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Free energy cost and accuracy in branched selection processes of biosynthesis

Published online by Cambridge University Press:  17 March 2009

Clas Blomberg
Affiliation:
Research Group for Theoretical Biophysics, Royal Institute of Technology, S-10044, Stockholm

Extract

Selection in biochemical synthesis processes is a very important task: processes as protein or nucleic acid synthesis must be very accurate although the cell abounds with closely related molecules which, intuitively, should be difficult to distinguish. The mechanisms of selection and the underlying processes have been extensively studied in the last years, and the ideas have been developed into mathematical models to visualize the potentials of recognition and error correction. There are several aspects on this, the main aspect of the present work being the important fact that the cell must pay for the increased accuracy in terms of available free energy: processes are driven from equilibrium, and do away with appreciable dissipation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1983

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References

Baldwin, A. & Berg, P. (1966). Transfer ribonucleic acid-induced hydrolysis of valyladenylate bound to isoleucyl ribonucleic acid synthetase. J. biol. Chem. 241, 839845.CrossRefGoogle ScholarPubMed
Bennet, Ch. H. (1979). Dissipation–error trade off in DNA replication. BioSystems 11, 8591.CrossRefGoogle Scholar
Bernardi, F. & Ninio, J. (1978). The accuracy of DNA replication. Biochimie 60, 10831095.CrossRefGoogle ScholarPubMed
Bernardi, F., Saghi, M., Dorizzi, M. & Ninio, J. (1979). A new approach to DNA polymerase kinetics. J. Molec. Biol. 129, 93112.CrossRefGoogle ScholarPubMed
Bessman, M. J., Muzyczka, N., Goodman, M. F. & Schnaar, R. L. (1974). Studies on the biochemical basis of spontaneous mutations. II. The incorporation of a base and its analogue into DNA by wild-type mutator and antimutator DNA polymerase. J. Molec. Biol. 88, 409421.CrossRefGoogle Scholar
Blomberg, C. (1977). A kinetic recognition process for tRNA at the ribosome. J. theor. Biol. 66, 307325.CrossRefGoogle ScholarPubMed
Blomberg, C. (1983). Thermodynamic aspects on accuracy in the synthesis of biomolecules. Int. J. Quantum. Chem. 23, 687707.CrossRefGoogle Scholar
Blomberg, C. & Eherenberg, M. (1981). Energy considerations for kinetic proofreading in biosynthesis. J. theor. Biol. 88, 631670.CrossRefGoogle ScholarPubMed
Blomberg, C., Ehrenberg, M. & Kurland, C. G. (1981). Free energy dissipation constraints on the accuracy of enzymatic selections. Q. Rev. Biophys. 13, 231254.CrossRefGoogle Scholar
Brutlag, D. & Kornberg, A. (1972). Enzymatic synthesis of deoxy-ribonucleic acid. XXXVI. A proofreading function for the 3′-5′ exonuclease activity in deoxyribonucleic acid polymerases. J. biol. Chem. 247, 241248.CrossRefGoogle Scholar
Chuprina, V. P. & Poltev, V. I. (1983). Possible conformations of double-helical polynucleotides containing incorrect base pairs. Nucl. Acids Res. (In the Press.)CrossRefGoogle Scholar
Claverie, P. (1971). Calculation of interaction energy between triplets in RNA-n configuration. J. Molec. Biol. 56, 7577.CrossRefGoogle Scholar
Clayton, L. K., Goodman, M. F., Branscomb, E. W. & Galas, D. J. (1979). Error induction and correction by mutant and wild type T4 DNA polymerases. Kinetic error discrimination mechanisms. J. biol. Chem. 254, 19021912.CrossRefGoogle ScholarPubMed
Crick, F. H. C. (1975). Discussion remark. Phil. Trans. R. Soc. Lond. 272, 193.Google Scholar
Durup, J. (1982). On the relation between error rates in DNA replication and elementary chemical rate constants. J. theor. Biol. 94, 607632.CrossRefGoogle ScholarPubMed
Ehrenberg, M. & Blomberg, C. (1980). Thermodynamic constraints on kinetic proofreading in biosynthesis pathways. Biophys. J. 31, 333358.CrossRefGoogle Scholar
Fersht, A. (1977). Enzyme Structure and Mechanism, ch. 11. Oxford: W. H. Freeman.Google Scholar
Fersht, A. R. (1981). Enzymatic editing mechanism and the genetic code. Proc. R. Soc. Land. B. 212, 351379.Google Scholar
Fersht, A. R. & Dingwall, C. (1979). Establishing the misacylation deacylation of the tRNA pathway of procaryatic and eurocaryotic valyl-tRNA synthetases. Biochemistry 18, 12381244.CrossRefGoogle Scholar
Fersht, A. R., Knill-Jones, J. W. & Tsui, W. C. (1982). Kinetic basis of spontaneous mutation. Misinsertion frequencies, proofreading specifications and cost of proofreading by DNA polymerases of Escherichia coli. J. Molec. Biol. 156, 3751.CrossRefGoogle ScholarPubMed
Freter, R. R. & Savageau, M. H. (1980). Proofreading systems of multiple stages for improved accuracy of biological discrimination. J. theor. Biol. 85, 99123.CrossRefGoogle ScholarPubMed
Galas, D. & Brascomb, E. (1979). Enzymatic determination of DNA polymerase accuracy. Theory of coliphage T4 polymerase mechanism. J. Molec. Biol. 124, 653687.CrossRefGoogle Scholar
Garduno, R., Rein, R., Egan, J. T., Coekelenberch, Y. & Macelroy, R. D. (1977). Purine–purine base pairs and origin of transversion-type mutations. Int. J. Quantum. Chem. Quant. Biol. Symp. 4, 197204.Google Scholar
Goodman, M. F., Gore, W. C., Muzyczka, N. & Bessman, M. J. (1974). Studies on the biochemical basis of spontaneous mutations. III. Rate model for DNA polymerase-effected nucleotide misincorporation. J. Molec. Biol. 88, 423435.CrossRefGoogle ScholarPubMed
Gorini, L. (1971). Ribosomal discrimination of tRNAs. Nature (New Biol.) 234, 261264.CrossRefGoogle ScholarPubMed
Goulian, M., Lucas, Z. J. & Kornberg, A. (1968). Enzymatic synthesis of deoxyribonucleic acid. XXV. Purification and properties of deoxy-ribonucleic acid polymerase induced by infection with phase T4. J. biol. Chem. 243, 627638.CrossRefGoogle Scholar
Grosjean, H. J., De Henau, S. & Crothers, D. M. (1978). On the physical basis for ambiguity in genetic coding interaction. Proc. natn. Acad. Sci. U.S.A. 75, 610614.CrossRefGoogle Scholar
Hopfield, J. J. (1974). Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. natn. Acad. Sci. U.S.A. 71, 41354139.CrossRefGoogle ScholarPubMed
Hopfield, J. J. (1980). The energy relay - a proofreading scheme based on dynamic cooperativity and lacking all characteristic symptoms of kinetic proofreading in DNA synthesis and protein synthesis. Proc. natn. Acad. Sci. U.S.A. 77, 52485252.CrossRefGoogle ScholarPubMed
Hopfield, J. J., Yamane, T., Yue, V. & Coutts, S. M. (1976). Direct experimental evidence for kinetic proofreading in amino acylation of tRNAIle. Proc. natn. Acad. Sci. U.S.A. 73, 11641168.CrossRefGoogle ScholarPubMed
Kremen, A. (1982). Information-theoretic significance of Gibbs energy supply to editing mechanisms. Biophys. J. 40, 149154.CrossRefGoogle ScholarPubMed
Kurland, C. G. (1978). The role of guanine nucleotides in protein biosynthesis. Biophys. J. 22, 373392.CrossRefGoogle ScholarPubMed
Kurland, C. G., Rigler, R., Ehrenberg, M. & Blomberg, C. (1975). Allosteric mechanism for codon-dependent tRNA selection on ribo-somes. Proc. natn. Acad. Sci. U.S.A. 72, 42484251.CrossRefGoogle Scholar
Labuda, D., Grosjean, H., Striker, G. & Pörschke, D. (1982). Codon: anticodon and anticodon: anticodon interaction. Evaluation of equilibrium and kinetic parameters of complexes involving a G: U wobble. Biochim. Biophys. Acta 698, 230236.CrossRefGoogle ScholarPubMed
Loeb, L. A., Dube, D. K., Beckman, R. A., Koplitz, M. & Gopinathan, K. P. (1981). On the fidelity of DNA replication. Nucleotide mono-phosphate generation during polymerization. J. biol. Chem. 256, 39783987.CrossRefGoogle Scholar
Loftfield, R. & Vanderjagt, D. (1972). The frequency of errors in protein biosynthesis. Biochem. J. 128, 13531355.CrossRefGoogle ScholarPubMed
Malygin, E. G. (1980). Coefficient of specificity of alternative substrates for enzymatic reactions. Biofizika 25, 185186.Google Scholar
Malygin, E. G. & Yashina, L. N. (1979). Kinetic description of proofreading mechanism for bifunctional DNA-polymerases. Dokl. Akad. Nauk. SSSR 250, 246250.Google Scholar
Mulvey, R. S. & Fersht, A. R. (1977). Editing mechanisms in amino-acylation of transfer-RNA: ATP consumption and the binding of aminoacyl transfer-RNA by elongation factor Tu. Biochemistry 16, 47314737.CrossRefGoogle ScholarPubMed
Ninio, J. (1974). A semiquantitative treatment of mis-sense and nonsense suppression in the str A and ram ribosomal mutants of Escherichia coli. Evaluation of some molecular parameters of translation in vivo. J. Molec. Biol. 84, 297313.CrossRefGoogle Scholar
Ninio, J.(1975). Kinetic amplification of enzyme discrimination. Biochimie 57, 587595.CrossRefGoogle ScholarPubMed
Norris, A. & Berg, P. (1964). Mechanism of aminoacyl RNA synthesis: studies with isolated aminoacyl adenylate complexes of isoleucyl RNA synthetase. Biochemistry 52, 330337.Google ScholarPubMed
Pauling, L. (1858). The probability of errors in the process of synthesis of protein molecules. In Festschrift Arthur Stoll(ed. A. G. Birkhauser), pp. 597602.Google Scholar
Poltev, V. I. & Bruskov, V. I. (1978). On molecular mechanisms of nucleic acid synthesis fidelity aspects, i. Contribution of base interactions. J. theor. Biol. 70, 6983.CrossRefGoogle ScholarPubMed
Rein, R., Coeckelenberch, Y. & Egan, J. T. (1975). Elaboration of principle of base complementarity and elements of a theory of point mutations. Int. J. Quantum. Chem. Quant. Biol. Symp. 2, 145153.Google Scholar
Ruusala, T., Ehrenberg, M. & Kurland, C. G. (1982). Is there proofreading during polypeptide synthesis? EMBO J. 1, 741745.CrossRefGoogle ScholarPubMed
Savageau, M. A. (1981). Accuracy of proofreading with zero energy cost. J. theor. Biol. 93, 179195.CrossRefGoogle ScholarPubMed
Savageau, M. A. & Freter, R. R. (1979 a). On the evolution of accuracy and cost of tRNA proofreading. Proc. natn. Acad. Sci. U.S.A. 76, 19021912.CrossRefGoogle ScholarPubMed
Savageau, M. A. & Freter, R. R. (1979 b). Energy cost of proofreading to increase fidelity of transfer ribonucleic acid amino acylation. Biochemistry 18, 34863492.CrossRefGoogle Scholar
Savageau, M. A. & Lapointe, D. S. (1981). Optimization of kinetic proofreading: a general method for derivation of the constraint relations and an exploration of a specific case. J. theor. Biol. 93, 157177.CrossRefGoogle Scholar
Schwartz, V. S. & Lysikov, B. N. (1974). Physical mechanisms of a ribosomal sieve. Dokl. Akad. Nauk SSSR 217, 14461448.Google Scholar
Thompson, R. C. & Dix, D. B. (1982). Accuracy of protein biosynthesis. A kinetic study of the reaction of poly(U)-programmed ribosomes with a leucyl tRNA2-elongation factor Tu-GTP complex. J. biol. Chem. 257, 66776682.CrossRefGoogle Scholar
Topal, M. D., Diguiseppi, S. R. & Sinha, N. K. (1980). Molecular basis for substitution mutations. Effect of primer terminal and template residues on nucleotide selection by phage T4 DNA polymerase in vitro. J. biol. Chem. 255, 1171711724.CrossRefGoogle ScholarPubMed
Topal, M. D. & Fresco, J. R. (1976). Complementary base pairing and origin of substitution mutations. Nature 263, 285289.CrossRefGoogle ScholarPubMed