Constructing kinetic models to elucidate structural dynamics of a complete RNA polymerase II elongation cycle

Physical Biology

Volumn 12, Issue 1, 2015, Pages

  Yu, Jin ^a   Da, Lin Tai ^b,c   Huang, Xuhui ^c  

^a BEIJING COMPUTATIONAL SCIENCE RESEARCH CENTER   (China)

^b Florida State University   (United States)

^c HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

Brownian ratchet; kinetic modeling; molecular dynamics simulation; RNA polymerase II; single molecule experiment

Indexed keywords

EUKARYOTA;

RNA POLYMERASE II;

ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; GENETIC TRANSCRIPTION; HUMAN; KINETICS; METABOLISM; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; TRANSCRIPTION ELONGATION;

ANIMALS; COMPUTER SIMULATION; HUMANS; KINETICS; MODELS, GENETIC; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; RNA POLYMERASE II; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84923345998     PISSN: 14783967     EISSN: 14783975     Source Type: Journal    
DOI: 10.1088/1478-3975/12/1/016004     Document Type: Article

References (64)

1. Young R A 1991 RNA polymerase II Ann. Rev. Biochem. 60 689-715
2. Kostek S A, Grob P, De Carlo S, Lipscomb J S, Garczarek F and Nogales E 2006 Molecular architecture and conformational flexibility of human RNA polymerase II Structure 14 1691-700
3. Kornberg R D 2007 The molecular basis of eukaryotic transcription Proc. Natl Acad. Sci. USA 104 12955-61
4. Svetlov V and Nudler E 2013 Basic mechanism of transcription by RNA polymerase II Biochimica Biophysica Acta 1829 20-8
5. Kornberg R D 1999 Eukaryotic transcriptional control Trends Cell Biol. 9 M46-9
6. Sims R J III, Belotserkovskaya R and Reinberg D 2004 Elongation by RNA polymerase II: the short and long of it Genes Dev. 18 2437-68
7. Greive S J and von Hippel P H 2005 Thinking quantitatively about transcriptional regulation Nat. Rev. Mol. Cell Biol. 6 221-32
8. Fuda N J, Ardehali M B and Lis J T 2009 Defining mechanisms that regulate RNA polymerase II transcription in vivo Nature 461 186-92
9. Zhou Q, Li T and Price D H 2012 RNA polymerase II elongation control Ann. Rev. Biochem. 81 119-43
10. He Y, Fang J, Taatjes D J and Nogales E 2013 Structural visualization of key steps in human transcription initiation Nature 495 481-6
11. Cramer P, Bushnell D A and Kornberg R D 2001 Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution Science 292 1863-76
12. Gnatt A L, Cramer P, Fu J, Bushnell D A and Kornberg R D 2001 Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution Science 292 1876-82
13. Woychlk N A and Hampsey M 2002 The RNA polymerase II machinery: structue illuminates function Cell 108 453-63
14. Hahn S 2004 Structure and mechanism of the RNA polymerase II transcription machinery Nat. Struct. Mol. Biol. 11 394-403
15. Wang D, Bushnell D A, Westover K D, Kaplan C D and Kornberg R 2006 Structural basis for transcription: role of the trigger loop in substrate specificty and catalysis Cell 127 941-54
16. Brueckner F, Ortiz J and Cramer P 2009 A movie of the RNA polymerase nucleotide addition cycle Curr. Opin. Struct. Biol. 19 294-9
17. Wang D, Bushnell D A, Huang X, Westover K D, Levitt M and Kornberg R D 2009 Structural basis of transcription: backtracked RNA polymerase II at 3.4 angstrom resolution Science 324 1203-6
18. Kostrewa D, Zeller M E, Armache K-J, Seizl M, Leike K, Thomm M and Cramer P 2009 RNA polymerase II-TFIIB structure and mechanism of transcription initiation Nature 462 323-30
19. Liu X, Bushnell D A, Wang D, Calero G and Kornberg R D 2010 Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism Science 327 206-9
20. Martinez-Rucobo F W and Cramer P 2013 Structural basis of transcription elongation Biochimica Biophysica Acta 1829 9-19
21. Toulokhonov I, Zhang J, Palangat M and Landick R 2007 A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing Mol. Cell 27 406-19
22. Nudler E 2009 RNA polymerase active center: the molecular engine of transcription Ann. Rev. Biochem. 78 335-61
23. Huang X, Wang D, Weiss D R, Bushnell D A, Kornberg R D and Levitt M 2010 RNA polymerase II trigger loop residues stabilize and position the incoming nucleotide triphosphate in transcription Proc. Natl Acad. Sci. USA 107 15745-50
24. Zhang J, Palagnat M and Landick R 2010 Role of the RNA polymerase trigger loop in catalysis and pausing Nat. Struct. Mol. Biol. 17 99-104
25. Fouqueau T, Zeller M E, Cheung A C, Cramer P and Thomm M 2013 The RNA polymerase trigger loop functions in all three phases of the transcription cycle Nucleic Acids Res. 41 7048-59
26. Wang B, Predeus A V and Burton Z F 2013 Energetic and structural details of the trigger-loop closing transition in RNA polymerase II Biophys. J. 105 767-75
27. Hein P P and Landick R 2010 The bridge helix coordinates movements of modules in RNA polymerase BMC Biol. 8 141-4
28. Weinzierl R O J 2011 The bridge helix of RNA polymerase acts as a central nanomechanical switchboard for coordinating catalysis and substrate movement Archaea 2011 608385
29. Herbert K M, Greenleaf W J and Block S M 2008 Single-molecule studies of RNA polymerase: motoring along Ann. Rev. Biochem. 77 149-76
30. Selth L A, Sugurdsson S and Svejstrup J Q 2010 Transcript elongation by RNA polymerase II Ann. Rev. Biochem. 79 271-93
31. Kireeva M, Kashlev M and Burton Z F 2010 Translocation by multi-subunit RNA polymerases Biochimica Biophysica Acta 1799 389-401
32. Kaplan C D 2013 Basic mechanisms of RNA polymerase II activity and alteration of gene expression in Saccharomyces cerevisiae Biochimica Biophysica Acta 1829 39-54
33. Zhang S and Wang D 2013 Understanding the molecular basis of RNA polymerase II transcription Isr. J. Chem. 53 442-9
34. Larson M H, Zhou J, Kaplan C D, Palangat M, Kornberg R D, Landick R and Block S M 2012 Trigger loop dynamics mediate the balance between the transcriptional fidelity and speed of RNA polymerase II Proc. Natl Acad. Sci. USA 109 6555-60
35. Dangkulwanich M, Ishibashi T, Liu S, Kireeva M L, Lubkowska L, Kashlev M and Bustamante C 2013 Complete dissection of transcription elongation reveals slow translocation of RNA polymerase II in a linear ratchet mechanism eLIFE 2 e00971
36. Dangkulwanich M, Ishibashi T, Bintu L and Bustamante C 2014 Molecular mechanisms of transcription through single-molecule experiments Chem. Rev. 114 3203-23
37. Abbondanzieri E A, Greenleaf W J, Shaevitz J W, Landick R and Block S M 2005 Direct observation of base-pair stepping by RNA polymerase Nature 438 460-5
38. Bar-Nahum G, Epshtein V, Ruckenstein A E, Rafikov R, Mustaev A and Nudler E 2005 A ratchet mechanism of transcription elongation and its control Cell 120 183-93
39. Peskin C S, Odell G M and Oster G F 1993 Cellular motions and thermal fluctuations: the Brownian ratchet Biophys. J. 65 316-24
40. Feig M and Burton Z F 2009 RNA polymerase II flexibility during translocation from normal mode analysis Proteins 78 434-46
41. Feig M and Burton Z F 2010 RNA polymerase II flexibility during translocation from normal mode analysis Proteins 78 434-46
42. Feig B and Burton Z F 2010 RNA polymerase II with open and closed trigger loops: active site dynamics and nucleic acid translocation Biophys. J. 99 2577-86
43. Da L, Wang D and Huang X 2011 Dynamics of pyrophosphate ion release and its coupled trigger loop motion from closed to open state in RNA polymerase II J. Am. Chem. Soc. 134 2399-406
44. Da L-T, Pardo Avila F, Wang D and Huang X 2013 A two-state model for the dynamics of the pyrophosphate ion release in bacterial RNA polymerase PLoS Comput. Biol. 9 e1003020
45. Pardo-Avila F, Da L-T, Wang Y and Huang X 2013 Theoretical investigations on elucidating fundamental mechanisms of catalysis and dynamics involved in transcription by RNA polymerase J. Theor. Comput. Chem. 12 1341005
46. Kireeva M L, Opron K, Seibold S A, Domecq C, Cukier R I, Coulombe B, Kashlev M and Burton Z F 2012 Molecular dynamics and mutational analysis of the catalytic and translocation cycle of RNA polymerase BMC Biophys. 5 11-28
47. Wang B, Feig M, Cukier R I and Burton Z F 2013 Computational simulation strategies for analysis of multisubunit RNA polymerases Chem. Rev. 113 8546-66
48. Silva D A, Weiss D R, Pardo Avila F, Da L T, Levitt M, Wang D and Huang X 2014 Millisecond dynamics of RNA polymerase II translocation at atomic resolution Proc. Natl Acad. Sci. USA 111 7665-70
49. Meuzelaar H, Tros M, Huerta-Viga A, van Dijk C N, Vreede J and Woutersen S 2014 Solvent-exposed salt bridges influence the kinetics of α helix folding and unfolding J. Phys. Chem. Lett. 5 900-4
50. Vassylyev D G, Vassylyeva M N, Zhang J, Palangat M, Artsimovitch I and Landick I 2007 Structural basis for substrate loading in bacterial RNA polymerase Nature 448 163-8
51. Anand V S and Patel S S 2006 Transient state kinetics of transcription elongation by T7 RNA polymerase J. Biol. Chem. 281 35677-85
52. Foster J E, Holmes S F and Erie D A 2001 Allosteric binding of nucleotide triphosphate to RNA polymerase regulates transcription elongation Cell 106 243-52
53. Kellinger M W, Ulrich S, Chong J, Kool E T and Wang D 2012 Dissecting chemical interactions governing RNA polymerase II transcriptional fidelity J. Am. Chem. Soc. 134 8231-40
54. Imashimizu M and Kashelv M 2014 Unveiling translocation intermediates of RNA polymerase Proc. Natl Acad. Sci. USA 111 7507-8
55. Bai L, Shundrovsky A and Wang M D 2004 Sequence-dependent kinetic model for transcription elongation by RNA polymerase J. Mol. Biol. 344 335-49
56. Yager T D and Von Hippel P H 1991 A thermodynamic analysis of RNA transcript elongation and termination in Escherichia coli Biochemistry 30 1097-118
57. Bai L, Fulbright R M and Wang M D 2007 Mechanochemical kinetics of transcription elongation Phys. Rev. Lett. 98 068103
58. Murakami K S 2013 X-ray crystal structure of Escherichia coli RNA polymerase α70 holoenzyme J. Biol. Chem. 288 9126-34
59. Kireeva M L, Nedialkov Y A, Cremona G H, Purtov Y A, Lubkowska L, Malagon F, Burton Z F, Strathern J N and Kashlev M 2008 Transient reversal of RNA polymerase II active site closing controls fidelity of transcription elongation. Mol. Cell 30 557-66
60. Nedialkov Y A, Gong X Q, Hovde S L, Yamaguchi Y, Handa H, Geiger J H, Yan H and Burton Z F 2003 NTP-driven translocation by human RNA polymerase II. J. Biol. Chem. 278 18303-12
61. Batada N N, Westover K D, Bushnell D A, Levitt M and Kornberg R D 2004 Diffusion of nucleoside triphosphates and role of the entry site to the RNA polymerase II active center Proc. Natl Acad. Sci. USA 105 17361-4
62. Westover K D, Bushnell D A and Kornberg R D 2004 Structural basis of transcription: nucleotide selection by rotation in the RNA polymerase II active center Cell 119 481-9
63. Yu J and Oster G 2012 A small post-translocation energy bias aids nucleotide selection in T7 RNA polymerase transcription Biophys. J. 102 532-41
64. Morris G M, Huey R, Lindstrom W, Sanner M F, Belew R K, Goodsell D S and Olson A J 2009 Autodock4 and autodocktools4: automated docking with selective receptor flexibility J. Comput. Chem. 30 2785-91