Genotype-specific differences in structural features of hepatitis C virus (HCV) p7 membrane protein

Biochimica et Biophysica Acta - Biomembranes

Volumn 1848, Issue 6, 2015, Pages 1383-1392

  Kalita, Monoj Mon ^a   Griffin, Stephen ^b   Chou, James J ^c   Fischer, Wolfgang B ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Channel gating; Genotypes; Molecular dynamics simulation; NMR structure; p7 of HCV; Viral channel protein

Indexed keywords

PROTEIN VP7; AMINO ACID; P7 PROTEIN, HEPATITIS C VIRUS; PROTON; VIRUS PROTEIN; WATER;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; GENOTYPE; HEPATITIS C VIRUS; LIPID BILAYER; MOLECULAR DYNAMICS; MOLECULAR MODEL; PH; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; SIMULATION; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; GENETICS; HEPACIVIRUS; METABOLISM; MOLECULAR GENETICS; PERMEABILITY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

HEPATITIS C VIRUS;

AMINO ACID SEQUENCE; AMINO ACIDS; COMPUTER SIMULATION; GENOTYPE; HEPACIVIRUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PERMEABILITY; PROTEIN STRUCTURE, TERTIARY; PROTONS; SEQUENCE ALIGNMENT; VIRAL PROTEINS; WATER;

EID: 84925430584     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.03.006     Document Type: Article

References (59)

1. W.B. Fischer, and M.S.P. Sansom Viral ion channels: structure and function Biochim. Biophys. Acta 1561 2002 27 45
2. M.E. Gonzales, and L. Carrasco Viroporins FEBS Lett. 552 2003 28 34
3. K. Wang, S. Xie, and B. Sun Viral proteins function as ion channels Biochim. Biophys. Acta 1808 2010 510 515
4. W.B. Fischer, Y.-T. Wang, C. Schindler, and C.-P. Chen Mechanism of function of viral channel proteins and implications for drug development Int. Rev. Cell Mol. Biol. 294 2012 259 321
5. J.L. Nieva, V. Madan, and L. Carrasco Viroporins: structure and biological functions Nat. Rev. Microbiol. 10 2012 563 574
6. B. OuYang, and J.J. Chou The minimalist architectures of viroporins and their therapeutic implications Biochim. Biophys. Acta 1838 2014 1058 1067
7. K.C. Duff, and R.H. Ashley The transmembrane domain of influenza A M2 protein forms amantadine-sensitive proton channels in planar lipid bilayers Virology 190 1992 485 489
8. U. Schubert, A.V. Ferrer-Montiel, M. Oblatt-Montal, P. Henklein, K. Strebel, and M. Montal Identification of an ion channel activity of the Vpu transmembrane domain and its involvement in the regulation of virus release from HIV-1-infected cells FEBS Lett. 398 1996 12 18
9. C.-C. Chen, J. Krüger, I. Sramala, H.-J. Hsu, P. Henklein, Y.-M.A. Chen, and W.B. Fischer ORF 8a of severe acute respiratory syndrome coronavirus forms an ion channel: experiments and molecular dynamics simulations Biochim. Biophys. Acta 1808 2011 572 579
10. D. Pavlović, D.C.A. Neville, O. Argaud, B. Blumberg, R.A. Dwek, W.B. Fischer, and N. Zitzmann The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives Proc. Natl. Acad. Sci. U. S. A. 100 2003 6104 6108
11. S.D.C. Griffin, L.P. Beales, D.S. Clarke, O. Worsfold, S.D. Evans, J. Jäger, M.P.G. Harris, and D.J. Rowlands The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, amantadine FEBS Lett. 535 2003 34 38
12. A. Premkumar, L. Wilson, G.D. Ewart, and P.W. Gage Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride FEBS Lett. 557 2004 99 103
13. F.J.M. van Kuppeveld, W.J.G. Melchers, K. Kirkegaard, and J.R. Doedens Structure-function analysis of coxsackie B3 virus protein 2B Virology 227 1997 111 118
14. W. Lu, B.-J. Zheng, K. Xu, W. Schwarz, L. Du, C.K.L. Wong, J. Chen, S. Duan, V. Deubel, and B. Sun Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release Proc. Natl. Acad. Sci. U. S. A. 103 2006 12540 12545
15. L.F. Wetherill, K.K. Holmes, M. Verow, M. Müller, G. Howell, M. Harris, C. Fishwick, N. Stonehouse, R. Foster, G.E. Blair, S. Griffin, and A. Macdonald High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors J. Virol. 86 2012 5341 5351
16. C. Lin, B.D. Lindenbach, B.M. Pragai, D.W. McCourt, and C.M. Rice Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini J. Virol. 68 1994 5063 5073
17. K. Elbers, N. Tautz, P. Becher, D. Stoll, T. Rumenapf, and H.J. Thiel Processing in the pestivirus E2-NS2 region: identification of proteins p7 and E2p7 J. Virol. 70 1996 4131 4135
18. V. Lohmann, F. Korner, J. Koch, U. Herian, L. Theilmann, and R. Bartenschlager Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line Science 285 1999 110 113
19. A. Sakai, M. St. Claire, K. Faulk, S. Govindarajan, S.U. Emerson, R.H. Purcell, and J. Bukh The p7 polypeptide of hepatitis C virus is critical for infectivity and contains functionally important genotype-specific sequences Proc. Natl. Acad. Sci. U. S. A. 100 2003 11646 11651
20. E. Steinmann, F. Penin, S. Kallis, A.H. Patel, R. Bartenschlager, and T. Pietschmann Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions PLoS Pathog. 3 2007 962 971
21. C.T. Jones, C.L. Murray, D.K. Eastman, J. Tassello, and C.M. Rice Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus J. Virol. 81 2007 8374 8383
22. E. Steinmann, and T. Pietschmann Hepatitis C virus p7 - a viroporin crucial for virus assembly and emerging target for antiviral therapy Viruses 2 2010 2078 2095
23. G. Vieyres, J. Dubuisson, and T. Pietschmann Incorporation of hepatitis C virus E1 and E2 glycoproteins: the keystones on a peculiar virion Viruses 6 2014 1149 1187
24. J. Gentzsch, C. Brohm, E. Steinmann, M. Friesland, N. Menzel, G. Vieyres, P.M. Perin, A. Frentzen, L. Kaderali, and T. Pietschmann Hepatitis C virus p7 is critical for capsid-assembly and envelopment PLoS Pathog. 9 2013 e1003355
25. A.L. Wozniak, S. Griffin, D. Rowlands, M. Harris, M.-K. Yi, S.M. Lemon, and S.A. Weinman Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production PLoS Pathog. 6 2010 e1001087
26. D. Clarke, S. Griffin, L. Beales, C.S. Gelais, S. Burgess, M. Harris, and D. Rowlands Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus p7 protein in vitro J. Biol. Chem. 281 2006 37057 37068
27. G.A. Cook, and S.J. Opella NMR studies of the p7 protein from hepatitis C virus Eur. Biophys. J. 39 2010 1097 1104
28. R. Montserret, N. Saint, C. Vanbelle, A.G. Salvay, J.P. Simorre, C. Ebel, N. Sapay, J.-G. Renisio, A. Böckmann, E. Steinmann, T. Pietschmann, J. Dubuisson, C. Chipot, and F. Penin NMR structure and ion channel activity of the p7 protein from hepatitis C virus J. Biol. Chem. 285 2010 31446 31461
29. B. OuYang, S. Xie, M.J. Berardi, X. Zhao, J. Dev, W. Yu, B. Sun, and J.J. Chou Unusual architecture of the p7 channel from hepatitis C virus Nature 498 2013 521 525
30. G. Patargias, N. Zitzmann, R. Dwek, and W.B. Fischer Protein-protein interactions: modeling the hepatitis C virus ion channel p7 J. Med. Chem. 49 2006 648 655
31. P. Luik, C. Chew, J. Aittoniemi, J. Chang, P. Wentworth Jr., R. Dwek, P.C. Biggin, C. Vénien-Bryan, and N. Zitzmann The 3-dimensional structure of the hepatitis C virus p7 ion channel by electron microscopy Proc. Natl. Acad. Sci. U. S. A. 106 2009 12712 12716
32. J. Krüger, and W.B. Fischer Assembly of viral membrane proteins J. Chem. Theory Comput. 5 2009 2503 2513
33. H.-J. Hsu, and W.B. Fischer In silico investigations of possible routes of assembly of ORF 3a from SARS-CoV J. Mol. Model. 18 2011 501 514
34. A.L. Grice, I.D. Kerr, and M.S.P. Sansom Ion channels formed by HIV-1 Vpu: a modelling and simulation study FEBS Lett. 405 1997 299 304
35. W.B. Fischer, M. Pitkeathly, B.A. Wallace, L.R. Forrest, G.R. Smith, and M.S. Sansom Transmembrane peptide NB of influenza B: a simulation, structure, and conductance study Biochemistry 39 2000 12708 12716
36. T.W. Allen, O.S. Andersen, and B. Roux Molecular dynamics - potential of mean force calculations as a tool for understanding ion permeation and selectivity in narrow channels Biophys. Chem. 124 2006 251 267
37. J.S. Hub, and B.L. de Groot Mechanism of selectivity in aquaporins and aquaglycoporins Proc. Natl. Acad. Sci. U. S. A. 105 2008 1198 1203
38. C. Kutzner, H. Grubmüller, B.L. de Groot, and U. Zachariae Computational electrophysiology: the molecular dynamics of ion channel permeation and selectivity in atomistic detail Biophys. J. 101 2011 809 817
39. D.E. Chandler, F. Penin, K. Schulten, and C. Chipot The p7 protein of hepatitis C virus forms structurally plastic, minimalist ion channels PLoS Comput. Biol. 8 2012 e1002702
40. T.L. Foster, M. Verow, A.L. Wozniak, M.J. Bentham, J. Thompson, E. Atkins, S.A. Weinmann, C. Fishwick, R. Foster, M. Harris, and S. Griffin Resistance mutations define specific antiviral effects for inhibitors of the hepatitis C virus p7 ion channel Hepatology 54 2011 79 90
41. M. Yanagi, M. St Claire, M. Shapiro, S.U. Emerson, R.H. Purcell, and J. Bukh Transcripts of a chimeric cDNA clone of hepatitis C virus genotype 1b are infectious in vivo Virology 244 1998 161 172
42. T.L. Foster, G.S. Thompson, A.P. Kalverda, J. Kankanala, M. Bentham, L.F. Wetherill, J. Thompson, A.M. Barker, D. Clarke, M. Noerenberg, A.R. Pearson, D.J. Rowlands, S.W. Homans, M. Harris, R. Foster, and S. Griffin Structure-guided design affirms inhibitors of hepatitis C virus p7 as a viable class of antivirals targeting virion release Hepatology 59 2014 408 422
43. I. Chandrasekhar, M. Kastenholz, R.D. Lins, C. Oostenbrink, L.D. Schuler, and W.F. van Gunsteren A consistent potential energy parameter set for lipids: dipalmitoylphosphatidylcholine as a benchmark of the GROMOS96 45A3 force field Eur. Biophys. J. 32 2003 67 77
44. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity-rescaling J. Chem. Phys. 126 2007 014101
45. S. Nosé A unified formulation of the constant temperature molecular dynamics methods J. Chem. Phys. 81 1984 511 519
46. W.G. Hoover Canonical dynamics: equilibrium phase-space distributions Phys. Rev. A 31 1985
47. Y.-T. Wang, R. Schilling, R.H.A. Fink, and W.B. Fischer Ion-dynamics in HCV p7 hexameric bundles - a molecular dynamics simulation study Biophys. Chem. 192 2014 33 40
48. F.S. Cordes, A.D. Tustian, M.S. Sansom, A. Watts, and W.B. Fischer Bundles consisting of extended transmembrane segments of Vpu from HIV-1: computer simulations and conductance measurements Biochemistry 41 2002 7359 7365
49. G. Patargias, T. Barke, A. Watts, and W.B. Fischer Model generation of viral channel forming 2B protein bundles from polio and coxsackie viruses Mol. Membr. Biol. 26 2009 309 320
50. G.A. Cook, and S.J. Opella Secondary structure, dynamics, and architecture of the p7 membrane protein from hepatitis C virus by NMR spectroscopy Biochim. Biophys. Acta 1808 2011 1448 1453
51. G.A. Cook, L.A. Dawson, Y. Tian, and S.J. Opella Three-dimensional structure and interaction studies of hepatitis C virus p7 in 1,2-dihexanoyl-sn-glycero-3-phosphatidylcholine by solution nuclear magnetic resonance Biochemistry 52 2013 5295 5303
52. D.B. Smith, J. Bukh, C. Kuiken, A.S. Muerhoff, C.M. Rice, J.T. Stapleton, and P. Simmonds Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource Hepatology 59 2014 318 327
53. B.D. Lindenbach, and C.M. Rice The ins and outs of hepatitis C virus entry and assembly Nat. Rev. Microbiol. 11 2013 688 700
54. S. Haid, M.P. Windisch, R. Bartenschlager, and T. Pietschmann Mouse-specific residues of claudin-1 limit hepatitis C virus genotype 2a infection in a human hepatocyte cell line J. Virol. 84 2010 964 975
55. C. Hourioux, R. Patient, A. Morin, E. Blanchard, A. Moreau, S. Trassad, B. Giraudeau, and P. Roingeard The genotype 3-specific hepatitis C virus core protein residue phenylalanine 164 increases steatosis in an in vitro cellular model Gut 56 2007 1302 1308
56. R. Bartenschlager, M. Frese, and T. Pietschmann Novel insights into hepatitis C virus replication and persistence Adv. Virus Res. 63 2004 71 180
57. M. Müller, U. Grauschopf, T. Maier, R. Glockshuber, and N. Ban The structure of a cytolytic alpha-helical toxin pore reveals its assembly mechanism Nature 459 2009 726 730
58. H. Bayley Piercing insights Nature 459 2009 651 652
59. Z. Meshkat, M. Audsley, C. Beyer, E.J. Gowans, and G. Haqshenas Reverse genetic analysis of a putative, influenza virus M2 HXXXW-like motif in the p7 protein of hepatitis C virus J. Viral Hepat. 16 2009 187 194