Structure-based simulations of the translocation mechanism of the Hepatitis C virus NS3 helicase along single-stranded nucleic acid

Biophysical Journal

Volumn 103, Issue 6, 2012, Pages 1343-1353

  Zheng, Wenjun ^a   Tekpinar, Mustafa ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APOPROTEIN; NS3 PROTEIN, HEPATITIS C VIRUS; PHOSPHATE; SINGLE STRANDED DNA; VIRUS PROTEIN;

ARTICLE; CHEMISTRY; CONFORMATION; ENZYMOLOGY; HEPATITIS C VIRUS; METABOLISM; MOLECULAR DYNAMICS; MOVEMENT (PHYSIOLOGY); PROTEIN TERTIARY STRUCTURE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APOPROTEINS; DNA, SINGLE-STRANDED; HEPACIVIRUS; MOLECULAR DYNAMICS SIMULATION; MOVEMENT; NUCLEIC ACID CONFORMATION; PHOSPHATES; PROTEIN STRUCTURE, TERTIARY; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS;

EID: 84866503271     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.08.026     Document Type: Article

References (62)

1. R. De Francesco, and G. Migliaccio Challenges and successes in developing new therapies for hepatitis C Nature 436 2005 953 960 (Pubitemid 41191671)
2. R.S. Brown Jr., and P.J. Gaglio Scope of worldwide hepatitis C problem Liver Transpl. 9 2003 S10 S13
3. D.N. Frick Helicases as antiviral drug targets Drug News Perspect. 16 2003 355 362 (Pubitemid 37221188)
4. A.E. Gorbalenya, and E.V. Koonin V.M. Blinov Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes Nucleic Acids Res. 17 1989 4713 4730 (Pubitemid 19165040)
5. K.D. Raney, and S.D. Sharma C.E. Cameron Hepatitis C virus non-structural protein 3 (HCV NS3): a multifunctional antiviral target J. Biol. Chem. 285 2010 22725 22731
6. V. Serebrov, and A.M. Pyle Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase Nature 430 2004 476 480 (Pubitemid 38987912)
7. W. Cheng, and S. Dumont C. Bustamante NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork Proc. Natl. Acad. Sci. USA 104 2007 13954 13959 (Pubitemid 350003319)
8. V. Serebrov, R.K. Beran, and A.M. Pyle Establishing a mechanistic basis for the large kinetic steps of the NS3 helicase J. Biol. Chem. 284 2009 2512 2521
9. D.N. Frick The hepatitis C virus NS3 protein: a model RNA helicase and potential drug target Curr. Issues Mol. Biol. 9 2007 1 20 (Pubitemid 46139067)
10. A.M. Pyle Translocation and unwinding mechanisms of RNA and DNA helicases Annu. Rev. Biophys 37 2008 317 336
11. J.L. Kim, and K.A. Morgenstern P.R. Caron Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding Structure 6 1998 89 100 (Pubitemid 28084402)
12. N. Yao, and P. Reichert P.C. Weber Molecular views of viral polyprotein processing revealed by the crystal structure of the hepatitis C virus bifunctional protease-helicase Structure 7 1999 1353 1363 (Pubitemid 29529876)
13. N. Yao, and T. Hesson P.C. Weber Structure of the hepatitis C virus RNA helicase domain Nat. Struct. Biol. 4 1997 463 467 (Pubitemid 27263599)
14. H.S. Cho, and N.C. Ha B.H. Oh Crystal structure of RNA helicase from genotype 1b hepatitis C virus. A feasible mechanism of unwinding duplex RNA J. Biol. Chem. 273 1998 15045 15052
15. M. Gu, and C.M. Rice Three conformational snapshots of the hepatitis C virus NS3 helicase reveal a ratchet translocation mechanism Proc. Natl. Acad. Sci. USA 107 2010 521 528
16. T.C. Appleby, and R. Anderson J.R. Somoza Visualizing ATP-dependent RNA translocation by the NS3 helicase from HCV J. Mol. Biol. 405 2011 1139 1153
17. S.S. Velankar, and P. Soultanas D.B. Wigley Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism Cell 97 1999 75 84 (Pubitemid 29165891)
18. J.Y. Lee, and W. Yang UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke Cell 127 2006 1349 1360 (Pubitemid 44960421)
19. S. Myong, and M.M. Bruno T. Ha Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase Science 317 2007 513 516 (Pubitemid 47196115)
20. W. Cheng, and S.G. Arunajadai C. Bustamante Single-base pair unwinding and asynchronous RNA release by the hepatitis C virus NS3 helicase Science 333 2011 1746 1749
21. V. Rajagopal, and M. Gurjar S.S. Patel The protease domain increases the translocation stepping efficiency of the hepatitis C virus NS3-4A helicase J. Biol. Chem. 285 2010 17821 17832
22. M.K. Levin, M. Gurjar, and S.S. Patel A Brownian motor mechanism of translocation and strand separation by hepatitis C virus helicase Nat. Struct. Mol. Biol. 12 2005 429 435 (Pubitemid 43085903)
23. M.D. Betterton, and F. Jülicher A motor that makes its own track: helicase unwinding of DNA Phys. Rev. Lett. 91 2003 258103
24. J. Yu, and W. Cheng G. Oster Coupling translocation with nucleic acid unwinding by NS3 helicase J. Mol. Biol. 404 2010 439 455
25. J. Yu, T. Ha, and K. Schulten Structure-based model of the stepping motor of PcrA helicase Biophys. J. 91 2006 2097 2114 (Pubitemid 44352393)
26. J. Yu, T. Ha, and K. Schulten How directional translocation is regulated in a DNA helicase motor Biophys. J. 93 2007 3783 3797 (Pubitemid 350223797)
27. V. Tozzini Coarse-grained models for proteins Curr. Opin. Struct. Biol. 15 2005 144 150
28. A.R. Atilgan, and S.R. Durell I. Bahar Anisotropy of fluctuation dynamics of proteins with an elastic network model Biophys. J. 80 2001 505 515
29. F. Tama, and Y.H. Sanejouand Conformational change of proteins arising from normal mode calculations Protein Eng. 14 2001 1 6 (Pubitemid 32318932)
30. K. Hinsen Analysis of domain motions by approximate normal mode calculations Proteins 33 1998 417 429 (Pubitemid 28516346)
31. M.M. Tirion Large amplitude elastic motions in proteins from a single-parameter, atomic analysis Phys. Rev. Lett. 77 1996 1905 1908 (Pubitemid 126625816)
32. W.G. Krebs, and V. Alexandrov M. Gerstein Normal mode analysis of macromolecular motions in a database framework: developing mode concentration as a useful classifying statistic Proteins 48 2002 682 695 (Pubitemid 34925457)
33. I. Bahar, and A.J. Rader Coarse-grained normal mode analysis in structural biology Curr. Opin. Struct. Biol. 15 2005 586 592 (Pubitemid 41393491)
34. W. Zheng, B.R. Brooks, and D. Thirumalai Allosteric transitions in biological nanomachines are described by robust normal modes of elastic networks Curr. Protein Pept. Sci. 10 2009 128 132
35. W. Zheng, and B. Brooks Identification of dynamical correlations within the myosin motor domain by the normal mode analysis of an elastic network model J. Mol. Biol. 346 2005 745 759 (Pubitemid 40247715)
36. W. Zheng, and B.R. Brooks Probing the local dynamics of nucleotide-binding pocket coupled to the global dynamics: myosin versus kinesin Biophys. J. 89 2005 167 178 (Pubitemid 41098273)
37. B.T. Miller, and W. Zheng B.R. Brooks Langevin network model of myosin J. Phys. Chem. B 112 2008 6274 6281
38. W. Zheng, and D. Thirumalai Coupling between normal modes drives protein conformational dynamics: illustrations using allosteric transitions in myosin II Biophys. J. 96 2009 2128 2137
39. W. Zheng Coarse-grained modeling of conformational transitions underlying the processive stepping of myosin V dimer along filamentous actin Proteins 79 2011 2291 2305
40. W. Zheng Multiscale modeling of structural dynamics underlying force generation and product release in actomyosin complex Proteins 78 2010 638 660
41. W. Zheng, and S. Doniach A comparative study of motor-protein motions by using a simple elastic-network model Proc. Natl. Acad. Sci. USA 100 2003 13253 13258 (Pubitemid 37444728)
42. I. Navizet, R. Lavery, and R.L. Jernigan Myosin flexibility: structural domains and collective vibrations Proteins 54 2004 384 393 (Pubitemid 38197353)
43. H. Yu, and L. Ma Q. Cui Mechanochemical coupling in the myosin motor domain. II. Analysis of critical residues PLOS Comput. Biol. 3 2007 e23
44. W. Zheng, B.R. Brooks, and G. Hummer Protein conformational transitions explored by mixed elastic network models Proteins 69 2007 43 57 (Pubitemid 47339138)
45. M. Tekpinar, and W. Zheng Predicting order of conformational changes during protein conformational transitions using an interpolated elastic network model Proteins 78 2010 2469 2481
46. W. Zheng, and M. Tekpinar Large-scale evaluation of dynamically important residues in proteins predicted by the perturbation analysis of a coarse-grained elastic model BMC Struct. Biol. 9 2009 45
47. W. Zheng Coarse-grained modeling of the structural states and transition underlying the powerstroke of dynein motor domain J. Chem. Phys. 136 2012 155103
48. 1 ATPase Proteins 76 2009 747 762
49. H. Flechsig, and A.S. Mikhailov Tracing entire operation cycles of molecular motor hepatitis C virus helicase in structurally resolved dynamical simulations Proc. Natl. Acad. Sci. USA 107 2010 20875 20880
50. H. Flechsig, D. Popp, and A.S. Mikhailov In silico investigation of conformational motions in superfamily 2 helicase proteins PLoS ONE 6 2011 e21809
51. W. Zheng, and J.C. Liao S. Doniach Toward the mechanism of dynamical couplings and translocation in hepatitis C virus NS3 helicase using elastic network model Proteins 67 2007 886 896 (Pubitemid 46753936)
52. W. Zheng Computer modeling of helicases using elastic network model Methods Mol. Biol. 587 2010 235 243
53. J. Hafner, and W. Zheng Optimal modeling of atomic fluctuations in protein crystal structures for weak crystal contact interactions J. Chem. Phys. 132 2010 014111
54. D. Ming, and M.E. Wall Allostery in a coarse-grained model of protein dynamics Phys. Rev. Lett. 95 2005 198103
55. W. Zheng A unification of the elastic network model and the Gaussian network model for optimal description of protein conformational motions and fluctuations Biophys. J. 94 2008 3853 3857
56. J.C. Phillips, and R. Braun K. Schulten Scalable molecular dynamics with NAMD J. Comput. Chem. 26 2005 1781 1802 (Pubitemid 43078511)
57. A.D. MacKerell Jr., N. Banavali, and N. Foloppe Development and current status of the CHARMM force field for nucleic acids Biopolymers 56 2000-2001 257 265 (Pubitemid 34105873)
58. W.G. Krebs, and M. Gerstein The Morph server: a standardized system for analyzing and visualizing macromolecular motions in a database framework Nucleic Acids Res. 28 2000 1665 1675 (Pubitemid 30199298)
59. J. Franklin, and P. Koehl M. Delarue MinActionPath: maximum likelihood trajectory for large-scale structural transitions in a coarse-grained locally harmonic energy landscape Nucleic Acids Res. 35 Web Server issue 2007 W477-W82
60. W. Zheng Accurate flexible fitting of high-resolution protein structures into cryo-electron microscopy maps using coarse-grained pseudo-energy minimization Biophys. J. 100 2011 478 488
61. W. Zheng, and M. Tekpinar Accurate flexible fitting of high-resolution protein structures to small-angle x-ray scattering data using a coarse-grained model with implicit hydration shell Biophys. J. 101 2011 2981 2991
62. C. Lin, and J.L. Kim Structure-based mutagenesis study of hepatitis C virus NS3 helicase J. Virol. 73 1999 8798 8807 (Pubitemid 29441745)