The Influence of Look-Ahead on the Error Rate of Transcription
Mathematical modelling of natural phenomena, Tome 5 (2010) no. 3, pp. 206-227.

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In this paper we study the error rate of RNA synthesis in the look-ahead model for the random walk of RNA polymerase along DNA during transcription. The model’s central assumption is the existence of a window of activity in which ribonucleoside triphosphates (rNTPs) bind reversibly to the template DNA strand before being hydrolyzed and linked covalently to the nascent RNA chain. An unknown, but important, integer parameter of this model is the window size w. Here, we use mathematical analysis and computer simulation to study the rate at which transcriptional errors occur as a function of w. We find dramatic reduction in the error rate of transcription as w increases, especially for small values of w. The error reduction method provided by look-ahead occurs before hydrolysis and covalent linkage of rNTP to the nascent RNA chain, and is therefore distinct from error correction mechanisms that have previously been considered.
DOI : 10.1051/mmnp/20105313

Y. R. Yamada 1 ; C. S. Peskin 2

1 Department of Mathematics, University of Michigan, 48109-1043 Ann Arbor, MI, USA
2 Courant Institute of Mathematical Sciences, New York University, New York, NY, USA
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Y. R. Yamada; C. S. Peskin. The Influence of Look-Ahead on the Error Rate of Transcription. Mathematical modelling of natural phenomena, Tome 5 (2010) no. 3, pp. 206-227. doi : 10.1051/mmnp/20105313. http://geodesic.mathdoc.fr/articles/10.1051/mmnp/20105313/

[1] A. Alon. An introduction to systems biology: design principles of biological circuits. Chapman and Hall, Boca Raton, 2007.

[2] E. Abbodanzieri, W. Greenleaf, J. Shaevitz, R. Landick, S. Block Direct observation of base-pair stepping by RNA polymerase Nature 2005 460 465

[3] L. Bai, R. Fulbright, M. Wang Mechanochemical kinetics of transcription elongation Phys. Rev. Lett. 2007

[4] G. Bar-Nahum, V. Epshtein, A. Ruckenstein, R. Rafikov, A. Mustaev, E. Nudler A ratchet mechanism of transcription elongation and its control Cell 2005 183 193

[5] A. Blank, J. Gallant, R. Burgess, L. Loeb An RNA polymerase mutant with reduced accuracy of chain elongation Biochemistry 1986 5920 5928

[6] Y. Chen, D. Chafin, D. Price, A. Greenleaf Drosophila RNA polymerase II mutants that affect transcription elongation Jour. Biol. Chem. 1996 5993 5999

[7] G. Eichhorn, P. Chuknyisky, J. Butzow, R. Beal, C. Garland, C. Janzen, P. Clark, E. Tarien A structural model for fidelity in transcription Proc. Natl. Acad. Sci. 1994 7613 7617

[8] D. Gillespie A general method for numerically simulating the stochastic time evolution of coupled chemical reactions J. Comp. Phys. 1976 403 434

[9] D. Gillespie Exact stochastic simulation of coupled chemical reactions J. Phys. Chem. 1977 2340 2361

[10] S. Greive, P. Von Hippel Thinking quantitatively about transcriptional regulation Nat. Rev. Mol. Cell Biol. 2005 221 232

[11] K. Herbert, W. Greenleaf, S. Block Single-molecule studies of RNA polymerase: motoring along Annu. Rev. Biochem. 2008 149 176

[12] W. Hlavacek, A. Redondo, H. Metzger, C. Wofsy, B. Goldstein Kinetic proofreading models for cell signaling predict ways to escape kinetic proofreading Proc. Natl. Acad. Sci. 2001 7295 7300

[13] S. Holmes, T. Santangelo, C. Cunningham, J. Roberts, D. Erie Kinetic investigation of Escherichia coli RNA polymerase mutants that influence nucleotide discrimination and transcription fidelity Jour. Biol. Chem. 2006 18677 18683

[14] J. Hopfield Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity Proc. Natl. Acad. Sci. 1974 4135 4139

[15] K. Howe, C. Kane, A. Ares Perturbation of transcription elongation influences the fidelity of internal exon inclusion in saccharomyces cerevisiae RNA 2003 993 1006

[16] C. Jeon, K. Agarwal Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS Proc. Natl. Acad. Sci. 1996 13677 13682

[17] M. Kireeva, Y. Nedlialkov, G. Cremona, Y. Purtov, L. Lubkowska, F. Malagon, Z. Burton, J. Strathern, M. Kashlev Transient reversal of RNA polymerase II active site closing controls fidelity of transcription elongation Mol. Cell 2008 557 566

[18] R. Libby, J. Gallant The role of RNA polymerase in transcriptional fidelity Mol. Microbiol. 1991 999 1004

[19] R. Libby, J Gallant Phosphorolytic error correction during transcription Mol. Microbiol. 1994 121 129

[20] R. Libby, L. Nelson, J. Calvo, J. Gallant Transcriptional proofreading in escherichia coli EMBO Jour. 1989 3153 3158

[21] F. Malagon, M. Kireeva, B. Shafer, L. Lubkowska, M. Kashlev, J. Strathern Mutations in the saccharomyces cerevisiae RPB1 gene conferring hypersensitivity to 6-Azauracil Genetics 2006 2201 2209

[22] P. Mason, K. Struhl Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo Mol. Cell 2005 831 840

[23] M. De La Mata, C. Alonso, S. Kadener, J. Fededa, M. Blaustein, J. Pelisch, P. Cramer, D. Bentley, A. Kornblihtt A Slow RNA Polymerase II Affects Alternative Splicing in Vivo Mol. Cell 2003 525 532

[24] T. Mckeithan Kinetic proofreading in T-cell receptor signal transduction Proc. Natl. Acad. Sci. 1995 5042 5046

[25] J. Ninio Kinetic amplification of enzyme discrimination Biochimie 1975 587 595

[26] J. Roberts, S. Shankar, J. Filter RNA polymerase elongation Ffactors Annu. Rev. Microbiol. 2008 211 233

[27] J. Roussel, R. Zhu Stochastic kinetics description of a simple transcription model Bull. Math. Biol. 2006 1681 1713

[28] J. Shaevitz, E. Abbondanzieri, R. Landick, S. Block Backtracking by single RNA polymerase molecules observed at near-base-pair resolution Nature 2003 684 687

[29] R. Sims, R. Belotserkovskaya, D. Reinberg Elongation by RNA polymerase II: the short and long of it Genes Dev. 2004 2437 2468

[30] C. Springgate, L. Loeb On the fidelity of transcription by escherichia coli ribonucleic acid polymerase J. Mol. Biol. 1975 577 591

[31] E. Stepanova, J. Lee, M. Ozerova, E. Semenova, K. Datsenko, B. Wanner, K. Severinov, S. Borukhov Analysis of promoter targets for Escheichia coli transcription elongation factor GreA in vivo and in vitro J. Bateriol. 2007 8772 8785

[32] P. Swain, E. Siggia The role of proofreading in signal transduction specifity Biophys. J. 2007 2928 2933

[33] V. Tadigotla, D. O’Maoileidigh, A. Sengupta, V. Epshtein, R. Ebright, E. Nudler, A. Ruckenstein Thermodynamic and kinetic modeling of transcriptional pausing Prof. Natl. Acad. Sci. 2006 4439 4444

[34] J. Thomas, A. Platas, D. Hawley Transcriptional fidelity and proofreading by RNA polymerase II Cell 1998 627 637

[35] T. Tlusty, R. Bar-Ziv, A. Libchaber High-fidelity DNA sensing by protein binding fluctuations Phys. Rev. Lett. 2004

[36] U. Vogel, K. Jensen The RNA chain elongation rate in escherichia coli depends on the growth rate J. Bacteriol. 1994 2807 2813

[37] M. Voliotis, N. Cohen, C. Molina-Paris, T. Liverpool Fluctuations, pauses, and backtracking in DNA transcription Biophys. J. 2008 334 348

[38] M. Voliotis, N. Cohen, C. Molina-Paris, T. Liverpool. Backtracking and error correction in DNA transcription in The Art and Science of Statistical Bioinformatics. 104-107, Leeds University Press, Leeds, 2008.

[39] P. Xie A dynamic model for transcription elongation and sequence-dependent short pauses by RNA polymerase BioSystems 2008 199 210

[40] Y. Yamada, C. Peskin. A chemical kinetic model of transcriptional elongation. LANL ArXiv (2006), q-bio.BM/0603012.

[41] Y. Yamada, C. Peskin A look-ahead model for the elongation dynamics of transcription Biophys. J. 2009 3015 3031

[42] N. Zenkin, Y. Yuzenkova, K. Severinov Transcript-assisted transcriptional proofreading Science 2006 518 520

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