A Translation-like Cycle is a Quality Control Checkpoint for Maturing 40S Ribosome Subunits

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2012 Jul 10

PMID 22770215

Citations 171

Authors

Bethany S Strunk

Megan N Novak

Crystal L Young

Katrin Karbstein

Affiliations

Soon will be listed here.

Abstract

Assembly factors (AFs) prevent premature translation initiation on small (40S) ribosomal subunit assembly intermediates by blocking ligand binding. However, it is unclear how AFs are displaced from maturing 40S ribosomes, if or how maturing subunits are assessed for fidelity, and what prevents premature translation initiation once AFs dissociate. Here we show that maturation involves a translation-like cycle whereby the translation factor eIF5B, a GTPase, promotes joining of large (60S) subunits with pre-40S subunits to give 80S-like complexes, which are subsequently disassembled by the termination factor Rli1, an ATPase. The AFs Tsr1 and Rio2 block the mRNA channel and initiator tRNA binding site, and therefore 80S-like ribosomes lack mRNA or initiator tRNA. After Tsr1 and Rio2 dissociate from 80S-like complexes Rli1-directed displacement of 60S subunits allows for translation initiation. This cycle thus provides a functional test of 60S subunit binding and the GTPase site before ribosomes enter the translating pool.

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References

Filbin M, Kieft J . Toward a structural understanding of IRES RNA function. Curr Opin Struct Biol. 2009; 19(3):267-76. PMC: 2757110. DOI: 10.1016/j.sbi.2009.03.005. View

Cole S, LaRiviere F, Merrikh C, Moore M . A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol Cell. 2009; 34(4):440-50. PMC: 2712825. DOI: 10.1016/j.molcel.2009.04.017. View

Granneman S, Nandineni M, Baserga S . The putative NTPase Fap7 mediates cytoplasmic 20S pre-rRNA processing through a direct interaction with Rps14. Mol Cell Biol. 2005; 25(23):10352-64. PMC: 1291222. DOI: 10.1128/MCB.25.23.10352-10364.2005. View

Soudet J, Gelugne J, Belhabich-Baumas K, Caizergues-Ferrer M, Mougin A . Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae. EMBO J. 2009; 29(1):80-92. PMC: 2808361. DOI: 10.1038/emboj.2009.307. View

Rabl J, Leibundgut M, Ataide S, Haag A, Ban N . Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science. 2011; 331(6018):730-6. DOI: 10.1126/science.1198308. View

Kispal G, Sipos K, Lange H, Fekete Z, Bedekovics T, Janaky T . Biogenesis of cytosolic ribosomes requires the essential iron-sulphur protein Rli1p and mitochondria. EMBO J. 2005; 24(3):589-98. PMC: 548650. DOI: 10.1038/sj.emboj.7600541. View

Lund E, Dahlberg J . Proofreading and aminoacylation of tRNAs before export from the nucleus. Science. 1998; 282(5396):2082-5. DOI: 10.1126/science.282.5396.2082. View

Acker M, Shin B, Nanda J, Saini A, Dever T, Lorsch J . Kinetic analysis of late steps of eukaryotic translation initiation. J Mol Biol. 2008; 385(2):491-506. PMC: 2654283. DOI: 10.1016/j.jmb.2008.10.029. View

Becker T, Armache J, Jarasch A, Anger A, Villa E, Sieber H . Structure of the no-go mRNA decay complex Dom34-Hbs1 bound to a stalled 80S ribosome. Nat Struct Mol Biol. 2011; 18(6):715-20. DOI: 10.1038/nsmb.2057. View

10.

Strunk B, Loucks C, Su M, Vashisth H, Cheng S, Schilling J . Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science. 2011; 333(6048):1449-53. PMC: 3402165. DOI: 10.1126/science.1208245. View

11.

Lamanna A, Karbstein K . An RNA conformational switch regulates pre-18S rRNA cleavage. J Mol Biol. 2010; 405(1):3-17. PMC: 3006654. DOI: 10.1016/j.jmb.2010.09.064. View

12.

Khoshnevis S, Gross T, Rotte C, Baierlein C, Ficner R, Krebber H . The iron-sulphur protein RNase L inhibitor functions in translation termination. EMBO Rep. 2010; 11(3):214-9. PMC: 2838684. DOI: 10.1038/embor.2009.272. View

13.

Bhattacharya A, McIntosh K, Willis I, Warner J . Why Dom34 stimulates growth of cells with defects of 40S ribosomal subunit biosynthesis. Mol Cell Biol. 2010; 30(23):5562-71. PMC: 2976434. DOI: 10.1128/MCB.00618-10. View

14.

Passmore L, Schmeing T, Maag D, Applefield D, Acker M, Algire M . The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol Cell. 2007; 26(1):41-50. DOI: 10.1016/j.molcel.2007.03.018. View

15.

Pisareva V, Skabkin M, Hellen C, Pestova T, Pisarev A . Dissociation by Pelota, Hbs1 and ABCE1 of mammalian vacant 80S ribosomes and stalled elongation complexes. EMBO J. 2011; 30(9):1804-17. PMC: 3101999. DOI: 10.1038/emboj.2011.93. View

16.

Strunk B, Karbstein K . Powering through ribosome assembly. RNA. 2009; 15(12):2083-104. PMC: 2779681. DOI: 10.1261/rna.1792109. View

17.

Valasek L, Szamecz B, Hinnebusch A, Nielsen K . In vivo stabilization of preinitiation complexes by formaldehyde cross-linking. Methods Enzymol. 2007; 429:163-83. DOI: 10.1016/S0076-6879(07)29008-1. View

18.

Liang X, Liu Q, Fournier M . rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol Cell. 2007; 28(6):965-77. DOI: 10.1016/j.molcel.2007.10.012. View

19.

Li Z, Lee I, Moradi E, Hung N, Johnson A, Marcotte E . Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol. 2009; 7(10):e1000213. PMC: 2749941. DOI: 10.1371/journal.pbio.1000213. View

20.

Arava Y, Wang Y, Storey J, Liu C, Brown P, Herschlag D . Genome-wide analysis of mRNA translation profiles in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2003; 100(7):3889-94. PMC: 153018. DOI: 10.1073/pnas.0635171100. View