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Journal of Statistical Physics

, Volume 162, Issue 5, pp 1167–1182 | Cite as

Protocols for Copying and Proofreading in Template-Assisted Polymerization

  • Simone PigolottiEmail author
  • Pablo Sartori
Article

Abstract

We discuss how information encoded in a template polymer can be stochastically copied into a copy polymer. We consider four different stochastic copy protocols of increasing complexity, inspired by building blocks of the mRNA translation pathway. In the first protocol, monomer incorporation occurs in a single stochastic transition. We then move to a more elaborate protocol in which an intermediate step can be used for error correction. Finally, we discuss the operating regimes of two kinetic proofreading protocols: one in which proofreading acts from the final copying step, and one in which it acts from an intermediate step. We review known results for these models and, in some cases, extend them to analyze all possible combinations of energetic and kinetic discrimination. We show that, in each of these protocols, only a limited number of these combinations leads to an improvement of the overall copying accuracy.

Keywords

Kinetic proofreading Biological copying Polymerization Speed-accuracy trade-off 

Notes

Acknowledgments

This work was supported by the Ministerio de Economia y Competividad (Spain) and FEDER (European Union), under Project FIS2012-37655-C02-01.

References

  1. 1.
    Andrieux, D., Gaspard, P.: Nonequilibrium generation of information in copolymerization processes. Proc. Natl. Acad. Sci. 105(28), 9516–9521 (2008)CrossRefADSGoogle Scholar
  2. 2.
    Andrieux, D., Gaspard, P.: Information erasure in copolymers. Europhys. Lett. 103(3), 30,004 (2013)CrossRefGoogle Scholar
  3. 3.
    Bennett, C.H.: Dissipation-error tradeoff in proofreading. BioSystems 11(2), 85–91 (1979)CrossRefGoogle Scholar
  4. 4.
    Betterton, M., Jülicher, F.: A motor that makes its own track: helicase unwinding of DNA. Phys. Rev. Lett. 91(25), 258,103 (2003)CrossRefGoogle Scholar
  5. 5.
    Bo, S., Del Giudice, M., Celani, A.: Thermodynamic limits to information harvesting by sensory systems. J. Stat. Mech. 2015(1), P01,014 (2015)CrossRefMathSciNetGoogle Scholar
  6. 6.
    Cady, F., Qian, H.: Open-system thermodynamic analysis of DNA polymerase fidelity. Phys. Biol. 6(3), 036,011 (2009)CrossRefGoogle Scholar
  7. 7.
    Esposito, M., Lindenberg, K., Van den Broeck, C.: Extracting chemical energy by growing disorder: efficiency at maximum power. J. Stat. Mech. 2010(01), P01,008 (2010)CrossRefGoogle Scholar
  8. 8.
    François, P., Voisinne, G., Siggia, E.D., Altan-Bonnet, G., Vergassola, M.: Phenotypic model for early t-cell activation displaying sensitivity, specificity, and antagonism. Proc. Natl. Acad. Sci. 110(10), E888–E897 (2013)CrossRefADSGoogle Scholar
  9. 9.
    Freter, R.R., Savageau, M.A.: Proofreading systems of multiple stages for improved accuracy of biological discrimination. J. Theor. Biol. 85(1), 99–123 (1980)CrossRefGoogle Scholar
  10. 10.
    Galburt, E.A., Grill, S.W., Wiedmann, A., Lubkowska, L., Choy, J., Nogales, E., Kashlev, M., Bustamante, C.: Backtracking determines the force sensitivity of RNAP II in a factor-dependent manner. Nature 446(7137), 820–823 (2007)CrossRefADSGoogle Scholar
  11. 11.
    Gromadski, K.B., Rodnina, M.V.: Kinetic determinants of high-fidelity trna discrimination on the ribosome. Mol. Cell 13(2), 191–200 (2004)CrossRefGoogle Scholar
  12. 12.
    Hartich, D., Barato, A.C., Seifert, U.: Nonequilibrium sensing and its analogy to kinetic proofreading. arXiv preprint arXiv:1502.02594 (2015)
  13. 13.
    Hopfield, J.J.: Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl. Acad. Sci. 71(10), 4135–4139 (1974)CrossRefADSGoogle Scholar
  14. 14.
    Johansson, M., Bouakaz, E., Lovmar, M., Ehrenberg, M.: The kinetics of ribosomal peptidyl transfer revisited. Mol. Cell 30(5), 589–598 (2008)CrossRefGoogle Scholar
  15. 15.
    Johansson, M., Lovmar, M., Ehrenberg, M.: Rate and accuracy of bacterial protein synthesis revisited. Curr. Opin. Microbiol. 11(2), 141–147 (2008)CrossRefGoogle Scholar
  16. 16.
    Lan, G., Sartori, P., Neumann, S., Sourjik, V., Tu, Y.: The energy-speed-accuracy trade-off in sensory adaptation. Nat. Phys. 8(5), 422–428 (2012)CrossRefGoogle Scholar
  17. 17.
    Loeb, L.A., Kunkel, T.A.: Fidelity of DNA synthesis. Annu. Rev. Biochem. 51(1), 429–457 (1982)CrossRefGoogle Scholar
  18. 18.
    Mckeithan, T.W.: Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. 92(11), 5042–5046 (1995)CrossRefADSGoogle Scholar
  19. 19.
    Mellenius, H., Ehrenberg, M.: DNA template dependent accuracy variation of nucleotide selection in transcription. PLoS One 10(3), e0119,588 (2015)CrossRefGoogle Scholar
  20. 20.
    Murugan, A., Huse, D.A., Leibler, S.: Speed, dissipation, and error in kinetic proofreading. Proc. Natl. Acad. Sci. 109(30), 12034–12039 (2012)CrossRefADSGoogle Scholar
  21. 21.
    Murugan, A., Huse, D.A., Leibler, S.: Discriminatory proofreading regimes in nonequilibrium systems. Phys. Rev. X 4(2), 021,016 (2014)Google Scholar
  22. 22.
    Ninio, J.: Kinetic amplification of enzyme discrimination. Biochimie 57(5), 587–595 (1975)CrossRefGoogle Scholar
  23. 23.
    Pape, T., Wintermeyer, W., Rodnina, M.: Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J. 18(13), 3800–3807 (1999)CrossRefGoogle Scholar
  24. 24.
    Parrondo, J.M., Horowitz, J.M., Sagawa, T.: Thermodynamics of information. Nat. Phys. 11(2), 131–139 (2015)CrossRefGoogle Scholar
  25. 25.
    Pauling, L.: Festschrift fuer Prof. Dr. Arthur Stoll. Birkhauser, Basel (1958)Google Scholar
  26. 26.
    Rao, R., Peliti, L.: Thermodynamics of accuracy in kinetic proofreading: Dissipation and efficiency trade-offs. arXiv preprint arXiv:1504.02494 (2015)
  27. 27.
    Sartori, P., Pigolotti, S.: Kinetic versus energetic discrimination in biological copying. Phys. Rev. Lett. 110(18), 188,101 (2013)CrossRefGoogle Scholar
  28. 28.
    Sartori, P., Pigolotti, S.: Thermodynamics of error correction. arXiv preprint arXiv:1504.06407 (2015)
  29. 29.
    Savir, Y., Tlusty, T.: The ribosome as an optimal decoder: a lesson in molecular recognition. Cell 153(2), 471–479 (2013)CrossRefGoogle Scholar
  30. 30.
    Thompson, R.C., Karim, A.M.: The accuracy of protein biosynthesis is limited by its speed: high fidelity selection by ribosomes of aminoacyl-tRNA ternary complexes containing GTP [gamma S]. Proc. Natl. Acad. Sci. 79(16), 4922–4926 (1982)CrossRefADSGoogle Scholar
  31. 31.
    Voliotis, M., Cohen, N., Molina-París, C., Liverpool, T.B.: Fluctuations, pauses, and backtracking in DNA transcription. Biophys. J 94(2), 334–348 (2008)CrossRefGoogle Scholar
  32. 32.
    Zaher, H.S., Green, R.: Fidelity at the molecular level: lessons from protein synthesis. Cell 136(4), 746–762 (2009)CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Universitat Politecnica de CatalunyaTerrassaSpain
  2. 2.Max Planck Institute for the Physics of Complex SystemsDresdenGermany

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