A small post-translocation energy bias aids nucleotide selection in T7 RNA polymerase transcription

Biophysical Journal

Volumn 102, Issue 3, 2012, Pages 532-541

  Yu, Jin ^a   Oster, George ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHAGE T7 RNA POLYMERASE; DNA; DNA DIRECTED RNA POLYMERASE; NUCLEOTIDE; VIRUS PROTEIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ENZYME SPECIFICITY; GENETIC TRANSCRIPTION; GENETICS; KINETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); PROTEIN CONFORMATION; PROTEIN SUBUNIT; THERMODYNAMICS;

DNA; DNA-DIRECTED RNA POLYMERASES; KINETICS; MODELS, MOLECULAR; MOVEMENT; NUCLEIC ACID CONFORMATION; NUCLEOTIDES; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SUBSTRATE SPECIFICITY; THERMODYNAMICS; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

EID: 84863082064     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.12.028     Document Type: Article

References (62)

1. F. Jacob, and J. Monod On the regulation of gene activity Cold Spring Harb. Symp. Quant. Biol. 26 1961 193 211
2. H. Buc, and T. Strick RNA Polymerase as Molecular Motors 2009 The Royal Society of Chemistry Cambridge, UK
3. S.J. Greive, and P.H. von Hippel Thinking quantitatively about transcriptional regulation Nat. Rev. Mol. Cell Biol. 6 2005 221 232 (Pubitemid 40314923)
4. W.T. McAllister, and C.A. Raskin The phage RNA polymerases are related to DNA polymerases and reverse transcriptases Mol. Microbiol. 10 1993 1 6 (Pubitemid 23311188)
5. S. Borukhov, and E. Nudler RNA polymerase: the vehicle of transcription Trends Microbiol. 16 2008 126 134
6. A. Hirata, and K.S. Murakami Archaeal RNA polymerase Curr. Opin. Struct. Biol. 19 2009 724 731
7. V. Sosunov, and E. Sosunova A. Goldfarb Unified two-metal mechanism of RNA synthesis and degradation by RNA polymerase EMBO J. 22 2003 2234 2244 (Pubitemid 36565546)
8. T.A. Steitz, and J.A. Steitz A general two-metal-ion mechanism for catalytic RNA Proc. Natl. Acad. Sci. USA 90 1993 6498 6502 (Pubitemid 23207240)
9. D.L. Ollis, and P. Brick T.A. Steitz Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP Nature 313 1985 762 766 (Pubitemid 15130824)
10. R. Sousa, and Y.J. Chung B.C. Wang Crystal structure of bacteriophage T7 RNA polymerase at 3.3 resolution Nature 364 1993 593 599 (Pubitemid 23274714)
11. S.N. Kochetkov, E.E. Rusakova, and V.L. Tunitskaya Recent studies of T7 RNA polymerase mechanism FEBS Lett. 440 1998 264 267 (Pubitemid 29052295)
12. R. Sousa, S. Mukherjee, and M. Kivie T7 RNA polymerase Progress in Nucleic Acid Research and Molecular Biology 2003 Academic Press New York 1 41 (Pubitemid 137639539)
13. T.A. Steitz The structural changes of T7 RNA polymerase from transcription initiation to elongation Curr. Opin. Struct. Biol. 19 2009 683 690
14. T.A. Steitz DNA polymerases: structural diversity and common mechanisms J. Biol. Chem. 274 1999 17395 17398
15. T.H. Tahirov, and D. Temiakov S. Yokoyama Structure of a T7 RNA polymerase elongation complex at 2.9 resolution Nature 420 2002 43 50 (Pubitemid 35291434)
16. Y.W. Yin, and T.A. Steitz The structural mechanism of translocation and helicase activity in T7 RNA polymerase Cell 116 2004 393 404 (Pubitemid 38366316)
17. D. Temiakov, and V. Patlan D.G. Vassylyev Structural basis for substrate selection by T7 RNA polymerase Cell 116 2004 381 391 (Pubitemid 38366315)
18. K.J. Durniak, S. Bailey, and T.A. Steitz The structure of a transcribing T7 RNA polymerase in transition from initiation to elongation Science 322 2008 553 557
19. L.G. Brieba, and R. Sousa Roles of histidine 784 and tyrosine 639 in ribose discrimination by T7 RNA polymerase Biochemistry 39 2000 919 923 (Pubitemid 30075318)
20. Q. Guo, and R. Sousa Translocation by T7 RNA polymerase: a sensitively poised Brownian ratchet J. Mol. Biol. 358 2006 241 254
21. V.S. Anand, and S.S. Patel Transient state kinetics of transcription elongation by T7 RNA polymerase J. Biol. Chem. 281 2006 35677 35685 (Pubitemid 46041298)
22. Y. Zhou, and D.M. Navaroli C.T. Martin Dissociation of halted T7 RNA polymerase elongation complexes proceeds via a forward-translocation mechanism Proc. Natl. Acad. Sci. USA 104 2007 10352 10357 (Pubitemid 47185669)
23. G.M. Skinner, and C.G. Baumann J.G. Hoggett Promoter binding, initiation, and elongation by bacteriophage T7 RNA polymerase. A single-molecule view of the transcription cycle J. Biol. Chem. 279 2004 3239 3244 (Pubitemid 38140557)
24. P. Thomen, P.J. Lopez, and F. Heslot Unraveling the mechanism of RNA-polymerase forward motion by using mechanical force Phys. Rev. Lett. 94 2005 128102
25. P. Thomen, and P.J. Lopez F. Heslot T7 RNA polymerase studied by force measurements varying cofactor concentration Biophys. J. 95 2008 2423 2433
26. J.H. Kim, and R.G. Larson Single-molecule analysis of 1D diffusion and transcription elongation of T7 RNA polymerase along individual stretched DNA molecules Nucleic Acids Res. 35 2007 3848 3858 (Pubitemid 47244676)
27. W.S. Yarnell, and J.W. Roberts Mechanism of intrinsic transcription termination and antitermination Science 284 1999 611 615 (Pubitemid 29289580)
28. D. Wang, and D.A. Bushnell R.D. Kornberg Structural basis of transcription: backtracked RNA polymerase II at 3.4 ngstrom resolution Science 324 2009 1203 1206
29. E.A. Galburt, and S.W. Grill C. Bustamante Backtracking determines the force sensitivity of RNAP II in a factor-dependent manner Nature 446 2007 820 823 (Pubitemid 46582033)
30. J.W. Shaevitz, and E.A. Abbondanzieri S.M. Block Backtracking by single RNA polymerase molecules observed at near-base-pair resolution Nature 426 2003 684 687 (Pubitemid 38009379)
31. N. Komissarova, and M. Kashlev Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3′ end of the RNA intact and extruded Proc. Natl. Acad. Sci. USA 94 1997 1755 1760
32. H.-Y. Wang, and T. Elston G. Oster Force generation in RNA polymerase Biophys. J. 74 1998 1186 1202 (Pubitemid 28108530)
33. C.S. Peskin, G.M. Odell, and G.F. Oster Cellular motions and thermal fluctuations: the Brownian ratchet Biophys. J. 65 1993 316 324 (Pubitemid 23206064)
34. S.M. Simon, C.S. Peskin, and G.F. Oster What drives the translocation of proteins? Proc. Natl. Acad. Sci. USA 89 1992 3770 3774
35. E.A. Abbondanzieri, and W.J. Greenleaf S.M. Block Direct observation of base-pair stepping by RNA polymerase Nature 438 2005 460 465 (Pubitemid 41742012)
36. G. Bar-Nahum, and V. Epshtein E. Nudler A ratchet mechanism of transcription elongation and its control Cell 120 2005 183 193 (Pubitemid 40174762)
37. C. Bustamante, D. Keller, and G. Oster The physics of molecular motors Acc. Chem. Res. 34 2001 412 420 (Pubitemid 32822163)
38. R. Sousa, and R. Padilla A mutant T7 RNA polymerase as a DNA polymerase EMBO J. 14 1995 4609 4621
39. A.A. Golosov, and J.J. Warren M. Karplus The mechanism of the translocation step in DNA replication by DNA polymerase I: a computer simulation analysis Structure 18 2010 83 93
40. D.G. Vassylyev, and M.N. Vassylyeva I. Artsimovitch Structural basis for transcription elongation by bacterial RNA polymerase Nature 448 2007 157 162 (Pubitemid 47067370)
41. D.G. Vassylyev, and M.N. Vassylyeva R. Landick Structural basis for substrate loading in bacterial RNA polymerase Nature 448 2007 163 168 (Pubitemid 47067369)
42. A.L. Gnatt, and P. Cramer R.D. Kornberg Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 resolution Science 292 2001 1876 1882 (Pubitemid 32538357)
43. F. Brueckner, J. Ortiz, and P. Cramer A movie of the RNA polymerase nucleotide addition cycle Curr. Opin. Struct. Biol. 19 2009 294 299
44. H. Kettenberger, K.J. Armache, and P. Cramer Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS Mol. Cell. 16 2004 955 965 (Pubitemid 40018405)
45. F. Brueckner, and P. Cramer Structural basis of transcription inhibition by α-amanitin and implications for RNA polymerase II translocation Nat. Struct. Mol. Biol. 15 2008 811 818
46. J. Huang, L.G. Brieba, and R. Sousa Misincorporation by wild-type and mutant T7 RNA polymerases: identification of interactions that reduce misincorporation rates by stabilizing the catalytically incompetent open conformation Biochemistry 39 2000 11571 11580
47. J. Petruska, L.C. Sowers, and M.F. Goodman Comparison of nucleotide interactions in water, proteins, and vacuum: model for DNA polymerase fidelity Proc. Natl. Acad. Sci. USA 83 1986 1559 1562 (Pubitemid 16018603)
48. J.J. Dunn, and F.W. Studier Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements J. Mol. Biol. 166 1983 477 535 (Pubitemid 13027896)
49. S.T. Jeng, J.F. Gardner, and R.I. Gumport Transcription termination in vitro by bacteriophage T7 RNA polymerase. The role of sequence elements within and surrounding a ρ-independent transcription terminator J. Biol. Chem. 267 1992 19306 19312
50. L. Bai, A. Shundrovsky, and M.D. Wang Sequence-dependent kinetic model for transcription elongation by RNA polymerase J. Mol. Biol. 344 2004 335 349 (Pubitemid 39441208)
51. K. Datta, and P.H. von Hippel Direct spectroscopic study of reconstituted transcription complexes reveals that intrinsic termination is driven primarily by thermodynamic destabilization of the nucleic acid framework J. Biol. Chem. 283 2008 3537 3549
52. T.D. Yager, and P.H. von Hippel A thermodynamic analysis of RNA transcript elongation and termination in Escherichia coli Biochemistry 30 1991 1097 1118
53. H.-J. Woo, Y. Liu, and R. Sousa Molecular dynamics studies of the energetics of translocation in model T7 RNA polymerase elongation complexes Proteins. Structure, Function, and Bioinformatics 73 2008 1021 1036
54. S. Tagami, and S.-i. Sekine S. Yokoyama Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein Nature 468 2010 978 982
55. D.G. Vassylyev, and S. Sekine S. Yokoyama Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 resolution Nature 417 2002 712 719 (Pubitemid 34640620)
56. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38 27-28 (Pubitemid 26152973)
57. 2NMR line shapes for aromatic ring motions in solids J. Am. Chem. Soc. 103 1981 7707 7710 (Pubitemid 12072211)
58. D. Gillespie A general method for numerically simulating the stochastic time evolution of coupled chemical reactions J. Comp. Phys. 22 1976 403 434
59. A. Senior Catalytic sites of Escherichia coli F1-ATPase J. Bioenerg. Biomembr. 24 1992 479 483
60. D.A. Erie, T.D. Yager, and P.H. von Hippel The single-nucleotide addition cycle in transcription: a biophysical and biochemical perspective Annu. Rev. Biophys. Biomol. Struct. 21 1992 379 415
61. M. Zuker MFold web server for nucleic acid folding and hybridization prediction Nucl. Acids Res. 31 2003 3406 3415 (Pubitemid 37442169)
62. N. Sugimoto, and S. Nakano M. Sasaki Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes Biochemistry 34 1995 11211 11216