Molecular dynamics studies of the energetics of translocation in model T7 RNA polymerase elongation complexes

Proteins: Structure, Function and Genetics

Volumn 73, Issue 4, 2008, Pages 1021-1036

  Woo, Hyung June ^a   Liu, Yuemin ^a   Sousa, Rui ^b  

^a UNIVERSITY OF NEVADA   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Elongation phase; Free energy; Molecular dynamics; RNA polymerase; Translocation

Indexed keywords

ELONGATION FACTOR; MAGNESIUM ION; NUCLEOTIDE; PYROPHOSPHATE; RNA POLYMERASE; DNA; DNA DIRECTED RNA POLYMERASE;

ARTICLE; BASE PAIRING; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA RNA HYBRIDIZATION; ENERGY TRANSFER; ENZYME ACTIVE SITE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; RNA CONFORMATION; RNA TRANSPORT; SIMULATION; THERMODYNAMICS; BACTERIOPHAGE T7; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; ENZYMOLOGY; GENETIC TRANSCRIPTION; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLIABILITY; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIOPHAGE T7; BASE SEQUENCE; BIOLOGICAL TRANSPORT; COMPUTER SIMULATION; DNA; DNA-DIRECTED RNA POLYMERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLIABILITY; THERMODYNAMICS; TRANSCRIPTION, GENETIC;

EID: 58149286535     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22134     Document Type: Article

References (44)

1. von Hippel PH. An integrated model of the transcription complex in elongation, termination, and editing. Science 1998;281:660-665. (Pubitemid 28387269)
2. Gelles J, Landick R. RNA polymerase as a molecular motor. Cell 1998;93:13-16.
3. Steitz TA. Visualizing polynucleotide polymerase machines at work. EMBO J 2006;25:3458-3468. (Pubitemid 44264857)
4. Sousa R, Chung YJ, Rose JP, Wang BC. Crystal structure of bacteriophage T7 RNA polymerase at 3.3 Å resolution. Nature 1993;364: 593-599. (Pubitemid 23274714)
5. Guo Q, Sousa R. Translocation by T7 RNA polymerase: a sensitively poised Brownian ratchet. J Mol Biol 2006;358:241-254.
6. Guajardo R, Sousa R. A model for the mechanism of polymerase translocation. J Mol Biol 1997;265:8-19.
7. Mukherjee S, Brieba LG, Sousa R. Structural transitions mediating transcription initiation by T7 RNA polymerase. Cell 2002;110:81-91. (Pubitemid 34874608)
8. Yin YW, Steitz TA. Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase. Science 2002;298:1387-1395. (Pubitemid 35346133)
9. Tahirov TH, Temiakov D, Anikin M, Patlan V, McAllister WT, Vassylyev DG, Yokoyama S. Structure of a T7 RNA polymerase elongation complex at 2.9 Å resolution. Nature 2002;420:43-50. (Pubitemid 35291434)
10. Yin YW, Steitz TA. The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell 2004;116:393-404. (Pubitemid 38366316)
11. Temiakov D, Patlan V, Anikin M, McAllister WT, Yokoyama S, Vassylyev DG. Structural basis for substrate selection by T7 RNA polymerase. Cell 2004;116:381-391. (Pubitemid 38366315)
12. Cheetham GMT, Steitz TA. Structure of a transcribing T7 RNA polymerase initiation complex. Science 1999;286:2305-2309. (Pubitemid 30016883)
13. Theis K, Gong P, Martin CT. Topological and conformational analysis of the initiation and elongation complex of T7 RNA polymerase suggests a new twist. Biochemistry 2004;43:12709-12715. (Pubitemid 39331789)
14. Yarnell WS, Roberts JW. Mechanism of intrinsic transcription termination and antitermination. Science 1999;284:611-615. (Pubitemid 29289580)
15. Zhou Y, Navaroli DM, Enuameh MS, Martin CT. Dissociation of halted T7 RNA polymerase elongation complexes proceeds via a forward-translocation mechanism. Proc Natl Acad Sci USA 2007; 104:10352-10357. (Pubitemid 47185669)
16. Bar-Nahum G, Epshtein V, Ruckenstein AE, Rafikov R, Mustaev A, Nudler E. A ratchet mechanism of transcription elongation and its control. Cell 2005;120:183-193. (Pubitemid 40174762)
17. Vassylyev DG, Artsimovitch I. Tracking RNA polymerase, one step at a time. Cell 2005;123:977-979. (Pubitemid 41785410)
18. Bai L, Shundrovsky A, Wang MD. Sequence-dependent kinetic model for transcription elongation by RNA polymerase. J Mol Biol 2004;344:335-349. (Pubitemid 39441208)
19. Thomen P, Lopez PJ, Heslot F. Unraveling the mechanism of RNApolymerase forward motion by using mechanical force. Phys Rev Lett 2005;94:128102.
20. Abbondanzieri EA, Greenleaf WJ, Shaevitz JW, Landick R, Block SM. Direct observation of base-pair stepping by RNA polymerase. Nature 2005;438:460-465. (Pubitemid 41742012)
21. Bai L, Santangelo TJ, Wang MD. Single-molecule analysis of RNA polymerase transcription. Annu Rev Biophys Biomol Struct 2006; 35:343-360. (Pubitemid 43877382)
22. Woo HJ. Analytical theory of the nonequilibrium spatial distribution of RNA polymerase translocations. Phys Rev E 2006;74:011907.
23. Torrie GM, Valleau JP. Non-physical sampling distributions in Monte-Carlo free-energy estimation-umbrella sampling. J Comput Phys 1977;23:187-199.
24. Kumar S, Bouzida D, Swendsen RH, Kollman PA, Rosenberg JM. The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J Comput Chem 1992;13: 1011-1021.
25. Souaille M, Roux B. Extension to the weighted histogram analysis method: combining umbrella sampling with free energy calculations. Comp Phys Comm 2001;135:40-57. (Pubitemid 32265281)
26. Bernèche S, Roux B. A microscopic view of ion conduction through the K1 channels. Proc Natl Acad Sci USA 2003;100:8644-8648. (Pubitemid 36899151)
27. Banavali NK, Roux B. The N-terminal end of the catalytic domain of Src kinase Hck is a conformational switch implicated in longrange allosteric regulation. Structure 2005;13:1715-1723. (Pubitemid 41571835)
28. Banavali NK, Roux B. Free energy landscape of A-DNA to B-DNA conversion in aqueous solution. J Am Chem Soc 2005;127:6866-6876. (Pubitemid 40664194)
29. Huang N, Banavali NK, MacKerell AD Jr. Protein-facilitated base flipping in DNA by cytosine-5-methyltransferase. Proc Natl Acad Sci USA 2003;100:68-73. (Pubitemid 36078031)
30. Guex N, Peitsch MC. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 1997;18:2714-2723. (Pubitemid 28059943)
31. 4 and Cl from statistical perturbation theory. Chem Phys 1989;129:193-200.
32. Drew HR, Wing RM, Takano T, Broka C, Tanaka S, Itakura K, Dickerson RE. Structure of a B-DNA dodecamer: conformation and dynamics. Proc Natl Acad Sci USA 1981;78:2179-2183.
33. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 1983;4: 187-217.
34. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102: 3586-3616. (Pubitemid 128576688)
35. Foloppe N, MacKerell AD Jr. All-atom empirical force field for nucleic acids. I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J Comput Chem 2000;21:86-104.
36. MacKerell AD Jr, Banavali NK. All-atom empirical force field for nucleic acids. II. Application to molecular dynamics simulations of DNA and RNA in solution. J Comput Chem 2000;21:105-120.
37. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Phys 1995;103: 8577-8593.
38. Im W, Bernèche S, Roux B. Generalized solvent boundary potential for computer simulations. J Chem Phys 2001;114:2924-2937. (Pubitemid 32253408)
39. Nina M, Im W, Roux B. Optimized atomic radii for protein continuum electrostatics solvation forces. Biophys Chem 1999;78:89-96. (Pubitemid 29206659)
40. Sousa R, Rose J, Wang BC. The thumbs's knuckle: flexibility in the thumb subdomain of T7 RNA polymerease is revealed by the structure of a T7/T3 RNA polymerase. J Mol Biol 1994;244: 6-12. (Pubitemid 124002206)
41. Jeruzalmi D, Steitz TA. Structure of T7 RNA polymerase complexed to the transcriptional inhibitor T7 lysozyme. EMBO J 1998;17:4101-4113. (Pubitemid 28333994)
42. Tadigotla VR, Maoiléidigh DÓ, Sengupta AM, Epshtein V, Ebright RH, Nudler E, Ruckenstein AE. Thermodynamic and kinetic modeling of transcriptional pausing. Proc Natl Acad Sci USA 2006;103:4439-4444.
43. Shaevitz JW, Abbondanzieri EA, Landick R, Block SM. Backtracking by single RNA polymerase molecules observed at near-base-pair resolution. Nature 2003;426:684-687. (Pubitemid 38009379)
44. Herbert K, La Porta A, Wong BJ, Mooney RA, Neuman KC, Landick R, Block SM. Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 2006;125:1083-1094. (Pubitemid 43866198)