Proofreading of Pre-40S Ribosome Maturation by a Translation Initiation Factor and 60S Subunits

Overview

Journal Nat Struct Mol Biol

Specialties Cell Biology
Molecular Biology

Date 2012 Jul 4

PMID 22751017

Citations 121

Authors

Simon Lebaron

Claudia Schneider

Robert W van Nues

Agata Swiatkowska

Dietrich Walsh

Bettina Bottcher

Sander Granneman

Nicholas J Watkins

David Tollervey

Affiliations

Soon will be listed here.

Abstract

In the final steps of yeast ribosome synthesis, immature translation-incompetent pre-40S particles that contain 20S pre-rRNA are converted to the mature translation-competent subunits containing the 18S rRNA. An assay for 20S pre-rRNA cleavage in purified pre-40S particles showed that cleavage by the PIN domain endonuclease Nob1 was strongly stimulated by the GTPase activity of Fun12, the yeast homolog of cytoplasmic translation initiation factor eIF5b. Cleavage of the 20S pre-rRNA was also inhibited in vivo and in vitro by blocking binding of Fun12 to the 25S rRNA through specific methylation of its binding site. Cleavage competent pre-40S particles stably associated with Fun12 and formed 80S complexes with 60S ribosomal subunits. We propose that recruitment of 60S subunits promotes GTP hydrolysis by Fun12, leading to structural rearrangements within the pre-40S particle that bring Nob1 and the pre-rRNA cleavage site together.

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References

Lebaron S, Papin C, Capeyrou R, Chen Y, Froment C, Monsarrat B . The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. EMBO J. 2009; 28(24):3808-19. PMC: 2797057. DOI: 10.1038/emboj.2009.335. View

Allmang C, Henry Y, Morrissey J, Wood H, Petfalski E, Tollervey D . Processing of the yeast pre-rRNA at sites A(2) and A(3) is linked. RNA. 1996; 2(1):63-73. PMC: 1369351. View

Decatur W, Fournier M . rRNA modifications and ribosome function. Trends Biochem Sci. 2002; 27(7):344-51. DOI: 10.1016/s0968-0004(02)02109-6. View

La Teana A, Gualerzi C, Brimacombe R . From stand-by to decoding site. Adjustment of the mRNA on the 30S ribosomal subunit under the influence of the initiation factors. RNA. 1995; 1(8):772-82. PMC: 1369318. View

Valasek L, Hasek J, Nielsen K, Hinnebusch A . Dual function of eIF3j/Hcr1p in processing 20 S pre-rRNA and translation initiation. J Biol Chem. 2001; 276(46):43351-60. DOI: 10.1074/jbc.M106887200. View

Collins S, Kemmeren P, Zhao X, Greenblatt J, Spencer F, Holstege F . Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteomics. 2007; 6(3):439-50. DOI: 10.1074/mcp.M600381-MCP200. View

Veith T, Martin R, Wurm J, Weis B, Duchardt-Ferner E, Safferthal C . Structural and functional analysis of the archaeal endonuclease Nob1. Nucleic Acids Res. 2011; 40(7):3259-74. PMC: 3326319. DOI: 10.1093/nar/gkr1186. View

Karbstein K, Jonas S, Doudna J . An essential GTPase promotes assembly of preribosomal RNA processing complexes. Mol Cell. 2005; 20(4):633-43. DOI: 10.1016/j.molcel.2005.09.017. View

Petracek M, Longtine M . PCR-based engineering of yeast genome. Methods Enzymol. 2002; 350:445-69. DOI: 10.1016/s0076-6879(02)50978-2. View

10.

Valle M, Zavialov A, Sengupta J, Rawat U, Ehrenberg M, Frank J . Locking and unlocking of ribosomal motions. Cell. 2003; 114(1):123-34. DOI: 10.1016/s0092-8674(03)00476-8. View

11.

Yeh L, Thweatt R, Lee J . Internal transcribed spacer 1 of the yeast precursor ribosomal RNA. Higher order structure and common structural motifs. Biochemistry. 1990; 29(25):5911-8. DOI: 10.1021/bi00477a005. View

12.

Lafontaine D, Delcour J, Glasser A, Desgres J, Vandenhaute J . The DIM1 gene responsible for the conserved m6(2)Am6(2)A dimethylation in the 3'-terminal loop of 18 S rRNA is essential in yeast. J Mol Biol. 1994; 241(3):492-7. DOI: 10.1006/jmbi.1994.1525. View

13.

Leshin J, Rakauskaite R, Dinman J, Meskauskas A . Enhanced purity, activity and structural integrity of yeast ribosomes purified using a general chromatographic method. RNA Biol. 2010; 7(3):354-60. PMC: 4118464. DOI: 10.4161/rna.7.3.11648. View

14.

Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M . The structure of the eukaryotic ribosome at 3.0 Å resolution. Science. 2011; 334(6062):1524-9. DOI: 10.1126/science.1212642. View

15.

Udem S, Warner J . The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J Biol Chem. 1973; 248(4):1412-6. View

16.

Shin B, Kim J, Acker M, Maher K, Lorsch J, Dever T . rRNA suppressor of a eukaryotic translation initiation factor 5B/initiation factor 2 mutant reveals a binding site for translational GTPases on the small ribosomal subunit. Mol Cell Biol. 2008; 29(3):808-21. PMC: 2630678. DOI: 10.1128/MCB.00896-08. View

17.

Roll-Mecak A, Cao C, Dever T, Burley S . X-Ray structures of the universal translation initiation factor IF2/eIF5B: conformational changes on GDP and GTP binding. Cell. 2000; 103(5):781-92. DOI: 10.1016/s0092-8674(00)00181-1. View

18.

Mangiarotti G, Chiaberge S, Bulfone S . rRNA maturation as a "quality" control step in ribosomal subunit assembly in Dictyostelium discoideum. J Biol Chem. 1997; 272(44):27818-22. DOI: 10.1074/jbc.272.44.27818. View

19.

Lee J, Pestova T, Shin B, Cao C, Choi S, Dever T . Initiation factor eIF5B catalyzes second GTP-dependent step in eukaryotic translation initiation. Proc Natl Acad Sci U S A. 2002; 99(26):16689-94. PMC: 139205. DOI: 10.1073/pnas.262569399. View

20.

Campbell T, Brown E . Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. J Bacteriol. 2008; 190(7):2537-45. PMC: 2293177. DOI: 10.1128/JB.01744-07. View