Asc1, homolog of human RACK1, prevents frameshifting in yeast by ribosomes stalled at CGA codon repeats

RNA

Volumn 21, Issue 5, 2015, Pages 935-945

  Wolf, Andrew S ^a   Grayhack, Elizabeth J ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Asc1; Frameshift; Rack1; Reading frame; Ribosome; Translation stalls

Indexed keywords

ASC1 PROTEIN; PROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG; ASC1 PROTEIN, S CEREVISIAE; CELL SURFACE RECEPTOR; CODON; GNB2L1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STOP CODON; TUMOR PROTEIN;

ARTICLE; CGA CODON; CODON; CONTROLLED STUDY; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; QUALITY CONTROL; RIBOSOMAL FRAMESHIFTING; RNA TRANSLATION; YEAST; GENETICS; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN SYNTHESIS; RIBOSOME; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STOP CODON; TRANSCRIPTION INITIATION SITE; TRINUCLEOTIDE REPEAT;

EUKARYOTA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BASE SEQUENCE; CODON; CODON, TERMINATOR; FRAMESHIFTING, RIBOSOMAL; GTP-BINDING PROTEINS; HUMANS; NEOPLASM PROTEINS; PROTEIN BIOSYNTHESIS; RECEPTORS, CELL SURFACE; RIBOSOMES; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY; TRANSCRIPTION INITIATION SITE; TRINUCLEOTIDE REPEATS;

EID: 84928016073     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.049080.114     Document Type: Article

References (59)

1. Adams DR, Ron D, Kiely PA. 2011. RACK1, A multifaceted scaffolding protein: structure and function. Cell Commun Signal 9: 22.
2. Alexandrov A, Vignali M, LaCount DJ, Quartley E, de Vries C, De Rosa D, Babulski J, Mitchell SF, Schoenfeld LW, Fields S, et al. 2004. A facile method for high-throughput co-expression of protein pairs. Mol Cell Proteomics 3: 934-938.
3. Balagopal V, Parker R. 2011. Stm1 modulates translation after 80S formation in Saccharomyces cerevisiae. RNA 17: 835-842.
4. Baranov PV, Gesteland RF, Atkins JF. 2004. P-site tRNA is a crucial initiator of ribosomal frameshifting. RNA 10: 221-230.
5. Baum S, Bittins M, Frey S, Seedorf M. 2004. Asc1p, a WD40-domain containing adaptor protein, is required for the interaction of the RNA-binding protein Scp160p with polysomes. Biochem J 380: 823-830.
6. Belcourt MF, Farabaugh PJ. 1990. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 62: 339-352.
7. Bengtson MH, Joazeiro CA. 2010. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467: 470-473.
8. Bhattacharya A, McIntosh KB, Willis IM, Warner JR. 2010. Why Dom34 stimulates growth of cells with defects of 40S ribosomal subunit biosynthesis. Mol Cell Biol 30: 5562-5571.
9. Bhushan S, Gartmann M, Halic M, Armache JP, Jarasch A, Mielke T, Berninghausen O, Wilson DN, Beckmann R. 2010. α-Helical nascent polypeptide chains visualized within distinct regions of the ribosomal exit tunnel. Nat Struct Mol Biol 17: 313-317.
10. Blobel G, Sabatini DD. 1970. Controlled proteolysis of nascent polypeptides in rat liver cell fractions. I. Location of the polypeptides within ribosomes. J Cell Biol 45: 130-145.
11. Brandman O, Stewart-Ornstein J, Wong D, Larson A, Williams CC, Li GW, Zhou S, King D, Shen PS, Weibezahn J, et al. 2012. A ribosome-bound quality control complex triggers degradation of nascent peptides and signals translation stress. Cell 151: 1042-1054.
12. Bruckmann A, Hensbergen PJ, Balog CI, Deelder AM, Brandt R, Snoek IS, Steensma HY, van Heusden GP. 2009. Proteome analysis of aerobically and anaerobically grown Saccharomyces cerevisiae cells. J Proteomics 71: 662-669.
13. Ceci M, Gaviraghi C, Gorrini C, Sala LA, Offenhäuser N, Marchisio PC, Biffo S. 2003. Release of eIF6 (p27BBP) from the 60S subunit allows 80S ribosome assembly. Nature 426: 579-584.
14. Chen L, Muhlrad D, Hauryliuk V, Cheng Z, Lim MK, Shyp V, Parker R, Song H. 2010. Structure of the Dom34-Hbs1 complex and implications for no-go decay. Nat Struct Mol Biol 17: 1233-1240.
15. Chu J, Hong NA, Masuda CA, Jenkins BV, Nelms KA, Goodnow CC, Glynne RJ, Wu H, Masliah E, Joazeiro CA, et al. 2009. A mouse forward genetics screen identifies LISTERIN as an E3 ubiquitin ligase involved in neurodegeneration. Proc Natl Acad Sci 106: 2097-2103.
16. Chu D, Kazana E, Bellanger N, Singh T, Tuite MF, von der Haar T. 2014. Translation elongation can control translation initiation on eukaryotic mRNAs. EMBO J 33: 21-34.
17. Coyle SM, Gilbert WV, Doudna JA. 2009. Direct link between RACK1 function and localization at the ribosome in vivo. Mol Cell Biol 29: 1626-1634.
18. Dean KM, Grayhack EJ. 2012. RNA-ID, a highly sensitive and robust method to identify cis-regulatory sequences using superfolder GFP and a fluorescence-based assay. RNA 18: 2335-2344.
19. Dinman JD. 2012. Mechanisms and implications of programmed translational frameshifting. Wiley Interdiscip Rev RNA 3: 661-673.
20. Doma MK, Parker R. 2006. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440: 561-564.
21. Fang Y, Treffers EE, Li Y, Tas A, Sun Z, van der Meer Y, de Ru AH, van Veelen PA, Atkins JF, Snijder EJ, et al. 2012. Efficient -2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc Natl Acad Sci 109: E2920-E2928.
22. Frischmeyer PA, van Hoof A, O'Donnell K, Guerrerio AL, Parker R, Dietz HC. 2002. An mRNA surveillance mechanism that eliminates transcripts lacking termination codons. Science 295: 2258-2261.
23. Gelperin DM, White MA, Wilkinson ML, Kon Y, Kung LA, Wise KJ, Lopez-Hoyo N, Jiang L, Piccirillo S, Yu H, et al. 2005. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev 19: 2816-2826.
24. Gerbasi VR, Weaver CM, Hill S, Friedman DB, Link AJ. 2004. Yeast Asc1p and mammalian RACK1 are functionally orthologous core 40S ribosomal proteins that repress gene expression. Mol Cell Biol 24: 8276-8287.
25. Grant TD, Snell EH, Luft JR, Quartley E, Corretore S, Wolfley JR, Snell ME, Hadd A, Perona JJ, Phizicky EM, et al. 2011. Structural conservation of an ancient tRNA sensor in eukaryotic glutaminyl-tRNA synthetase. Nucleic Acids Res 40: 3723-3731.
26. Guarraia C, Norris L, Raman A, Farabaugh PJ. 2007. Saturation mutagenesis of a +1 programmed frameshift-inducing mRNA sequence derived from a yeast retrotransposon. RNA 13: 1940-1947.
27. Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH. 2002. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30: e23.
28. Gutierrez E, Shin BS, Woolstenhulme CJ, Kim JR, Saini P, Buskirk AR, Dever TE. 2013. eIF5A promotes translation of polyproline motifs. Mol Cell 51: 35-45.
29. Guydosh NR, Green R. 2014. Dom34 rescues ribosomes in 3′ untranslated regions. Cell 156: 950-962.
30. Hoffmann B, Mösch HU, Sattlegger E, Barthelmess IB, Hinnebusch A, Braus GH. 1999. The WD protein Cpc2p is required for repression of Gcn4 protein activity in yeast in the absence of amino-acid starvation. Mol Microbiol 31: 807-822.
31. Isken O, Maquat LE. 2007. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev 21: 1833-1856.
32. Kim HK, Liu F, Fei J, Bustamante C, Gonzalez RL Jr, Tinoco I Jr. 2014. A frameshifting stimulatory stem loop destabilizes the hybrid state and impedes ribosomal translocation. Proc Natl Acad Sci 111: 5538-5543.
33. Kiss-László Z, Henry Y, Bachellerie JP, Caizergues-Ferrer M, Kiss T. 1996. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 85: 1077-1088.
34. Kramer G, Ramachandiran V, Hardesty B. 2001. Cotranslational folding - omnia mea mecum porto? Int J Biochem Cell Biol 33: 541-553.
35. Kurland CG. 1992. Translational accuracy and the fitness of bacteria. Annu Rev Genet 26: 29-50.
36. Kuroha K, Akamatsu M, Dimitrova L, Ito T, Kato Y, Shirahige K, Inada T. 2010. Receptor for activated C kinase 1 stimulates nascent polypeptide-dependent translation arrest. EMBO Rep 11: 956-961.
37. Lareau LF, Hite DH, Hogan GJ, Brown PO. 2014. Distinct stages of the translation elongation cycle revealed by sequencing ribosome-protected mRNA fragments. eLife 3: e01257.
38. Letzring DP, Dean KM, Grayhack EJ. 2010. Control of translation efficiency in yeast by codon-anticodon interactions. RNA 16: 2516-2528.
39. Letzring DP, Wolf AS, Brule CE, Grayhack EJ. 2013. Translation of CGA codon repeats in yeast involves quality control components and ribosomal protein L1. RNA 19: 1208-1217.
40. Malkin LI, Rich A. 1967. Partial resistance of nascent polypeptide chains to proteolytic digestion due to ribosomal shielding. J Mol Biol 26: 329-346.
41. Martinez AK, Gordon E, Sengupta A, Shirole N, Klepacki D, Martinez-Garriga B, Brown LM, Benedik MJ, Yanofsky C, Mankin AS, et al. 2014. Interactions of the TnaC nascent peptide with rRNA in the exit tunnel enable the ribosome to respond to free tryptophan. Nucleic Acids Res 42: 1245-1256.
42. Moore SD, Sauer RT. 2007. The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 76: 101-124.
43. Murphy FV IV, Ramakrishnan V. 2004. Structure of a purine-purine wobble base pair in the decoding center of the ribosome. Nat Struct Mol Biol 11: 1251-1252.
44. 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.
45. Rachfall N, Schmitt K, Bandau S, Smolinski N, Ehrenreich A, Valerius O, Braus GH. 2013. RACK1/Asc1p, a ribosomal node in cellular signaling. Mol Cell Proteomics 12: 87-105.
46. Ramu H, Vazquez-Laslop N, Klepacki D, Dai Q, Piccirilli J, Micura R, Mankin AS. 2011. Nascent peptide in the ribosome exit tunnel affects functional properties of the A-site of the peptidyl transferase center. Mol Cell 41: 321-330.
47. Seidman JS, Janssen BD, Hayes CS. 2011. Alternative fates of paused ribosomes during translation termination. J Biol Chem 286: 31105-31112.
48. Sengupta J, Nilsson J, Gursky R, Spahn CM, Nissen P, Frank J. 2004. Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat Struct Mol Biol 11: 957-962.
49. Shoemaker CJ, Green R. 2011. Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proc Natl Acad Sci 108: E1392-E1398.
50. Shoemaker CJ, Green R. 2012. Translation drives mRNA quality control. Nat Struct Mol Biol 19: 594-601.
51. Shoemaker CJ, Eyler DE, Green R. 2010. Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330: 369-372.
52. Somogyi P, Jenner AJ, Brierley I, Inglis SC. 1993. Ribosomal pausing during translation of an RNA pseudoknot. Mol Cell Biol 13: 6931-6940.
53. Tsuboi T, Kuroha K, Kudo K, Makino S, Inoue E, Kashima I, Inada T. 2012. Dom34:hbs1 plays a general role in quality-control systems by dissociation of a stalled ribosome at the 3′ end of aberrant mRNA. Mol Cell 46: 518-529.
54. Tu C, Tzeng TH, Bruenn JA. 1992. Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc Natl Acad Sci 89: 8636-8640.
55. Tumu S, Patil A, Towns W, Dyavaiah M, Begley TJ. 2012. The gene-specific codon counting database: a genome-based catalog of one-, two-, three-, four- and five-codon combinations present in Saccharomyces cerevisiae genes. Database (Oxford) 2012: bas002.
56. van Hoof A, Frischmeyer PA, Dietz HC, Parker R. 2002. Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295: 2262-2264.
57. Wilson MA, Meaux S, van Hoof A. 2007. A genomic screen in yeast reveals novel aspects of nonstop mRNA metabolism. Genetics 177: 773-784.
58. Woolstenhulme CJ, Parajuli S, Healey DW, Valverde DP, Petersen EN, Starosta AL, Guydosh NR, Johnson WE, Wilson DN, Buskirk AR. 2013. Nascent peptides that block protein synthesis in bacteria. Proc Natl Acad Sci 110: E878-E887.
59. Zhou J, Lancaster L, Donohue JP, Noller HF. 2013. Crystal structures of EF-G-ribosome complexes trapped in intermediate states of translocation. Science 340: 1236086.