Translation of CGA codon repeats in yeast involves quality control components and ribosomal protein L1

RNA

Volumn 19, Issue 9, 2013, Pages 1208-1217

  Letzring, Daniel P ^a,b   Wolf, Andrew S ^a   Brule, Christina E ^a   Grayhack, Elizabeth J ^a  

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

^b Monroe County Crime Laboratory   (United States)

Author keywords

Codons; Genetic code; Ribosome; Translation; Ubiquitin; Yeast

Indexed keywords

ARGININE TRANSFER RNA; CYCLOHEXIMIDE; HYBRID PROTEIN; MESSENGER RNA; NUCLEAR PROTEIN; PAROMOMYCIN; PROTEASOME; PROTEIN HEL 2; RENILLA LUCIFERIN 2 MONOOXYGENASE; RIBOSOMAL PROTEIN L1; RIBOSOMAL PROTEIN L1 B; RIBOSOME RNA; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MASH1; TRANSFER RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CODON; COMPARATIVE STUDY; FUSION GENE; GENE DELETION; GENE EXPRESSION; GENE INACTIVATION; GENE MUTATION; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC CODE; GROWTH INHIBITION; HUMAN; METAGENOMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; PROTEIN SYNTHESIS; QUALITY CONTROL; RIBOSOME; RNA CLEAVAGE; RNA DEGRADATION; RNA TRANSLATION; SEGMENTAL DUPLICATION; STOP CODON; SUPPRESSOR GENE; UPREGULATION; WASTE;

CODONS; GENETIC CODE; RIBOSOME; TRANSLATION; UBIQUITIN; YEAST;

CODON; PAROMOMYCIN; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, FUNGAL; RNA, MESSENGER; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84883142045     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.039446.113     Document Type: Article

References (59)

1. 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.
2. Alexandrov A, Chernyakov I, GuW, Hiley SL, Hughes TR, Grayhack EJ, Phizicky EM. 2006. Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21: 87-96.
3. Aslanidis C, de Jong PJ. 1990. Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 18: 6069-6074.
4. Bengtson MH, Joazeiro CA. 2010. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467: 470-473.
5. Bonetti B, Fu L, Moon J, Bedwell DM. 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J Mol Biol 251: 334-345.
6. 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.
7. 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.
8. Cornish PV, Ermolenko DN, Staple DW, Hoang L, Hickerson RP, Noller HF, Ha T. 2009. Following movement of the L1 stalk between three functional states in single ribosomes. Proc Natl Acad Sci 106: 2571-2576.
9. 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.
10. Curran JF. 1995. Decoding with the A:I wobble pair is inefficient. Nucleic Acids Res 23: 683-688.
11. Curran JF, Yarus M. 1989. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J Mol Biol 209: 65-77.
12. Dang Y, Schneider-Poetsch T, Eyler DE, Jewett JC, Bhat S, Rawal VH, Green R, Liu JO. 2011. Inhibition of eukaryotic translation elongation by the antitumor natural product Mycalamide B. RNA 17: 1578-1588.
13. 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.
14. Dimitrova LN, Kuroha K, Tatematsu T, Inada T. 2009. Nascent peptidedependent translation arrest leads to Not4p-mediated protein degradation by the proteasome. J Biol Chem 284: 10343-10352.
15. Doma MK, Parker R. 2006. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440: 561-564.
16. Eberle AB, Lykke-Andersen S, Muhlemann O, Jensen TH. 2009. SMG6 promotes endonucleolytic cleavage of nonsense mRNA in human cells. Nat Struct Mol Biol 16: 49-55.
17. Fan-Minogue H, Bedwell DM. 2008. Eukaryotic ribosomal RNA determinants of aminoglycoside resistance and their role in translational fidelity. RNA 14: 148-157.
18. Fang P, Spevak CC, Wu C, Sachs MS. 2004. A nascent polypeptide domain that can regulate translation elongation. Proc Natl Acad Sci 101: 4059-4064.
19. Fei J, Kosuri P, MacDougall DD, Gonzalez RL Jr. 2008. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol Cell 30: 348-359.
20. Fei JY, Bronson JE, Hofman JM, Srinivas RL, Wiggins CH, Gonzalez RL. 2009. Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc Natl Acad Sci 106: 15702-15707.
21. 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.
22. Fujii K, Kitabatake M, Sakata T, Miyata A, Ohno M. 2009. A role for ubiquitin in the clearance of nonfunctional rRNAs. Genes Dev 23: 963-974.
23. Gatfield D, Izaurralde E. 2004. Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429: 575-578.
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. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
26. Grosjean H, de Crécy-Lagard V, Marck C. 2010. Deciphering synonymous codons in the three domains of life: Co-evolution with specific tRNA modification enzymes. FEBS Lett 584: 252-264.
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. Hinnebusch AG. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59: 407-450.
29. Huntzinger E, Kashima I, Fauser M, Saulière J, Izaurralde E. 2008. SMG6 is the catalytic endonuclease that cleaves mRNAs containing nonsense codons in metazoan. RNA 14: 2609-2617.
30. Ingolia NT, Lareau LF, Weissman JS. 2011. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147: 789-802.
31. Isken O, Maquat LE. 2007. Quality control of eukaryotic mRNA: Safeguarding cells from abnormal mRNA function. Genes Dev 21: 1833-1856.
32. Ito-Harashima S, Kuroha K, Tatematsu T, Inada T. 2007. Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev 21: 519-524.
33. 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.
34. LaRiviere FJ, Cole SE, Ferullo DJ, Moore MJ. 2006. A late-acting quality control process for mature eukaryotic rRNAs. Mol Cell 24: 619-626.
35. Letzring DP, Dean KM, Grayhack EJ. 2010. Control of translation efficiency in yeast by codon-anticodon interactions. RNA 16: 2516-2528.
36. Malkowski MG, Quartley E, Friedman AE, Babulski J, Kon Y, Wolfley J, Said M, Luft JR, Phizicky EM, DeTitta GT, et al. 2007. Blocking Sadenosylmethionine synthesis in yeast allows selenomethionine incorporation and multiwavelength anomalous dispersion phasing. Proc Natl Acad Sci 104: 6678-6683.
37. McIntosh KB, Bhattacharya A, Willis IM, Warner JR. 2011. Eukaryotic cells producing ribosomes deficient in Rpl1 are hypersensitive to defects in the ubiquitin-proteasome system. PLoS One 6: e23579.
38. Moore SD, Sauer RT. 2007. The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 76: 101-124.
39. Murphy FV, 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.
40. Nikulin A, Eliseikina I, Tishchenko S, Nevskaya N, Davydova N, Platonova O, Piendl W, Selmer M, Liljas A, Drygin D, et al. 2003. Structure of the L1 protuberance in the ribosome. Nat Struct Biol 10: 104-108.
41. Nilsson J, Sengupta J, Frank J, Nissen P. 2004. Regulation of eukaryotic translation by the RACK1 protein: A platform for signalling molecules on the ribosome. EMBO Rep 5: 1137-1141.
42. Pedersen S. 1984. Escherichia coli ribosomes translate in vivo with variable rate. EMBO J 3: 2895-2898.
43. Petitjean A, Bonneaud N, Lacroute F. 1995. The duplicated Saccharomyces cerevisiae gene SSM1 encodes a eucaryotic homolog of the eubacterial and archaebacterial L1 ribosomal proteins. Mol Cell Biol 15: 5071-5081.
44. Quartley E, Alexandrov A, Mikucki M, Buckner FS, Hol WG, DeTitta GT, Phizicky EM, Grayhack EJ. 2009. Heterologous expression of L. major proteins in S. cerevisiae: A test of solubility, purity, and gene recoding. J Struct Funct Genomics 10: 233-247.
45. Roche ED, Sauer RT. 1999. SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity. EMBO J 18: 4579-4589.
46. Schneider-Poetsch T, Ju J, Eyler DE, Dang Y, Bhat S, Merrick WC, Green R, Shen B, Liu JO. 2010. Inhibition of eukaryotic translation elongation by cycloheximide and lactimidomycin. Nat Chem Biol 6: 209-217.
47. Sherman F. 1991. Getting started with yeast. Methods Enzymol 194: 3-21.
48. Shoemaker CJ, Green R. 2012. Translation drives mRNA quality control. Nat Struct Mol Biol 19: 594-601.
49. Singh RK, Gonzalez M, Kabbaj MH, Gunjan A. 2012. Novel E3 ubiquitin ligases that regulate histone protein levels in the budding yeast Saccharomyces cerevisiae. PLoS One 7: e36295.
50. Sorensen MA, Kurland CG, Pedersen S. 1989. Codon usage determines translation rate in Escherichia coli. J Mol Biol 207: 365-377.
51. Stadler M, Fire A. 2011. Wobble base-pairing slows in vivo translation elongation in metazoans. RNA 17: 2063-2073.
52. Tanner DR, Cariello DA, Woolstenhulme CJ, Broadbent MA, Buskirk AR. 2009. Genetic identification of nascent peptides that induce ribosome stalling. J Biol Chem 284: 34809-34818.
53. Tkach JM, Yimit A, Lee AY, Riffle M, Costanzo M, Jaschob D, Hendry JA, Ou J, Moffat J, Boone C, et al. 2012. Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat Cell Biol 14: 966-976.
54. 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.
55. 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.
56. Varenne S, Buc J, Lloubes R, Lazdunski C. 1984. Translation is a nonuniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J Mol Biol 180: 549-576.
57. Wilson DN, Nierhaus KH. 2006. The E-site story: The importance of maintaining two tRNAs on the ribosome during protein synthesis. Cell Mol Life Sci 63: 2725-2737.
58. Wilson MA, Meaux S, van Hoof A. 2007. A genomic screen in yeast reveals novel aspects of nonstop mRNA metabolism. Genetics 177: 773-784.
59. Wu C, Wei J, Lin PJ, Tu L, Deutsch C, Johnson AE, Sachs MS. 2012. Arginine changes the conformation of the arginine attenuator peptide relative to the ribosome tunnel. J Mol Biol 416: 518-533.