Small ribosomal protein RPS0 stimulates translation initiation by mediating 40S-binding of eIF3 via its direct contact with the eIF3a/TIF32 subunit

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Kouba, Tomáš ^a   Dányi, István ^a   Gunišová, Stanislava ^a   Munzarová, Vanda ^a   Vlčková, Vladislava ^a   Cuchalová, Lucie ^a   Neueder, Andreas ^b   Milkereit, Philipp ^b   Valášek, Leoš Shivaya ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR; INITIATION FACTOR 3; INITIATION FACTOR 3A; MESSENGER RNA; PROTEIN S0A; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CONTROLLED STUDY; MONOSOME; NONHUMAN; POLYSOME; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN INTERACTION; RIBOSOME; RIBOSOME SUBUNIT; TRANSLATION INITIATION;

EUKARYOTIC INITIATION FACTOR-3; GENE KNOCKOUT TECHNIQUES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

EUKARYOTA;

EID: 84863633085     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040464     Document Type: Article

References (40)

1. Valášek LS, (2012) 'Ribozoomin' - Translation Initiation from the Perspective of the Ribosome-bound Eukaryotic Initiation Factors (eIFs). Curr Protein Pept Sci: in press.
2. Koromilas AE, Lazaris-Karatzas A, Sonenberg N, (1992) mRNAs containing extensive secondary structure in their 5′ non-coding region translate efficiently in cells overexpressing initiation factor eIF-4E. EMBO J 11: 4153-4158.
3. Pestova TV, Kolupaeva VG, (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16: 2906-2922.
4. Jivotovskaya A, Valášek L, Hinnebusch AG, Nielsen KH, (2006) Eukaryotic translation initiation factor 3 (eIF3) and eIF2 can promote mRNA binding to 40S subunits independently of eIF4G in yeast. Mol Cell Biol 26: 1355-1372.
5. Mitchell SF, Walker SE, Algire MA, Park E-H, Hinnebusch AG, et al. (2010) The 5′-7-Methylguanosine Cap on Eukaryotic mRNAs Serves Both to Stimulate Canonical Translation Initiation and to Block an Alternative Pathway. Mol Cell 39: 950-962.
6. Cuchalová L, Kouba T, Herrmannová A, Danyi I, Chiu W-l, et al. (2010) The RNA Recognition Motif of Eukaryotic Translation Initiation Factor 3g (eIF3g) Is Required for Resumption of Scanning of Posttermination Ribosomes for Reinitiation on GCN4 and Together with eIF3i Stimulates Linear Scanning. Mol Cell Biol 30: 4671-4686.
7. Nielsen KH, Szamecz B, Valasek LJ, A., Shin BS, Hinnebusch AG, (2004) Functions of eIF3 downstream of 48S assembly impact AUG recognition and GCN4 translational control. EMBO J 23: 1166-1177.
8. Valášek L, Nielsen KH, Zhang F, Fekete CA, Hinnebusch AG, (2004) Interactions of Eukaryotic Translation Initiation Factor 3 (eIF3) Subunit NIP1/c with eIF1 and eIF5 Promote Preinitiation Complex Assembly and Regulate Start Codon Selection. Mol Cell Biol 24: 9437-9455.
9. Nielsen KH, Valášek L, Sykes C, Jivotovskaya A, Hinnebusch AG, (2006) Interaction of the RNP1 motif in PRT1 with HCR1 promotes 40S binding of eukaryotic initiation factor 3 in yeast. Mol Cell Biol 26: 2984-2998.
10. ElAntak L, Wagner S, Herrmannová A, Karásková M, Rutkai E, et al. (2010) The indispensable N-terminal half of eIF3j co-operates with its structurally conserved binding partner eIF3b-RRM and eIF1A in stringent AUG selection. J Mol Biol 396: 1097-1116.
11. Chiu W-L, Wagner S, Herrmannová A, Burela L, Zhang F, et al. (2010) The C-Terminal Region of Eukaryotic Translation Initiation Factor 3a (eIF3a) Promotes mRNA Recruitment, Scanning, and, Together with eIF3j and the eIF3b RNA Recognition Motif, Selection of AUG Start Codons. Mol Cell Biol 30: 4415-4434.
12. Herrmannová A, Daujotyte D, Yang JC, Cuchalová L, Gorrec F, et al. (2012) Structural analysis of an eIF3 subcomplex reveals conserved interactions required for a stable and proper translation pre-Initiation complex assembly. Nucleic Acids Res 40: 2294-2311.
13. Asano K, Clayton J, Shalev A, Hinnebusch AG, (2000) A multifactor complex of eukaryotic initiation factors eIF1, eIF2, eIF3, eIF5, and initiator tRNAMet is an important translation initiation intermediate in vivo. Genes Dev 14: 2534-2546.
14. Sokabe M, Fraser CS, Hershey JWB, (2011) The human translation initiation multi-factor complex promotes methionyl-tRNAi binding to the 40S ribosomal subunit. Nucleic Acids Research 40: 905-913.
15. Dennis MD, Person MD, Browning KS, (2009) Phosphorylation of Plant Translation Initiation Factors by CK2 Enhances the in Vitro Interaction of Multifactor Complex Components. J Biol Chem 284: 20615-20628.
16. Valášek L, Nielsen KH, Hinnebusch AG, (2002) Direct eIF2-eIF3 contact in the multifactor complex is important for translation initiation in vivo. EMBO J 21: 5886-5898.
17. Yamamoto Y, Singh CR, Marintchev A, Hall NS, Hannig EM, et al. (2005) The eukaryotic initiation factor (eIF) 5 HEAT domain mediates multifactor assembly and scanning with distinct interfaces to eIF1, eIF2, eIF3, and eIF4G. Proc Natl Acad Sci U S A 102: 16164-16169.
18. Valášek L, Mathew A, Shin BS, Nielsen KH, Szamecz B, et al. (2003) The Yeast eIF3 Subunits TIF32/a and NIP1/c and eIF5 Make Critical Connections with the 40S Ribosome in vivo. Genes Dev 17: 786-799.
19. Rabl J, Leibundgut M, Ataide SF, Haag A, Ban N, (2011) Crystal Structure of the Eukaryotic 40S Ribosomal Subunit in Complex with Initiation Factor 1. Science 331: 730-736.
20. Kouba T, Rutkai E, Karasková M, Valášek LS, (2012) The eIF3c/NIP1 PCI domain interacts with RNA and RACK1/ASC1 and promotes assembly of the pre-initiation complexes. Nucleic Acids Research 40: 2683-2699.
21. Szamecz B, Rutkai E, Cuchalova L, Munzarova V, Herrmannova A, et al. (2008) eIF3a cooperates with sequences 5′ of uORF1 to promote resumption of scanning by post-termination ribosomes for reinitiation on GCN4 mRNA. Genes Dev 22: 2414-2425.
22. Spahn CM, Beckmann R, Eswar N, Penczek PA, Sali A, et al. (2001) Structure of the 80S ribosome from Saccharomyces cerevisiae- tRNA ribosome and subunit-subunit interactions. Cell 107: 373-386.
23. Ford CL, Randal-Whitis L, Ellis SR, (1999) Yeast proteins related to the p40/laminin receptor precursor are required for 20S ribosomal RNA processing and the maturation of 40S ribosomal subunits. Cancer Res 59: 704-710.
24. Demianova M, Formosa TG, Ellis SR, (1996) Yeast proteins related to the p40/laminin receptor precursor are essential components of the 40 S ribosomal subunit. J Biol Chem 271: 11383-11391.
25. Ben-Shem A, Jenner L, Yusupova G, Yusupov M, (2010) Crystal Structure of the Eukaryotic Ribosome. Science 330: 1203-1209.
26. Valášek L, Szamecz B, Hinnebusch AG, Nielsen KH, (2007) In vivo stabilization of preinitiation complexes by formaldehyde cross-linking. Methods Enzymol 429: 163-183.
27. Soudet J, Gelugne J-P, Belhabich-Baumas K, Caizergues-Ferrer M, Mougin A, (2010) Immature small ribosomal subunits can engage in translation initiation in Saccharomyces cerevisiae. EMBO J 29: 80-92.
28. Ferreira-Cerca S, Poll G, Kuhn H, Neueder A, Jakob S, et al. (2007) Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol Cell 28: 446-457.
29. Fraser CS, Berry KE, Hershey JW, Doudna JA, (2007) 3j is located in the decoding center of the human 40S ribosomal subunit. Mol Cell 26: 811-819.
30. Valášek L, Phan L, Schoenfeld LW, Valášková V, Hinnebusch AG, (2001) Related eIF3 subunits TIF32 and HCR1 interact with an RNA recoginition motif in PRT1 required for eIF3 integrity and ribosome binding. EMBO J 20: 891-904.
31. Lumsden T, Bentley AA, Beutler W, Ghosh A, Galkin O, et al. (2010) Yeast strains with N-terminally truncated ribosomal protein S5: implications for the evolution, structure and function of the Rps5/Rps7 proteins. Nucleic Acids Research 38: 1261-1272.
32. Munzarová V, Pánek J, Gunišová S, Dányi I, Szamecz B, et al. (2011) Translation Reinitiation Relies on the Interaction between eIF3a/TIF32 and Progressively Folded cis-Acting mRNA Elements Preceding Short uORFs. PLoS Genet 7: e1002137.
33. Ferreira-Cerca S, Pöll G, Gleizes P-E, Tschochner H, Milkereit P, (2005) Roles of Eukaryotic Ribosomal Proteins in Maturation and Transport of Pre-18S rRNA and Ribosome Function. Molecular Cell 20: 263-275.
34. Nemoto N, Singh CR, Udagawa T, Wang S, Thorson E, et al. (2010) Yeast 18S rRNA is directly involved in the ribosomal response to stringent AUG selection during translation initiation. Journal of Biological Chemistry: in press.
35. Voth WP, Jiang YW, Stillman DJ, (2003) New 'marker swap' plasmids for converting selectable markers on budding yeast gene disruptions and plasmids. Yeast 20: 985-993.
36. Gietz RD, Sugino A, (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74: 527-534.
37. Smith DB, Johnson KS, (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67: 31-40.
38. Nielsen KH, Valášek L, (2007) In vivo deletion analysis of the architecture of a multi-protein complex of translation initiation factors. Methods Enzymol 431: 15-32.
39. Acker MG, Kolitz SE, Mitchell SF, Nanda JS, Lorsch JR, et al. (2007) Reconstitution of Yeast Translation Initiation. Methods in Enzymology: Academic Press. pp pp. 111-145.
40. Taylor DJ, Devkota B, Huang AD, Topf M, Narayanan E, et al. (2009) Comprehensive Molecular Structure of the Eukaryotic Ribosome. Structure 17: 1591-1604.