptotic signals induce specific degradation of ribosomal RNA in yeast. Nucleic Acids Res. 2008, 36:2874-2888.
44. Thompson D.M., et al. tRNA cleavage is a conserved response to oxidative stress in eukaryotes. RNA 2008, 14:2095-2103.
45. Thompson D.M., Parker R. The RNase Rny1p cleaves tRNAs and promotes cell death during oxidative stress in Saccharomyces cerevisiae. J. Cell Biol. 2009, 185:43-50.
46. Derenzini M., et al. What the nucleolus says to a tumour pathologist. Histopathology 2009, 54:753-762.
47. Mayer C., Grummt I. Cellular stress and nucleolar function. Cell Cycle 2005, 4:1036-1038.
48. Rubbi C.P., Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J. 2003, 22:6068-6077.
49. Azuma M., et al. Perturbation of rRNA synthesis in the bap28 mutation leads to apoptosis mediated by p53 in the zebrafish central nervous system. J. Biol. Chem. 2006, 281:13309-13316.
50. Pestov D.G., et al. Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: effects of nucleolar protein Bop1 on G(1)/S transition. Mol. Cell. Biol. 2001, 21:4246-4255.
51. Johnson R.M., et al. Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14790-14795.
52. Lempiainen H., Shore D. Growth control and ribosome biogenesis. Curr. Opin. Cell Biol. 2009, 21:1-9.
53. Jorgensen P., et al. Forging the factory: ribosome synthesis and growth control in budding yeast. Cell Growth: Control of Cell Size 2004, 329-370. CSHL Press. M.N. Hall (Ed.).
54. Neumann S., et al. Formation and nuclear export of tRNA, rRNA and mRNA is regulated by the ubiquitin ligase Rsp5p. EMBO Rep. 2003, 4:1156-1162.
55. Lam Y.W., et al. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 2007, 17:749-760.
56. Stavreva D.A., et al. Potential roles for ubiquitin and the proteasome during ribosome biogenesis. Mol. Cell Biol. 2006, 26:5131-5145.
57. Osheim Y.N., et al. Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol. Cell 2004, 16:943-954.
58. Honma Y., et al. TOR regulates late steps of ribosome maturation in the nucleoplasm via Nog1 in response to nutrients. EMBO J. 2006, 25:3832-3842.
59. Vanrobays E., et al. TOR regulates the subcellular distribution of DIM2, a KH domain protein required for cotranscriptional ribosome assembly and pre-40S ribosome export. RNA 2008, 14:2061-2073.
60. Schafer T., et al. Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 2006, 441:651-655.
61. Ulbrich C., et al. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 2009, 138:911-922.
62. Krick R., et al. Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol. Biol. Cell 2008, 19:4492-4505.
63. Perez-Fernandez J., et al. The 90S preribosome is a multimodular structure that is assembled through a hierarchical mechanism. Mol. Cell. Biol. 2007, 27:5414-5429.
64. Rudra D., et al. Potential interface between ribosomal protein production and pre-rRNA processing. Mol. Cell Biol. 2007, 27:4815-4824.
65. Ho J.H., Johnson A.W. NMD3 encodes an essential cytoplasmic protein required for stable 60S ribosomal subunits in Saccharomyces cerevisiae. Mol. Cell Biol. 1999, 19:2389-2399.
66. Iordanov M.S., et al. Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J. Biol. Chem. 1998, 273:15794-15803.
67. Mirzaei H., Regnier F. Protein-RNA cross-linking in the ribosomes of yeast under oxidative stress. J. Proteome Res. 2006, 5:3249-3259.
68. Ding Q., et al. Decreased RNA, and increased RNA oxidation, in ribosomes from early Alzheimer's disease. Neurochem. Res. 2006, 31:705-710.
69. Ding Q., et al. Ribosome dysfunction is an early event in Alzheimer's disease. J. Neurosci. 2005, 25:9171-9175.
70. Martinet W., et al. RNA damage in human atherosclerosis: pathophysiological significance and implications for gene expression studies. RNA Biol. 2005, 2:4-7.
71. Martinet W., et al. Reactive oxygen species induce RNA damage in human atherosclerosis. Eur. J. Clin. Invest. 2004, 34:323-327.
72. Nunomura A., et al. RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease. J. Neurosci. 1999, 19:1959-1964.
73. Honda K., et al. Ribosomal RNA in Alzheimer disease is oxidized by bound redox-active iron. J. Biol. Chem. 2005, 280:20978-20986.
74. Finley D., et al. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 1989, 338:394-401.
75. Spence J., et al. Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 2000, 102:67-76.
76. Lacombe T., et al. Linear ubiquitin fusion to Rps31 and its subsequent cleavage are required for the efficient production and functional integrity of 40S ribosomal subunits. Mol. Microbiol. 2009, 72:69-84.
77. 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.
78. Soudet J., et al. Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae. EMBO J 2010, 29:80-92.
79. Aas P.A., et al. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 2003, 421:859-863.
80. Ougland R., et al. AlkB restores the biological function of mRNA and tRNA inactivated by chemical methylation. Mol. Cell 2004, 16:107-116.
81. Pulk A., et al. Ribosome reactivation by replacement of damaged proteins. Mol. Microbiol 2009, Epub ahead of print PMID 19968789.