A Jump-from-Cavity Pyrophosphate Ion Release Assisted by a Key Lysine Residue in T7 RNA Polymerase Transcription Elongation

PLoS Computational Biology

Volumn 11, Issue 11, 2015, Pages

  Da, Lin Tai ^a   E, Chao ^b   Duan, Baogen ^b   Zhang, Chuanbiao ^c   Zhou, Xin ^c   Yu, Jin ^b  

^a Florida State University   (United States)

^b BEIJING COMPUTATIONAL SCIENCE RESEARCH CENTER   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CHEMICAL ACTIVATION; ELONGATION; HYDROGEN BONDS; MOLECULAR DYNAMICS; RNA;

ACTIVATION PROCESS; CONFORMATIONAL CHANGE; COUPLING MECHANISM; DYNAMICS SIMULATION; ION RELEASE; LYSINE RESIDUES; MECHANOCHEMICAL COUPLINGS; POLYMERASE COMPLEX; RNA POLYMERASE; T7 RNA POLYMERASE;

TRANSCRIPTION;

ARGININE; ASPARTIC ACID DERIVATIVE; DNA POLYMERASE; HYDROGEN; LYSINE; PYROPHOSPHATE; RNA POLYMERASE; BACTERIOPHAGE T7 RNA POLYMERASE; DIPHOSPHORIC ACID; DNA DIRECTED RNA POLYMERASE; PYROPHOSPHORIC ACID DERIVATIVE; VIRAL PROTEIN;

ARTICLE; CATALYSIS; CHEMICAL INTERACTION; CHEMICAL PHENOMENA; DISSOCIATION; ENTEROBACTERIA PHAGE T7; ENZYME ACTIVATION; ENZYME STRUCTURE; HYDROGEN BOND; KINETICS; MOLECULAR DYNAMICS; MOLECULAR MODEL; PYROPHOSPHATE ION RELEASE; RESIDUE ANALYSIS; SIMULATION; TRANSCRIPTION ELONGATION; AMINO ACID SEQUENCE; BIOLOGY; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROMOTER REGION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; DIPHOSPHATES; DNA-DIRECTED RNA POLYMERASES; LYSINE; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; SEQUENCE ALIGNMENT; VIRAL PROTEINS;

EID: 84949194602     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004624     Document Type: Article

References (70)

1. Buc H, Strick T, , editors (2009) RNA polymerase as molecular motors. Cambridge, UK: The Royal Society of Chemistry.
2. Borukhov S, Nudler E, (2008) RNA polymerase: the vehicle of transcription. Trends in Microbiology 16: 126–134. doi: 10.1016/j.tim.2007.12.006 18280161
3. Bai L, Santangelo TJ, Wang MD, (2006) SINGLE-MOLECULE ANALYSIS OF RNA POLYMERASE TRANSCRIPTION. Annual Review of Biophysics and Biomolecular Structure 35: 343–360. 16689640
4. Eid J, Fehr A, Gray J, Luong K, Lyle J, et al. (2009) Real-Time DNA Sequencing from Single Polymerase Molecules. Science 323: 133–138. doi: 10.1126/science.1162986 19023044
5. Ronaghi M, Uhlén M, Nyrén P, (1998) A Sequencing Method Based on Real-Time Pyrophosphate. Science 281: 363–365. 9705713
6. Guo Q, Sousa R, (2006) Translocation by T7 RNA Polymerase: A Sensitively Poised Brownian Ratchet. Journal of Molecular Biology 358: 241–254. 16516229
7. Yin YW, Steitz TA, (2004) The Structural Mechanism of Translocation and Helicase Activity in T7 RNA Polymerase. Cell 116: 393–404. 15016374
8. Wang H-Y, Elston T, Mogilner A, Oster G, (1998) Force Generation in RNA Polymerase. Biophysical Journal 74: 1186–1202. 9512018
9. Gelles J, Landick R, (1998) RNA Polymerase as a Molecular Motor. Cell 93: 13–16. 9546386
10. Wang H, Oster G, (2002) Ratchets, power strokes, and molecular motors. Applied Physics A 75: 315–323.
11. Bustamante C, Keller D, Oster G, (2001) The physics of molecular motors. Accounts of Chemical Research 34: 412–420. 11412078
12. Dangkulwanich M, Ishibashi T, Liu S, Kireeva ML, Lubkowska L, et al. (2013) Complete dissection of transcription elongation reveals slow translocation of RNA polymerase II in a linear ratchet mechanism. eLIFE 2: e00971. doi: 10.7554/eLife.00971 24066225
13. Abbondanzieri EA, Greenleaf WJ, Shaevitz JW, Landick R, Block SM, (2005) Direct observation of base-pair stepping by RNA polymerase. Nature 438: 460–465. 16284617
14. Thomen P, Lopez PJ, Heslot F, (2005) Unravelling the Mechanism of RNA-Polymerase Forward Motion by Using Mechanical Force. Physical Review Letters 94: 128102. 15903965
15. Rong M, He B, McAllister WT, Durbin RK, (1998) Promoter specificity determinants of T7 RNA polymerase. PNAS 95: 515–519. 9435223
16. Shis DL, Bennett MR, (2014) Synthetic biology: the many facets of T7 RNA polymerase. Molecular Systems Biology 10: n/a–n/a.
17. Citorik RJ, Mimee M, Lu TK, (2014) Bacteriophage-based synthetic biology for the study of infectious diseases. Current Opinion in Microbiology 19: 59–69. doi: 10.1016/j.mib.2014.05.022 24997401
18. Steitz TA, (2009) The structural changes of T7 RNA polymerase from transcription initiation to elongation. Current Opinion in Structural Biology 19: 683–690. doi: 10.1016/j.sbi.2009.09.001 19811903
19. Temiakov D, Patlan V, Anikin M, McAllister WT, Yokoyama S, et al. (2004) Structural Basis for Substrate Selection by T7 RNA Polymerase. Cell 116: 381–391. 15016373
20. Thomen P, Lopez PJ, Bockelmann U, Guillerez J, Dreyfus M, et al. (2008) T7 RNA Polymerase Studied by Force Measurements Varying Cofactor Concentration. Biophysical Journal 95: 2423–2433. doi: 10.1529/biophysj.107.125096 18708471
21. Kim JH, Larson RG, (2007) Single-molecule analysis of 1D diffusion and transcription elongation of T7 RNA polymerase along individual stretched DNA molecules. Nucleic Acids Research: gkm332.
22. Tang G-Q, Roy R, Bandwar RP, Ha T, Patel SS, (2009) Real-time observation of the transition from transcription initiation to elongation of the RNA polymerase. Proceedings of the National Academy of Sciences 106: 22175–22180.
23. Anand VS, Patel SS, (2006) Transient State Kinetics of Transcription Elongation by T7 RNA Polymerase. The jouornal of biological chemistry 281: 35677–35685.
24. Sousa R, Mukherjee S, Kivie M, (2003) T7 RNA Polymerase. Progress in Nucleic Acid Research and Molecular Biology: Academic Press. pp. 1–41.
25. Da L-T, Pardo A, F., Wang D, Huang X, (2013) A Two-State Model for the Dynamics of the Pyrophosphate Ion Release in Bacterial RNA Polymerase. PloS Computational Biology 9: e1003020. doi: 10.1371/journal.pcbi.1003020 23592966
26. Da L, Wang D, Huang X, (2011) Dynamics of Pyrophosphate Ion Release and Its Coupled Trigger Loop Motion from Closed to Open State in RNA Polymerase II. Journal of the American Chemical Society 134: 2399–2406.
27. Da L-T, Sheong F, Silva D-A, Huang X, Han K-l, Zhang X, Yang M-j, (2014) Application of Markov State Models to Simulate Long Timescale Dynamics of Biological Macromolecules. In: Protein Conformational Dynamics: Springer International Publishing. pp. 29–66.
28. Chodera JD, Noé F, (2014) Markov state models of biomolecular conformational dynamics. Current Opinion in Structural Biology 25: 135–144. doi: 10.1016/j.sbi.2014.04.002 24836551
29. Pande VS, Beauchamp K, Bowman GR, (2010) Everything you wanted to know about Markov State Models but were afraid to ask. Methods (San Diego, Calif) 52: 99–105.
30. Noe F, Fischer S, (2008) Transition networks for modeling the kinetics of conformational change in macromolecules. Curr Opin Struct Biol 18: 154–162. doi: 10.1016/j.sbi.2008.01.008 18378442
31. Chodera JD, Singhal N, Pande VS, Dill KA, Swope WC, (2007) Automatic discovery of metastable states for the construction of Markov models of macromolecular conformational dynamics. J Chem Phys 126: 155101. 17461665
32. Zhuang W, Cui RZ, Silva DA, Huang X, (2011) Simulating the T-jump-triggered unfolding dynamics of trpzip2 peptide and its time-resolved IR and two-dimensional IR signals using the Markov state model approach. J Phys Chem B 115: 5415–5424. doi: 10.1021/jp109592b 21388153
33. Lane T, Bowman G, Beauchamp K, Voelz V, Pande V, (2011) Markov State Model Reveals Folding and Functional Dynamics in Ultra-Long MD Trajectories. Journal of the American Chemical Society 133: 18413–18419. doi: 10.1021/ja207470h 21988563
34. Huang X, Bowman GR, Bacallado S, Pande VS, (2009) Rapid equilibrium sampling initiated from nonequilibrium data. PNAS 106: 19765–19769. doi: 10.1073/pnas.0909088106 19805023
35. Kohlhoff KJ, Shukla D, Lawrenz M, Bowman GR, Konerding DE, et al. (2014) Cloud-based simulations on Google Exacycle reveal ligand modulation of GPCR activation pathways. Nat Chem 6: 15–21. doi: 10.1038/nchem.1821 24345941
36. Silva DA, Bowman GR, Sosa-Peinado A, Huang X, (2011) A Role for Both Conformational Selection and Induced Fit in Ligand Binding by the LAO Protein. PLos Computational Biology 7: e1002054. doi: 10.1371/journal.pcbi.1002054 21637799
37. Choudhary OP, Paz A, Adelman JL, Colletier JP, Abramson J, et al. (2014) Structure-guided simulations illuminate the mechanism of ATP transport through VDAC1. Nat Struct Mol Biol 21: 626–632. doi: 10.1038/nsmb.2841 24908397
38. Silva DA, Weiss DR, Pardo Avila F, Da LT, Levitt M, et al. (2014) Millisecond dynamics of RNA polymerase II translocation at atomic resolution. Proc Natl Acad Sci U S A 111: 7665–7670. doi: 10.1073/pnas.1315751111 24753580
39. Fouqueau T, Zeller ME, Cheung AC, Cramer P, Thomm M, (2013) The RNA polymerase trigger loop functions in all three phases of the transcription cycle. Nucleic Acids Research 41: 7048–7059. doi: 10.1093/nar/gkt433 23737452
40. Toulokhonov I, Zhang J, Palangat M, Landick R, (2007) A Central Role of the RNA Polymerase Trigger Loop in Active-Site Rearrangement during Transcriptional Pausing. Molecular Cell 27: 406–419. 17679091
41. Miller BR, IIIParish CA, Wu EY, (2014) Molecular Dynamics Study of the Opening Mechanism for DNA Polymerase I. PLos Computational Biology 10: e1003961. doi: 10.1371/journal.pcbi.1003961 25474643
42. Duan B, Wu S, Da L-T, Yu J, (2014) A Critical Residue Selectively Recruits Nucleotides for T7 RNA Polymerase Transcription Fidelity Control. Biophysical Journal 107: 2130–2140. doi: 10.1016/j.bpj.2014.09.038 25418098
43. Yu J, Oster G, (2012) A Small Post-translocation Energy Bias Aids Nucleotide Selection in T7 RNA Polymerase Transcription. Biophysical Journal 102: 532–541. doi: 10.1016/j.bpj.2011.12.028 22325276
44. Golosov A, Warren J, Beese L, Karplus M, (2010) The Mechanism of the Translocation Step in DNA Replication by DNA Polymerase I: A Computer Simulation Analysis. Structure 18: 83–93. doi: 10.1016/j.str.2009.10.014 20152155
45. Woo H-J, Liu Y, Sousa R, (2008) Molecular dynamics studies of the energetics of translocation in model T7 RNA polymerase elongation complexes. Proteins: Structure, Function, and Bioinformatics 73: 1021–1036.
46. Florián J, Goodman MF, Warshel A, (2005) Computer simulations of protein functions: Searching for the molecular origin of the replication fidelity of DNA polymerases. Proceedings of the National Academy of Sciences of the United States of America 102: 6819–6824. 15863620
47. Schlick T, Arora K, Beard WA, Wilson SH, (2012) Perspective: pre-chemistry conformational changes in DNA polymerase mechanisms. Theoretcial Chemistry Accounts 131: 1287.
48. Steitz TA, (1999) DNA Polymerases: Structural Diversity and Common Mechanisms. Journal of Biological Chemistry 274: 17395–17398. 10364165
49. Sosunov V, Zorov S, Sosunova E, Nikolaev A, Zakeyeva I, et al. (2005) The involvement of the aspartate triad of the active center in all catalytic activities of multisubunit RNA polymerase. Nucleic Acids Research 33: 4202–4211. 16049026
50. Yin YW, Steitz TA, (2002) Structural Basis for the Transition from Initiation to Elongation Transcription in T7 RNA Polymerase. Science 298: 1387–1395. 12242451
51. Gong L, Zhou X, Ouyang Z, (2015) Systematically Constructing Kinetic Transition Network in Polypeptide from Top to Down: Trajectory Mapping. PLos One 10: e0125932. doi: 10.1371/journal.pone.0125932 25962177
52. McWilliam H, Li W, Uludag M, Squizzato S, Park YM, et al. (2013) Analysis Tool Web Services from the EMBL-EBI. Nucleic acids research 41: W597–600. doi: 10.1093/nar/gkt376 23671338
53. Eargle J, Wright D, Luthey-Schulten Z, (2006) Multiple Alignment of protein structures and sequences for VMD. Bioinformatics 22: 504–506. 16339280
54. Salomon-Ferrer R, Case DA, Walker RC, (2012) An overview of the Amber biomolecular simulation package. Wiley Interdisciplinary Reviews: Computational Molecular Science 3: 198–210.
55. Dupradeau FY, Pigache A, Zaffran T, Savineau C, Lelong R, et al. (2010) The R.E.D. tools: advances in RESP and ESP charge derivation and force field library building. Phys Chem Chem Phys 12: 7821–7839. doi: 10.1039/c0cp00111b 20574571
56. Wang J, Wang W, Kollman PA, Case DA, (2006) Automatic atom type and bond type perception in molecular mechanical calculations. Journal of Molecular Graphics and Modelling 25: 247260.
57. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA, (2004) Development and testing of a general AMBER force field. Journal of Computational Chemistry 25: 1157–1174. 15116359
58. Hess B, Kutzner C, van der Spoel D, Lindahl E, (2008) GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. Journal of Chemical Theory and Computation 4: 435–447.
59. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins: Structure, Function, and Bioinformatics 65: 712–725.
60. Joung IS, Cheatham TE, (2009) Molecular Dynamics Simulations of the Dynamic and Energetic Properties of Alkali and Halide Ions Using Water-Model-Specific Ion Parameters. The Journal of Physical Chemistry B 113: 13279–13290. doi: 10.1021/jp902584c 19757835
61. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, et al. (1995) A smooth particle mesh Ewald method. The Journal of Chemical Physics 103: 8577–8593.
62. Bussi G, Donadio D, Parrinello M, (2007) Canonical sampling through velocity rescaling. The Journal of Chemical Physics 126: -.
63. Parrinello M, Rahman A, (1981) Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics 52: 7182–7190.
64. Nosé S, Klein ML, (1983) Constant pressure molecular dynamics for molecular systems. Molecular Physics 50: 1055–1076.
65. Isralewitz B, Gao M, Schulten K, (2001) Steered molecular dynamics and mechanical functions of proteins. Current Opinion in Structural Biology 11: 224–230. 11297932
66. Bowman GR, Huang X, Pande VS, (2009) Using generalized ensemble simulations and Markov state models to identify conformational states. Methods 49: 197–201. doi: 10.1016/j.ymeth.2009.04.013 19410002
67. Beauchamp KA, Bowman GR, Lane TJ, Maibaum L, Haque IS, et al. (2011) MSMBuilder2: Modeling Conformational Dynamics at the Picosecond to Millisecond Scale. Journal of chemical theory and computation 7: 3412–3419. 22125474
68. Bowman G, Livesay DR, (2014) A Tutorial on Building Markov State Models with MSMBuilder and Coarse-Graining Them with BACE. In: Protein Dynamics: Humana Press. pp. 141–158.
69. Noé F, Schütte C, Vanden-Eijnden E, Reich L, Weikl TR, (2009) Constructing the equilibrium ensemble of folding pathways from short off-equilibrium simulations. Proceedings of the National Academy of Sciences 106: 19011–19016.
70. Deuflhard P, Weber M, (2005) Robust Perron cluster analysis in conformation dynamics. Linear Algebra Appl 398: 161–184.