The Ribosome-Bound Chaperones RAC and Ssb1/2p Are Required for Accurate Translation in Saccharomyces cerevisiae

REFERENCES

• Alksne, L. E., Anthony R. A., Liebman S. W., and Warner J. R.. 1993. An accuracy center in the ribosome conserved over 2 billion years. Proc. Natl. Acad. Sci. USA 90:9538–9541.
   PubMed Web of Science ®Google Scholar
• All-Robyn, J. A., Kelley-Geraghty D., Griffin E., Brown N., and Liebman S. W.. 1990. Isolation of omnipotent suppressors in an [eta+] yeast strain. Genetics 124:505–514.
   PubMedGoogle Scholar
• Ban, N., Nissen P., Hansen J., Moore P. B., and Steitz T. A.. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289:905–920.
   PubMed Web of Science ®Google Scholar
• Bidou, L., Stahl G., Hatin I., Namy O., Rousset J. P., and Farabaugh P. J.. 2000. Nonsense-mediated decay mutants do not affect programmed −1 frameshifting. RNA 6:952–961.
   PubMedGoogle Scholar
• Boeke, J. D., LaCroute F., and Fink G. R.. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345–346.
   PubMedGoogle Scholar
• Branchini, B. R., Magyar R. A., Murtiashaw M. H., and Portier N. C.. 2001. The role of active site residue arginine 218 in firefly luciferase bioluminescence. Biochemistry 40:2410–2418.
   PubMedGoogle Scholar
• Chacinska, A., Boguta M., Krzewska J., and Rospert S.. 2000. Prion-dependent switching between respiratory competence and deficiency in the yeast nam9-1 mutant. Mol. Cell. Biol. 20:7220–7229.
   PubMedGoogle Scholar
• Chernoff, Y. O., Newnam G. P., Kumar J., Allen K., and Zink A. D.. 1999. Evidence for a protein mutator in yeast: role of the Hsp70-related chaperone ssb in formation, stability, and toxicity of the [PSI] prion. Mol. Cell. Biol. 19:8103–8112.
   PubMed Web of Science ®Google Scholar
• Chernoff, Y. O., Vincent A., and Liebman S. W.. 1994. Mutations in eukaryotic 18S ribosomal RNA affect translational fidelity and resistance to aminoglycoside antibiotics. EMBO J. 13:906–913.
   PubMed Web of Science ®Google Scholar
• Christianson, T. W., Sikorski R. S., Dante M., Shero J. H., and Hieter P.. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119–122.
   PubMed Web of Science ®Google Scholar
• Craig, E. A., Eisenman H. C., and Hundley H. A.. 2003. Ribosome-tethered molecular chaperones: the first line of defense against protein misfolding? Curr. Opin. Microbiol. 6:157–162.
   PubMed Web of Science ®Google Scholar
• Dean, N. 1995. Yeast glycosylation mutants are sensitive to aminoglycosides. Proc. Natl. Acad. Sci. USA 92:1287–1291.
   PubMedGoogle Scholar
• Dresios, J., Derkatch I. L., Liebman S. W., and Synetos D.. 2000. Yeast ribosomal protein L24 affects the kinetics of protein synthesis and ribosomal protein L39 improves translational accuracy, while mutants lacking both remain viable. Biochemistry 39:7236–7244.
   PubMed Web of Science ®Google Scholar
• Eustice, D. C., Wakem L. P., Wilhelm J. M., and Sherman F.. 1986. Altered 40 S ribosomal subunits in omnipotent suppressors of yeast. J. Mol. Biol. 188:207–214.
   PubMedGoogle Scholar
• Fourmy, D., Yoshizawa S., and Puglisi J. D.. 1998. Paromomycin binding induces a local conformational change in the A-site of 16 S rRNA. J. Mol. Biol. 277:333–345.
   PubMedGoogle Scholar
• Fünfschilling, U., and Rospert S.. 1999. Nascent polypeptide-associated complex stimulates protein import into yeast mitochondria. Mol. Biol. Cell. 10:3289–3299.
   PubMedGoogle Scholar
• Gabashvili, I. S., Agrawal R. K., Grassucci R., Squires C. L., Dahlberg A. E., and Frank J.. 1999. Major rearrangements in the 70S ribosomal 3D structure caused by a conformational switch in 16S ribosomal RNA. EMBO J. 18:6501–6507.
   PubMedGoogle Scholar
• Gabashvili, I. S., Gregory S. T., Valle M., Grassucci R., Worbs M., Wahl M. C., Dahlberg A. E., and Frank J.. 2001. The polypeptide tunnel system in the ribosome and its gating in erythromycin resistance mutants of L4 and L22. Mol. Cell. 8:181–188.
   PubMed Web of Science ®Google Scholar
• Gabashvili, I. S., Whirl-Carrillo M., Bada M., Banatao D. R., and Altman R. B.. 2003. Ribosomal dynamics inferred from variations in experimental measurements. RNA 9:1301–1307.
   PubMedGoogle Scholar
• Garcia, P. D., Hansen W., and Walter P.. 1991. In vitro protein translocation across microsomal membranes of Saccharomyces cerevisiae. Methods Enzymol. 194:675–682.
   PubMedGoogle Scholar
• Gautschi, M., Just S., Mun A., Ross S., Rücknagel P., Dubaquié Y., Ehrenhofer-Murray A., and Rospert S.. 2003. The yeast Nα-acetyltransferase NatA is quantitatively anchored to the ribosome and interacts with nascent polypeptides. Mol. Cell. Biol. 23:7403–7414.
   PubMed Web of Science ®Google Scholar
• Gautschi, M., Lilie H., Fünfschilling U., Mun A., Ross S., Lithgow T., Rücknagel P., and Rospert S.. 2001. RAC, a stable ribosome-associated complex in yeast formed by the DnaK-DnaJ homologs Ssz1p and zuotin. Proc. Natl. Acad. Sci. USA 98:3762–3767.
   PubMedGoogle Scholar
• Gautschi, M., Mun A., Ross S., and Rospert S.. 2002. A functional chaperone triad on the yeast ribosome. Proc. Natl. Acad. Sci. USA 99:4209–4214.
   PubMedGoogle Scholar
• Gietz, R. D., and 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.
   PubMed Web of Science ®Google Scholar
• Gromadski, K. B., and Rodnina M. V.. 2004. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell. 13:191–200.
   PubMed Web of Science ®Google Scholar
• Haid, A., and Suissa M.. 1983. Immunochemical identification of membrane proteins after sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Methods Enzymol. 96:192–205.
   PubMedGoogle Scholar
• Hallstrom, T. C., Katzmann D. J., Torres R. J., Sharp W. J., and Moye-Rowley W. S.. 1998. Regulation of transcription factor Pdr1p function by an Hsp70 protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:1147–1155.
   PubMed Web of Science ®Google Scholar
• Hartl, F. U., and Hayer-Hartl M.. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:1852–1858.
   PubMed Web of Science ®Google Scholar
• Heitmann, J., Movva N. R., Hiestand P. C., and Hall M. N.. 1991. FK 506-binding protein proline rotamase is a target for the immunosuppressive agent FK 506 in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88:1948–1952.
   PubMedGoogle Scholar
• Hundley, H., Eisenman H., Walter W., Evans T., Hotokezaka Y., Wiedmann M., and Craig E.. 2002. The in vivo function of the ribosome-associated Hsp70, Ssz1, does not require its putative peptide-binding domain. Proc. Natl. Acad. Sci. USA 99:4203–4208.
   PubMedGoogle Scholar
• Jerinic, O., and Joseph S.. 2000. Conformational changes in the ribosome induced by translational miscoding agents. J. Mol. Biol. 304:707–713.
   PubMedGoogle Scholar
• Jones, G. W., Song Y., and Masison D. C.. 2003. Deletion of the Hsp70 chaperone gene SSB causes hypersensitivity to guanidine toxicity and curing of the [PSI+] prion by increasing guanidine uptake in yeast. Mol. Genet. Genomics 269:304–311.
   PubMedGoogle Scholar
• Kaminska, J., Tobiasz A., Gniewosz M., and Zoladek T.. 2000. The growth of mdp1/rsp5 mutants of Saccharomyces cerevisiae is affected by mutations in the ATP-binding domain of the plasma membrane H+-ATPase. Gene 242:133–140.
   PubMedGoogle Scholar
• Kandl, K. A., Munshi R., Ortiz P. A., Andersen G. R., Kinzy T. G., and Adams A. E.. 2002. Identification of a role for actin in translational fidelity in yeast. Mol. Genet. Genomics 268:10–18.
   PubMedGoogle Scholar
• Katzmann, D. J., Epping E. A., and Moye-Rowley W. S.. 1999. Mutational disruption of plasma membrane trafficking of Saccharomyces cerevisiae Yor1p, a homologue of mammalian multidrug resistance protein. Mol. Cell. Biol. 19:2998–3009.
   PubMedGoogle Scholar
• Kurland, C. G. 1992. Translational accuracy and the fitness of bacteria. Annu. Rev. Genet. 26:29–50.
   PubMedGoogle Scholar
• Kushnirov, V. V., and Ter-Avanesyan M. D.. 1998. Structure and replication of yeast prions. Cell 94:13–16.
   PubMed Web of Science ®Google Scholar
• Masurekar, M., Palmer E., Ono B. I., Wilhelm J. M., and Sherman F.. 1981. Misreading of the ribosomal suppressor SUP46 due to an altered 40 S subunit in yeast. J. Mol. Biol. 147:381–390.
   PubMedGoogle Scholar
• Namy, O., Duchateau-Nguyen G., Hatin I., Hermann-Le Denmat S., Termier M., and Rousset J. P.. 2003. Identification of stop codon readthrough genes in Saccharomyces cerevisiae. Nucleic Acids Res. 31:2289–2296.
   PubMed Web of Science ®Google Scholar
• Namy, O., Hatin I., and Rousset J. P.. 2001. Impact of the six nucleotides downstream of the stop codon on translation termination. EMBO Rep. 2:787–793.
   PubMed Web of Science ®Google Scholar
• Nelson, R. J., Ziegelhoffer T., Nicolet C., Werner-Washburne M., and Craig E. A.. 1992. The translation machinery and 70 kd heat shock protein cooperate in protein synthesis. Cell 71:97–105.
   PubMedGoogle Scholar
• O'Connor, M., and Dahlberg A. E.. 1995. The involvement of two distinct regions of 23 S ribosomal RNA in tRNA selection. J. Mol. Biol. 254:838–847.
   PubMedGoogle Scholar
• Ogle, J. M., Carter A. P., and Ramakrishnan V.. 2003. Insights into the decoding mechanism from recent ribosome structures. Trends Biochem. Sci. 28:259–266.
   PubMed Web of Science ®Google Scholar
• Ogle, J. M., Murphy F. V., Tarry M. J., and Ramakrishnan V.. 2002. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111:721–732.
   PubMed Web of Science ®Google Scholar
• Osherovich, L. Z., and Weissman J. S.. 2002. The utility of prions. Dev. Cell. 2:143–151.
   PubMed Web of Science ®Google Scholar
• Palmer, E., Wilhelm J. M., and Sherman F.. 1979. Phenotypic suppression of nonsense mutants in yeast by aminoglycoside antibiotics. Nature 277:148–150.
   PubMedGoogle Scholar
• Pfund, C., Lopez-Hoyo N., Ziegelhoffer T., Schilke B. A., Lopez-Buesa P., Walter W. A., Wiedmann M., and Craig E. A.. 1998. The molecular chaperone Ssb from Saccharomyces cerevisiae is a component of the ribosome-nascent chain complex. EMBO J. 17:3981–3989.
   PubMedGoogle Scholar
• Puglisi, J. D., Blanchard K. D., Dahlquist R. G. E., Eason R. G., Fourmy D., Lynch S. R., Recht M. I., and Yoshizawa S.. 2000. Aminoglycoside antibiotics and decoding, p. 419–429. In Garrett R. A., Douthwaite S. R., Liljas A., Matheson P. B., Moore P. B., and Noller H. F. (ed.), The ribosome: structure, function, antibiotics, and cellular interactions. ASM Press, Washington, D.C.
   Google Scholar
• Recht, M. I., Douthwaite S., and Puglisi J. D.. 1999. Basis for prokaryotic specificity of action of aminoglycoside antibiotics. EMBO J. 18:3133–3138.
   PubMedGoogle Scholar
• Rodnina, M. V., Daviter T., Gromadski K., and Wintermeyer W.. 2002. Structural dynamics of ribosomal RNA during decoding on the ribosome. Biochimie 84:745–754.
   PubMedGoogle Scholar
• Rodnina, M. V., Pape T., Savelsbergh A., Mohr D., Matassova N. B., and Wintermeyer W.. 2000. Mechanisms of partial reactions of the elongation cycle catalyzed by elongation factors Tu and G, p. 301–317. In Garrett R. A., Douthwaite S. R., Liljas A., Matheson P. B., Moore P. B., and Noller H. F. (ed.), The ribosome: structure, function, antibiotics, and cellular interactions. ASM Press, Washington, D.C.
   Google Scholar
• Rodnina, M. V., and Wintermeyer W.. 2001. Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annu. Rev. Biochem. 70:415–435.
   PubMed Web of Science ®Google Scholar
• Rospert, S. 2004. Ribosome function: how to govern the fate of a nascent polypeptide. Curr. Biol. 14:R386–R388.
   PubMedGoogle Scholar
• Rospert, S., Gautschi M., Rakwalska M., and Raue U.. 2004. Ribosome-bound proteins acting on newly synthesized polypeptide chains. In Buchner J. and Kiefhaber T. (ed.), Handbook in protein folding, vol. II. in press. Wiley-VCH Verlag GmbH & Co., Weinheim, Germany.
   Google Scholar
• Ruggero, D., and Londei P.. 1996. Differential antibiotic sensitivity determined by the large ribosomal subunit in thermophilic archaea. J. Bacteriol. 178:3396–3398.
   PubMedGoogle Scholar
• Schägger, H., and von Jagow G.. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368–379.
   PubMed Web of Science ®Google Scholar
• Sherman, F., Fink G. R., and Hicks J. B.. 1986. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, New York, N.Y.
   Google Scholar
• Siegers, K., Bolter B., Schwarz J. P., Bottcher U. M., Guha S., and Hartl F. U.. 2003. TRiC/CCT cooperates with different upstream chaperones in the folding of distinct protein classes. EMBO J. 22:5230–5240.
   PubMedGoogle Scholar
• Singh, A., Ursic D., and Davies J.. 1979. Phenotypic suppression and misreading Saccharomyces cerevisiae. Nature 277:146–148.
   PubMed Web of Science ®Google Scholar
• Stahl, G., Bidou L., Rousset J. P., and Cassan M.. 1995. Versatile vectors to study recoding: conservation of rules between yeast and mammalian cells. Nucleic Acids Res. 23:1557–1560.
   PubMedGoogle Scholar
• Stansfield, I., Jones K. M., Herbert P., Lewendon A., Shaw W. V., and Tuite M. F.. 1998. Missense translation errors in Saccharomyces cerevisiae. J. Mol. Biol. 282:13–24.
   PubMed Web of Science ®Google Scholar
• Synetos, D., Frantziou C. P., and Alksne L. E.. 1996. Mutations in yeast ribosomal proteins S28 and S4 affect the accuracy of translation and alter the sensitivity of the ribosomes to paromomycin. Biochim. Biophys. Acta 1309:156–166.
   PubMedGoogle Scholar
• True, H. L., and Lindquist S. L.. 2000. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407:477–483.
   PubMed Web of Science ®Google Scholar
• Tuite, M. F., and Lindquist S. L.. 1996. Maintenance and inheritance of yeast prions. Trends Genet. 12:467–471.
   PubMedGoogle Scholar
• Wach, A., Brachat A., Pohlmann R., and Philippsen P.. 1994. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10:1793–1808.
   PubMed Web of Science ®Google Scholar
• Wakem, L. P., and Sherman F.. 1990. Isolation and characterization of omnipotent suppressors in the yeast Saccharomyces cerevisiae. Genetics 124:515–522.
   PubMedGoogle Scholar
• Wegrzyn, R. D., Bapat K., Newnam G. P., Zink A. D., and Chernoff Y. O.. 2001. Mechanism of prion loss after Hsp104 inactivation in yeast. Mol. Cell. Biol. 21:4656–4669.
   PubMed Web of Science ®Google Scholar
• Wickner, R. B., Taylor K. L., Edskes H. K., Maddelein M. L., Moriyama H., and Roberts B. T.. 2000. Prions of yeast as heritable amyloidoses. J. Struct. Biol. 130:310–322.
   PubMed Web of Science ®Google Scholar
• Woolhead, C. A., McCormick P. J., and Johnson A. E.. 2004. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 116:725–736.
   PubMed Web of Science ®Google Scholar
• Yan, W., Schilke B., Pfund C., Walter W., Kim S., and Craig E. A.. 1998. Zuotin, a ribosome-associated DnaJ molecular chaperone. EMBO J. 17:4809–4817.
   PubMed Web of Science ®Google Scholar