Skip to main content

The secret life of the ribosome

  • Chapter
Book cover Accuracy in Molecular Processes

Abstract

We begin by admitting that it is not yet possible to describe in molecular detail how ribosomes carry out the accurate translation of a messenger RNA. Indeed, there is still some question about how accurate protein synthesis really is. Nevertheless, some recent developments have provided unexpected insights into the origin and containment of translation errors. The principal thrust of recent work has been to explore the interpretation that the errors of translation and the strategies to contain them are of an essentially kinetic character. This notion can be motivated on at least two levels.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andersson, D. and Kurland, C. G. (1983) Ram ribosomes are defective proofreaders. Mol. Gen. Genet., 191, 378–381.

    Article  Google Scholar 

  • Andersson, S. G. E., Buckingham, R. H. and Kurland, C. G. (1984) Does codon-composition influence ribosome function? EMBO J., 3, 91–94.

    Google Scholar 

  • Atkins, J. F., Elseviers, D. and Gorini, L. (1972) Low activity galactosidase in frameshift mutants of Escherichia coli. Proc. Natl Acad. Sci. USA, 69, 1192–1195.

    Article  Google Scholar 

  • Atkins, J. F., Gesteland, R. F., Ried, B. R. and Anderson, C. W. (1979) Normal tRNAs promote ribosomal frameshifting. Cell, 18, 1119–1131.

    Article  Google Scholar 

  • Barnett, L., Brenner, S., Crick, F. H. C., Shulman, R. G. and Watts-Tobin, R. J. (1967) Phase-shift and other mutants in the first part of the r II B cistron of bacteriophage T4. Phil. Trans. Royal Soc. B, 252, 387–560.

    Article  Google Scholar 

  • Blomberg, C. and Ehrenberg, M. (1981) Energy considerations for kinetic proofreading in biosynthesis. J. Theor. Biol., 88, 631–670.

    Article  Google Scholar 

  • Blomberg, C., Ehrenberg, M. and Kurland, C. G. (1980) Free-energy dissipation constraints of the accuracy of enzymatic selections. Quart. Rev. Biophys., 13, 231–254.

    Article  Google Scholar 

  • Böck, A., Fairman, L. E. and Neidhardt, F. C. (1966) Biochemical and genetic characterization of a mutant of Escherichia coli with a temperature-sensitive valyl ribonucleic acid synthetase. J. Bacteriol., 92, 1076–1082.

    Google Scholar 

  • Bohman, K. T., Ruusala, T., Jelenc, P. C. and Kurland, C. G. (1984) Hyper-accurate ribosomes inhibit growth. Mol. Gen. Genet., 198, 90–99.

    Article  Google Scholar 

  • Bossi, L. (1983) Context effects: translation of UAG codon by suppressor tRNA is affected by the sequence following UAG in the message. J. Mol. Biol., 164, 73–87.

    Article  Google Scholar 

  • Bossi, L. and Roth, J. R. (1980) The influence of codon contest on genetic code translation. Nature, 286, 123 - 127.

    Article  Google Scholar 

  • Bouadloun, F., Donner, D. and Kurland, C. G. (1983) Codon-specific missense errors in vivo. EMBO J., 2, 1351–1356.

    Google Scholar 

  • Buckingham, R. H. and Kurland, C. G. (1977) Codon specificity of UGA suppressor tryptophan tRNA from E. coli. Proc. Natl Acad. Sci. USA, 74, 5496–5499.

    Google Scholar 

  • Crick, F. H. C. (1958) On protein synthesis. Symp. Soc. Exp. Biol. XII, 138–163.

    Google Scholar 

  • Crick, F. H. C. (1966) Codon-anticodon pairing: the wobble hypothesis. J. Mol. Biol., 19, 548–555.

    Article  Google Scholar 

  • Crick, F. H. C., Barnett, L., Brenner, S. and Watts-Tobin, R. J. (1961) The general nature of the genetic code for proteins. Nature, 192, 1227–1232.

    Article  Google Scholar 

  • De Wilde, M., Cabezon, T., Herzog, A. and Bollen, A. (1977) Apport de la génétique à la connaissance du ribosome bactérien. Biochimie, 59, 125–140.

    Article  Google Scholar 

  • Edelmann, P. and Gallant, J. (1977) Mistranslation in E. coli. Cell, 10, 131–137.

    Google Scholar 

  • Ehrenberg, M. and Blomberg, C. (1980) Thermodynamic constraints on kinetic proofreading in biosynthetic pathways. Biophys. J., 31, 333–358.

    Article  Google Scholar 

  • Ehrenberg, M. and Kurland, C. G. (1984) Costs of accuracy determined by a maximal growth rate constraint. Quart. Rev. Biophys., 17, 45–82.

    Article  Google Scholar 

  • Ellis, N. and Gallant, J. (1982) An estimate of the global error frequency in translation. Mol. Gen. Genet., 188, 169–172.

    Article  Google Scholar 

  • Fluck, M. M., Salser, W. and Epstein, R. H. (1977) The influence of the reading context upon the suppression of nonsense codons. Mol. Gen. Genet., 151, 137–149.

    Article  Google Scholar 

  • Gallant, J. (1979) Stringent control in E. coli. Ann. Rev. Genetics, 13, 393–415.

    Article  Google Scholar 

  • Gallant, J. and Foley, D. (1980) On the causes and prevention of mistranslation. In Ribosomes, Structure and Function, and Genetics (eds G. Chambliss, G. R. Craven, J. Davies, K. Davis, L. Kahan and M. Nomura ), University Park Press, Baltimore, pp. 615–638.

    Google Scholar 

  • Gallant, J., Erlich, H., Weiss, R., Palmer, L., and Nyari, L. (1982) Nonsense suppression in aminoacyl-tRNA limited cells. Mol. Gen. Genet., 186, 221–226.

    Article  Google Scholar 

  • Gallant, J. and Palmer, L. (1979). Error propagation in viable cells. Mech. Ageing Dev., 10, 27–38.

    Article  Google Scholar 

  • Gallant, J., Weiss, R., Murphy, J. and Brown, M. (1985) Some puzzles of translational accuracy. In The Molecular Biology for Bacterial Growth (eds M. Schaechter, F. Neidhardt and J. Ingraham ), Barlett and Jones, Boston, Mass.

    Google Scholar 

  • Garen, A. and Siddiqi, O. (1962) Suppression of mutations in the alkaline phosphatase structure cistron of E. coli. Proc. Natl Acad. Sei. USA, 48, 1121–1126.

    Article  Google Scholar 

  • Gorini, L. (1974) Streptomycin and misreading of the genetic code. In Ribosome (eds M. Nomura, A. Tissieres, and P. Lengy) Cold Spring Harbor Laboratory, New York, pp. 791–804.

    Google Scholar 

  • Hall, B. and Gallant, J. (1972) Defective translation in RC cells. Nature New Biol., 237, 131–135.

    Google Scholar 

  • Hirsh, D. (1973) Tryptophan transfer RNA as the UGA suppressor. J. Mol. Biol., 58, 439–458.

    Article  Google Scholar 

  • Hopfield, J. J. (1974) Kinetic proofreading. Proc. Natl Acad. Sei. USA, 71, 4135–4141.

    Article  Google Scholar 

  • Jelenc, P. C. and Kurland, C. G. (1979) Nucleoside triphosphate regeneration decreases the frequency of translation errors. Proc. Natl Acad. Sei. USA, 76, 3174–3178.

    Article  Google Scholar 

  • Jelenc, P. C. and Kurland, C. G. (1984) Multiple effects of kanamycin on translational accuracy. Mol. Gen. Genet., 194, 195–199.

    Article  Google Scholar 

  • Kaziro, Y. (1978) The role of guanosine 5’-triphosphate in polypeptide chain elongation. Biochim. Biophys. Acta, 505, 95–112.

    Google Scholar 

  • Kornberg, A. (1969) Active Center of DNA polymerase. Science, 163: 1410–1414.

    Article  Google Scholar 

  • Kuhlberger, R., Piepersberg, W., Petzet, A., Buckel, P. and Böck, A. (1979) Alteration of ribosomal protein L6 in gentamycin resistant strains Escherichia coli. Effects on fidelity of protein synthesis. Biochemistry, 18, 187–193.

    Article  Google Scholar 

  • Kurland, C. G. (1978) Role of guanine nucleotide in protein biosynthesis. Biophys. J., 22, 373–392.

    Article  Google Scholar 

  • Kurland, C. G. (1979) Reading frame errors on ribosomes. In Nonsense Mutations and tRNA Suppressors (eds J. E. Celis and J. D. Smith ), Academic Press, London, pp. 97 - 108.

    Google Scholar 

  • Kurland, C. G. (1983) Accuracy strategies. Biochem. Soc. Symp., 47, 1–9.

    Google Scholar 

  • Kurland, C. G. and Ehrenberg, M. (1984). Optimization of translational accuracy. Progr. Nud. Acid Res. Mol. Biol., 31, 191–219.

    Article  Google Scholar 

  • Kurland, C. G., Andersson, D. I., Andersson, S. G. E., Bohman, K., Bouadloun, F., Ehrenberg, M., Jelenc, P. C. and Ruusala, T. (1984) Translational accuracy and bacterial growth. In Alfred Benzon Symposium 19, Gene expression (eds B. F. C. Clark and H. V. Peterson ), Munksgaard, Copenhagen, pp. 193–207.

    Google Scholar 

  • Kurland, C. G., Rigler, R., Ehrenberg, M. and Blomberg, C. (1975) Allosteric mechanism for codon-dependent tRNA selection on ribosomes. Proc. Natl Acad. Sci. USA, 72, 4248–4251.

    Article  Google Scholar 

  • Laffler, T. and Gallant, J. (1974) Stringent control of protein synthesis in E. coli. Cell, 3, 47–49.

    Google Scholar 

  • Langridge, J. (1968) Thermal responses of mutant enzymes and temperature limits to growth. Mol. Gen. Genet., 103, 116–126.

    Article  Google Scholar 

  • Lipmann, F. (1969) Polypeptide chain elongation in protein biosynthesis. Science, 164, 1024–1031.

    Article  Google Scholar 

  • Loftfield, R. and Vanderjagt, D. (1972) The frequency of errors in protein synthesis. Biochem. J., 128, 1353–1356.

    Google Scholar 

  • Manley, J. L. (1979) Synthesis and degradation of termination and premature termination fragments of ß-galaetosidase in vitro. J. Mol. Biol., 125, 407–432.

    Article  Google Scholar 

  • Menninger, J. (1978) The accumulation as peptidyl-transfer RNA of isoaccepting transfer RNA families in E. coli with temperature-sensitive peptidyl transfer RNA hydrolase. J. Biol. Chem.,253, 6808–6813.

    Google Scholar 

  • Miller, J. H. (1979) Genetic studies of the lac repressor: XI On aspects of the lac repressor structure suggestion of genetic experiments. J. Mol. Biol., 131, 249–258.

    Article  Google Scholar 

  • Miller, J. H. and Albertini, A. M. (1983) Effects of surrounding sequence on the suppression of nonsense codons. J. Mol. Biol., 164, 59–71.

    Article  Google Scholar 

  • Newton, A. (1970) Isolation and characterization of frameshift mutations in the lac operon. J. Mol. Biol., 49, 589–601.

    Article  Google Scholar 

  • Ninio, J. (1974) A semiquantitative treatment of missense and no sense suppression in the str A and ram ribosomal mutants of E. coli. J. Mol. Biol., 84, 297–313.

    Google Scholar 

  • Ninio, J. (1975) Kinetic amplification of enzyme discrimination. Biochimie, 57, 487–595.

    Article  Google Scholar 

  • O’Farrell, P. H. (1978) The suppression of defective translation by ppGpp and its role in the stringent response. Cell, 14, 545–557.

    Article  Google Scholar 

  • Orgel, L. E. (1963) The maintenance of the accuracy of protein synthesis and its relevance to ageing. Proc. Natl Acad. Sci. USA, 49, 517–521.

    Article  Google Scholar 

  • Parker, J., Johnston, T. C. and Borgia, P. T. (1980) Mistranslation in cells infected with bacteriophage MS2: direct evidence of Lys for Asn substitution. Mol. Gen. Genet., 180, 275–281.

    Article  Google Scholar 

  • Parker, J., Flanagan, J., Murphy, J. and Gallant, J. (1981) On the accuracy of protein synthesis in Drosphila melanogaster. Mech. Ageing Dev., 16, 127–139.

    Article  Google Scholar 

  • Pauling, L. (1957) In Festschrift Arthur Stoll, Birkhauser Verlag, Basel, pp. 597–602.

    Google Scholar 

  • Pettersson, I. and Kurland, C. G. (1980) Ribosomal protein L7/L12 is required for optimal translation. Proc. Natl Acad. Sci. USA, 77, 4007–4010.

    Article  Google Scholar 

  • Picard-Bennoun, M. (1976) Genetic evidence for ribosomal anti-suppressions in Podospora anserina. Mol. Gen. Genet., 147, 299–306.

    Article  Google Scholar 

  • Piepersberg, W., Geyl, D., Buclel, P. and Böck, A. (1979) Studies on the coordination of tRNA charging and polypeptide synthesis activity in E. coli. In Regulation of Macromolecular Synthesis by Low Molecular Weight Mediators (eds G. Koch and D. Richter ), Academic Press, New York.

    Google Scholar 

  • Pribnow, D., Sigurdson, D. C., Gold, L., Singer, B. S., Napoli, C., Brosius, J., Dull, T. J. and Noller, H. F. (1981) rIIcistrons of bacteriophage T4: DNA sequence around the intercistronic divide and positions of genetic landmarks. J. Mol. Biol., 149, 337–376.

    Article  Google Scholar 

  • Riddle, D. and Carbon, J. (1973) Frameshift suppression: A nucleotide addition in the anticodon of a glycine transfer RNA. Nature New Biol., 242, 230–234.

    Google Scholar 

  • Rojas, A.-M., Ehrenberg, M., Andersson, S. G. E. and Kurland, C. G. (1984) ppGpp inhibition of elongation factors Tu, G and Ts during polypeptide synthesis. Mol. Gen. Genet., 197, 36–45.

    Article  Google Scholar 

  • Ruusala, T., Ehrenberg, M. and Kurland, C. G. (1982a) Catalytic effects of elongation factor Ts on polypeptide synthesis. EMBO J., 1, 75–78.

    Google Scholar 

  • Ruusala, T., Ehrenberg, M. and Kurland, C. G. (1982b) Is there proofreading during polypeptide synthesis? EMBO J., 1, 741–745.

    Google Scholar 

  • Ruusala, T., Andersson, D., Ehrenberg, M. and Kurland, C. G. (1984) Hyper- accurate ribosomes inhibit growth. EMBO J., 3, 2575–2580.

    Google Scholar 

  • Ruusala, T. and Kurland, C. G. (1984) Streptomycin perturbs preferentially ribosomal proofreading. Mol. Gen. Genet., 198, 100–104.

    Article  Google Scholar 

  • Sambrook, J. F., Fan, D. P. and Brenner, S. (1967) A strong suppressor specific for UGA. Nature, 214, 452–453.

    Article  Google Scholar 

  • Spirin, A. S. (1978) Energetics of the ribosome. Prog. Nucl. Acids Res. Mol. Biol., 21, 39–63.

    Article  Google Scholar 

  • Thompson, R. C. and Stone, P. J. (1977) Proofreading of the codon-anticodon interaction on ribosomes. Proc. Natl Acad. Sei. USA, 74, 198–202.

    Article  Google Scholar 

  • Thompson, R. C., Dix, D. B., Gerson, R. B. and Karin, A. M. (1981) A GTPase reaction accompanying the ejection of Leu-tRNA by UUU-programmed ribosomes. J. Biol. Chem., 256, 81–86.

    Google Scholar 

  • Wagner, E. G. H. and Kurland, C. G. (1980) Translational accuracy enhanced in vitro by (p)ppGpp. Mol. Gen. Genet., 180, 139–145.

    Article  Google Scholar 

  • Wagner, E. G. H., Jelenc, P. C., Ehrenberg, M. and Kurland, C. G. (1982a) Rate of elongation of polyphenylalanine in vitro. Eur. J. Biochem., 122, 193–197.

    Article  Google Scholar 

  • Wagner, E. G. H., Ehrenberg, M. and Kurland, C. G. (1982b) Kinetic suppression of translational errors by (p)ppGpp. Mol. Gen. Genet., 185, 269–274.

    Article  Google Scholar 

  • Weiss, R. and Gallant, J. (1983) Mechanism of ribosome frameshifting during translation of the genetic code. Nature, 302, 389–393.

    Article  Google Scholar 

  • Weiss, R. (1983) Mechanism of ribosome frameshifting during translation of the genetic code. PhD Thesis, University of Washington.

    Google Scholar 

  • Weiss, R. (1984) Molecular model of ribosome frameshifting. Proc. Natl Acad. Sei. USA, 81, 5797–5801.

    Article  Google Scholar 

  • Weiss, R., Murphy, J., Wagner, G. and Gallant, J. (1984) The ribosome’s frame of mind. In Alfred Benzon Symposium 19: Gene Expression, the Translational Step and its Control (eds B. F. C. clark and H. U. Peterson ), Munksgaard, Copenhagen, pp. 208–220.

    Google Scholar 

  • Woese, C. (1970) Molecular mechanism of translation: a reciprocating ratchet mechanism. Nature, 226,817–820. Yegian, C. D. and Stent, G. S. (1969) An unusual condition of leucine transfer RNA appearing during leucine starvation of Escherichia coli. J. Mol. Biol., 39, 45–58.

    Google Scholar 

  • Yegian, C. D. and Stent, G. S. (1969) An unusual condition of leucine transfer RNA appearing during leucine starvation of Escherichia coli. J. Mol. Biol. , 39, 45–58.

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1986 Chapman and Hall

About this chapter

Cite this chapter

Kurland, C.G., Gallant, J.A. (1986). The secret life of the ribosome. In: Kirkwood, T.B.L., Rosenberger, R.F., Galas, D.J. (eds) Accuracy in Molecular Processes. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-4097-0_6

Download citation

  • DOI: https://doi.org/10.1007/978-94-009-4097-0_6

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-8318-8

  • Online ISBN: 978-94-009-4097-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics