Abstract
The combination of genetic, molecular and biochemical approaches have made the yeastSaccharomyces cerevisiae a convenient organism to study translation. The sequence similarity of translation factors from yeast and other organisms suggests a high degree of conservation in the translational machineries. This view is also strengthened by a functional analogy of some proteins implicated in translation. Beautiful genetic experiments have confirmed existing models and added new insights in the mechanism of translation. This review summarizes recent experiments using yeast as a model system for the analysis of this complex process.
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Abastado JP, Miller PF, Jackson BM & Hinnebusch AG (1991) Suppression of ribosomal reinitiation at upstream open reading frames in amino acid-starved cells forms the basis forGCN4 translational control. Mol. Cell. Biol. 11: 486–496
Altmann M & Trachsel H (1989) Altered mRNA cap recognition activity of initiation factor 4E in the yeast cell cycle division mutant cdc33. Nucleic Acids Res. 17: 5923–5931
Altmann M, Edery I, Sonenberg N & Trachsel H (1985) Purification and characterization of protein synthesis initiation factor eIF-4E from the yeastSaccharomyces cerevisae. Biochem. 24: 6085–6089
Altmann M, Handschin C & Trachsel H (1987) mRNA cap-binding protein: cloning of the gene encoding protein synthesis initiation factor eIF-4E fromSaccharomyces cerevisae. Mol. Cell. Biol. 7: 998–1003
Altmann M, Edery I, Trachsel H & Sonenberg N (1988) Site-directed mutagenesis of the tryptophan residues in yeast eukaryotic initiation factor 4E. Effects on cap binding activity. J. Biol. Chem. 263: 17229–17232
Altmann M, Krieger M & Trachsel H (1989a) Nucleotide sequence of the gene encoding a 20 kDa protein associated with the cap binding protein eIF-4E fromSaccharomyces cerevisae. Nucleic Acids Res. 17: 7520
Altmann M, Müller PP, Pelletier J, Sonenberg N & Trachsel H (1989b) A mammalian translation initiation factor can substitute for its yeast homologuein vivo. J. Biol. Chem. 264: 12145–12147
Altmann M, Sonenberg N & Trachsel H (1989c) Translation inSaccharomyces cerevisae: initiation factor 4E-dependent cell-free system. Mol. Cell. Biol. 9: 4467–4472
Altmann M, Blum S, Wilson TMA & Trachsel H (1990) The 5′-leader sequence of tobacco mosaic virus RNA mediates initiation-factor-4E-independent, but still initiation-factor-4A-dependent translation in yeast extracts. Gene 91: 127–129
Baim SB & Sherman F (1988) mRNA structures influencing translation in the yeastSaccharomyces cerevisae. Mol. Cell. Biol. 8: 1591–1601
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
Bennetzen JL & Hall BD (1982) Codon selection in yeast. J. Biol. Chem. 257: 3026–3031
Blum S, Mueller M, Schmid SR, Linder P & Trachsel H (1989) Translation inSaccharomyces cerevisae: initiation factor 4A-dependent cell-free system. Proc. Natl. Acad. Sci. USA 86: 6043–6046
Brenner C, Nakayama N, Goebl M, Tanaka K, Toh-e A & Matsumoto K (1988) CDC33 encodes mRNA cap-binding protein eIF-4E ofSaccharomyces cerevisae. Mol. Cell. Biol. 8: 3556–3559
Brown CM, Stockwell PA, Trotman CN & Tate WP (1990) Sequence analysis suggests that tetra-nucleotides signal the termination of protein synthesis in eukaryotes. Nucleic Acids Res. 18: 6339–6345
Burke DJ & Church D (1991) Protein synthesis requirements for nuclear division, cytokinesis, and cell separation inSaccharomyces cerevisae. Mol. Cell. Biol. 11: 3691–3698
Capieaux E, Vignais ML, Sentenac A & Goffeau A (1989) The yeast H+-ATPase gene is controlled by the promoter binding factor TUF. J. Biol. Chem. 264: 7437–7446
Chen JJ, Throop MS, Gehrke L, Kuo I, Pal JK, Brodsky M & London IM (1991) Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2a (eIF-2a) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF-2 alpha kinase. Proc. Natl. Acad. Sci. USA 88: 7729–7733
Chen JY & Bodley JW (1988) Biosynthesis of diphthamide inSaccharomyces cerevisiae. Partial purification and characterization of a specific S-adenosylmethionine: elongation factor 2 methyltransferase. J. Biol. Chem. 263: 11692–11696
Chen JY, Bodley JW & Livingston DM (1985) Diphtheria toxin-resistant mutants ofSaccharomyces cerevisae. Mol. Cell. Biol. 5: 3357–3360
Cigan AM & Donahue TF (1987) Sequence and structural features associated with translational initiator regions in yeast—a review. Gene 59: 1–18
Cigan AM, Feng L & Donahue TF (1988) tRNAi(met) functions in directing the scanning ribosome to the start site of translation. Science 242: 93–97
Cigan AM, Pabich EK & Donahue TF (1988) Mutational analysis of theHIS4 translational initiator region inSaccharomyces cerevisae. Mol. Cell. Biol. 8: 2964–2975
Cigan AM, Pabich EK, Feng L & Donahue TF (1989) Yeast translation initiation suppressorsui2 encodes the a subunit of eukaryotic initiation factor 2 and shares sequence identity with the human a subunit. Proc. Natl. Acad. Sci. USA 86: 2784–2788
Cigan AM, Foiani M, Hannig EM & Hinnebusch AG (1991) Complex formation by positive and negative translational regulators ofGCN4. Mol. Cell. Biol. 11: 3217–3228
Cottrelle P, Cool M, Thuriaux P, Price VL, Thiele D, Buhler JM & Fromageot P (1985a) Either one of the two yeast EF-1 alpha genes is required for cell viability. Curr. Genet. 9: 693–697
Cottrelle P, Thiele D, Price VL, Memet S, Micouin JY, Marck C, Buhler JM, Sentenac A & Fromageot P (1985b) Cloning, nucleotide sequence, and expression of one of two genes coding for yeast elongation factor 1 alpha. J. Biol. Chem. 260: 3090–3096
Crouzet M & Tuite MF (1987) Genetic control of translational fidelity in yeast: molecular cloning and analysis of the allosuppressor geneSAL3. Mol. Gen. Genet. 210: 581–583
Crouzet M, Izgu F, Grant CM & Tuite MF (1988) The allosuppressor geneSAL4 encodes a protein important for maintaining translational fidelity inSaccharomyces cerevisae. Curr. Genet. 14: 537–43
Dever TE, Costello CE, Owens CL, Rosenberry TL & Merrick WC (1989) Location of seven post-translational modifications in rabbit elongation factor 1 alpha including dimethyllysine, trimethyllysine, and glycerylphosphorylethanolamine. J. Biol. Chem. 264: 20518–20525
Dieckmann CL, Homison G & Tzagoloff A (1984) Assembly of the mitochondrial membrane system. Nucleotide sequence a yeast nuclear gene (CBP1) involved in 5′ end processing cytochrome b pre-mRNA. J. Biol. Chem. 259: 4732–4738
Donahue TF, Cigan AM, Pabich EK & Castilho Valavicius B (1988) Mutations at a Zn(II) finger motif in the yeast eIF-2β gene alter ribosomal start-site selection during the scanning process. Cell 54: 621–632
Edery I, Humbelin M, Darveau A, Lee KAW, Milburn S, Hershey JWB, Trachsel H & Sonenberg N (1983) Involvement of eukaryotic initiation factor 4A in the cap recognition process. J. Biol. Chem. 258: 11398–11403
Feinberg B, McLaughlin CS & Moldave K (1982) Analysis of temperature-sensitive mutant ts 187 ofSaccharomyces cerevisae altered in a component required for the initiation of protein synthesis. J. Biol. Chem. 257: 10846–10851
Foiani M, Cigan AM, Paddon CJ, Harashima S & Hinnebusch AG (1991)GCD2, a translational repressor of the GCN4 gene, has a general function in the initiation of protein synthesis inSaccharomyces cerevisae. Mol. Cell. Biol. 11: 3203–3216
Gasior E, Herrera F, Sadnik I, McLaughlin CS & Moldave K (1979) The preparation and characterization of a cell-free system fromSaccharomyces cerevisae that translates natural messenger ribonucleic acid. J. Biol. Chem. 254: 3965–3969
Goyer C, Altmann M, Trachsel H & Sonenberg N (1989) Identification and characterization of cap-binding proteins from yeast. J. Biol. Chem. 264: 7603–7610
Hartwell BLH & McLaughlin CS (1968a) A mutant of yeast apparently defective in the initiation of protein synthesis. Biochem. 62: 468–474
Hartwell LH & McLaughlin CS (1968b) Temperature-sensitive mutants of yeast exhibiting a rapid inhibition of protein synthesis. J. Bacteriol. 96: 1664–1671
Hershey JWB (1989) Protein phosphorylation controls translation rates. J. Biol. Chem. 264: 20823–20826
Hershey JWB, Smit-McBride Z & Schnier J (1990) The role of mammalian initiation factor eIF-4D and its hypusine modification in translation. Biochim. Biophys. Acta 1050: 160–162
Hinnebusch AG (1988) Mechanisms of gene regulation in the general control of amino acid biosynthesis inSaccharomyces cerevisae. Microbiol. Rev. 52: 248–273
Hoekema A, Kastelein RA, Vasser M & de Boer HA (1987) Codon replacement in the PGK1 gene ofSaccharomyces cerevisae: experimental approach to study the role of biased codon usage in gene expression. Mol. Cell. Biol. 7: 2914–2924
Jackson R (1991) The ATP requirement for initiation of eukaryotic translation varies according to the mRNA species. Eur. J. Biochem. 200: 285–294
Jaramillo M, Browning K, Dever TE, Blum S, Trachsel H, Merrick WC, Ravel JM & Sonenberg N (1990) Translation initiation factors that function as RNA helicases from mammals, plants and yeast. Biochim. Biophys. Acta 1050: 134–139
Kikuchi Y, Shimatake H & Kikuchi A (1988) A yeast gene required for the G1-to-S transition encodes a protein containing an A-kinase target site and GTPase domain. EMBO J. 7: 1175–1182
Kozak M (1978) How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell 15: 1109–1123
Kozak M (1989) The scanning model for translation: an update. J. Cell Biol. 108: 229–241
Kushnirov VV, Ter AMD, Telckov MV, Surguchov AP, Smirnov VN & Inge VSG (1988) Nucleotide sequence of theSUP2 (SUP35) gene ofSaccharomyces cerevisae. Gene 66: 45–54
Linder P & Prat A (1990) Baker's yeast, the new work horse in protein synthesis studies: analyzing eukaryotic translation initiation. BioEssays 12: 519–526
Linder P & Slonimski PP (1989) An essential yeast protein, encoded by duplicated genesTIF1 andTIF2 and homologous to the mammalian translation initiation factor eIF-4A, can suppress a mitochondrial missense mutation. Proc. Natl. Acad. Sci. USA 86: 2286–2290
Linder P, Lasko PF, Ashburner M, Leroy P, Nielsen PJ, Nishi K, Schnier J & Slonimski PP (1989) Birth of the D-E-A-D box. Nature 337: 121–122
Losson R, Fuchs RPP & Lacroute F (1983)In vivo transcription of eukaryotic regulatory gene. EMBO J. 2: 2179–2184
Maicas E, Shago M & Friesen JD (1990) Translation of theSaccharomyces cerevisae tcml gene in the absence of a 5′-untranslated leader. Nucleic Acids Res. 18: 5823–5828
McIntosh EM & Haynes RH (1986) Sequence and expression of the dCMP deaminase gene (DCD1) ofSaccharomyces cerevisae. Mol. Cell. Biol. 6: 1711–1721
Mehta KD, Leung D, Lefebvre L & Smith M (1990) The ANB1 locus ofSaccharomyces cerevisae encodes the protein synthesis initiation factor eIF-4D. J. Biol. Chem. 265: 8802–8807
Miller PF & Hinnebusch AG (1989) Sequences that surround the stop codons of upstream open reading frames inGCN4 mRNA determine their distinct functions in translational control. Genes Dev. 3: 1217–1225
Moldave K (1985) Eukaryotic protein synthesis. Ann. Rev. Biochem. 54: 1109–1149
Mueller PP & Hinnebusch AG (1986) Multiple upstream AUG codons mediate translational control ofGCN4. Cell 45: 201–207
Nagata S, Nagashiman K, Tsunetsugu-Yokota Y, Fujimura K, Miyazaki M & Kaziro Y (1984) Polypeptide chain elongation factor 1α (EF-1α from yeast: nucleotide sequence of one of the two genes for EF-1α fromSaccharomyces cerevisiae. EMBO J. 3: 1825–1830
Najarian D, Dihanich ME, Martin NC & Hopper AK (1987) DNA sequence and transcript mapping of MOD5: features of the 5′ region which suggest two translational starts. Mol. Cell. Biol. 7: 185–191
Omura F, Kohno K & Uchida T (1989) The histidine residue of codon 715 is essential for function of elongation factor 2. Eur. J. Biochem. 180: 1–8
Perentesis JP, Phan LD, Gleason WB, LaPorte DC, Livingston DM & Bodley JW (1991)Saccharomyces cerevisae elongation factor 2: genetic cloning, characterization of expression, and G-domain modeling. J. Biol. Chem. 267: 1190–1197
Prat A, Schmid SR, Buser P, Blum S, Trachsel H, Nielsen PJ & Linder P (1990) Expression of translation initiation factor 4A from yeast and mouse inSaccharomyces cerevisae. Biochim. Biophys. Acta 1050: 140–145
Qin SL, Moldave K & McLaughlin CS (1987) Isolation of the yeast gene encoding elongation factor 3 for protein synthesis. J. Biol. Chem. 262: 7802–7807
Qin SL, Xie AG, Bonato MC & McLaughlin CS (1990) Sequence analysis of the translational elongation factor 3 fromSaccharomyces cerevisae. J. Biol. Chem. 265: 1903–1912
Rhoads RE (1988) Cap recognition and the entry of mRNA into the protein synthesis initiation cycle. Trends Biochem. Sci. 13: 52–56
Riis B, Rattan SIS, Clark BFC & Merrick WC (1990) Eukaryotic protein elongation factors. Trends Biochem. Sci. 15: 420–424
Rozen F, Edery I, Meerovitch K, Dever TE, Merrick WC & Sonenberg N (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 10: 1134–1144
Ryazanov AG, Shestakova EA & Natapov PG (1988) Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature 334: 170–173
Sachs AB (1990) Isolation of thelsd mutations inSaccharomyces cerevisae. In: McCarthy JEG & Tuite MF (Eds) Post-transcriptional Control of Gene Expression (pp 549–555). NATO ASI Series, Springer-Verlag, Berlin
Sachs AB & Davis RW (1989) The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunit-dependent translation initiation. Cell 58: 857–867
Sachs AB & Davis RW (1990) Translation initiation and ribosomal biogenesis: involvement of a putative rRNA helicase andRPL46. Science 247: 1077–1079
Sandbaken MG & Culbertson MR (1988) Mutations in elongation factor EF-1 alpha affect the frequency of frameshifting and amino acid misincorporation inSaccharomyces cerevisae. Genetics 120: 923–934
Sandbaken MG, Lupisella JA, DiDomenico B & Charkraburtty K (1990) Protein synthesis in yeast. J. Biol. Chem. 265: 15838–15844
Schirmaier F & Philippsen P (1984) Identification of two genes coding for the translation elongation factor EF-1α ofS. cerevisiae. EMBO J. 3: 3311–3315
Schmid SR & Linder P (1991) Translation initiation factor 4A fromSaccharomyces cerevisae: analysis of residues conserved in the D-E-A-D family of RNA helicases. Mol. Cell. Biol. 11: 3463–3471
Schmid SR & Linder P (1992) D-E-A-D protein family of putative RNA helicases. Mol. Microbiol. 6: 283–292
Schnier J, Schwelberger HG, Smit-McBride Z, Ah Kang H & Hershey JWB (1991) Translation initiation factor 5A and its hypusine modification are essential for cell viability in the yeastSaccharomyces cerevisae. Mol. Cell. Biol. 11: 3105–3114
Sharp PM & Bulmer M (1988) Selective differences among translation termination codons. Gene 63: 141–145
Sharp PM, Tuohy TM & Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res. 14: 5125–5143
Sherman F (1982) Suppression in the yeastSaccharomyces cerevisae. In: Strathern JN, Jones EW & Broach JR (Eds) The Molecular Biology of the Yeast Saccharomyces. Metabolism and Gene Expression (pp 463–486). Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Slobin LI (1980) The role of eucaryotic factor Tu in protein synthesis. The measurement of the elongation factor Tu content of rabbit reticulocytes and other mammalian cells by a sensitive radioimmunoassay. Eur. J. Biochem. 110: 555–563
Sonenberg N (1988) Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation. Prog. Nucleic Acid Res. Mol. Biol. 35: 173–207
Sonenberg N & Pelletier J (1989) Poliovirus translation: a paradigm for a novel initiation mechanism. BioEssays 11: 128–132
Song JM, Picologlou S, Grant CM, Firoozan M, Tuite MF & Liebman S (1989) Elongation factor EF-1 alpha gene dosage alters translational fidelity inSaccharomyces cerevisae. Mol. Cell. Biol. 9: 4571–4575
Strick CA & Fox TD (1987)Saccharomyces cerevisae positive regulatory genePET111 encodes a mitochondrial protein that is translated from an mRNA with a long 5′ leader. Mol. Cell. Biol. 7: 2728–2734
Surguchov AP (1988) ‘Omnipotent’ nonsense suppressors: new clues to an old puzzle. TIBS 13: 120–123
Trachsel H (1991). Translation in Eukaryotes. CRC Press, Boca Raton, Ann Arbor, Boston and London
Tuite MF (1989) Protein synthesis. In: Rose AH & Harrison JS (Eds) The Yeasts (pp 161–204). Academic Press, NY
van den Heuvel JJ, Bergkamp RJ, Planta RJ & Raue HA (1989) Effect of deletions in the 5′-noncoding region on the translational efficiency of phosphoglycerate kinase mRNA in yeast. Gene 79: 83–95
van den Heuvel JJ, Planta RJ & Raue HA (1990) Effect of leader primary structure on the translational efficiency of phosphoglycerate kinase mRNA in yeast. Yeast 6: 473–482
Warner JR (1989) Synthesis of ribosomes inSaccharomyces cerevisae. Microbiol. Rev. 53: 256–271
Wek RC, Jackson BM & Hinnebusch AG (1989) Juxtaposition of domains homologous to protein kinases and histidyl-tRNA synthetases in GCN2 protein suggests a mechanism for coupling GCN4 expression to amino acid availability. Proc. Natl. Acad. Sci. USA 86: 4579–4583
Werner M, Feller A, Messenguy F & Piérard A (1987) The leader peptide of yeast gene CPA1 is essential for the translational repression of its expression. Cell 49: 805–813
Williams NP, Hinnebusch AG & Donahue TF (1989) Mutations in the structural genes for eukaryotic initiation factors 2 alpha and 2 beta ofSaccharomyces cerevisae disrupt translational control of GCN4 mRNA. Proc. Natl. Acad. Sci. USA 86: 7515–7519
Wilson PG & Culbertson MR (1988) SUF12 suppressor protein of yeast. A fusion protein related to the EF-1 family of elongation factors. J. Mol. Biol. 199: 559–573
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Linder, P. Molecular biology of translation in yeast. Antonie van Leeuwenhoek 62, 47–62 (1992). https://doi.org/10.1007/BF00584462
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DOI: https://doi.org/10.1007/BF00584462