Determinants of hepatitis C virus p7 ion channel function and drug sensitivity identified in vitro

Journal of Virology

Volumn 83, Issue 16, 2009, Pages 7970-7981

  StGelais, Corine ^a   Foster, Toshana L ^a   Verow, Mark ^a   Atkins, Elizabeth ^a   Fishwick, Colin W G ^a   Rowlands, David ^a   Harris, Mark ^a   Griffin, Stephen ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMANTADINE; ION CHANNEL; P7 PROTEIN; RIMANTADINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHRONIC HEPATITIS; CONTROLLED STUDY; DRUG SENSITIVITY; HEPATITIS C VIRUS; IN VITRO STUDY; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; SEQUENCE ANALYSIS; VIRUS INFECTION;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; VIRAL PROTEINS;

HEPATITIS C VIRUS;

EID: 67749139975     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00521-09     Document Type: Article

References (45)

1. Carrere-Kremer, S., C. Montpellier-Pala, L. Cocquerel, C. Wychowski, F. Penin, and J. Dubuisson. 2002. Subcellular localization and topology of the p7 polypeptide of hepatitis C virus. J. Virol. 76:3720-3730.
2. Chew, C. F., R. Vijayan, J. Chang, N. Zitzmann, and P. C. Biggin. 2009. Determination of pore-lining residues in the hepatitis C virus p7 protein. Biophys. J. 96:L10-L12.
3. Choo, Q. L., G. Kuo, A. J. Weiner, L. R. Overby, D. W. Bradley, and M. Houghton. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
4. Clarke, D., S. Griffin, L. Beales, C. S. Gelais, S. Burgess, M. Harris, and D. Rowlands. 2006. Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus p7 protein in vitro. J. Biol. Chem. 281:37057-37068.
5. Cocquerel, L., C. Wychowski, F. Minner, F. Penin, and J. Dubuisson. 2000. Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a major role in the processing, subcellular localization, and assembly of these envelope proteins. J. Virol. 74:3623-3633.
6. Deltenre, P., J. Henrion, V. Canva, S. Dharancy, F. Texier, A. Louvet, S. De Maeght, J. C. Paris, and P. Mathurin. 2004. Evaluation of amantadine in chronic hepatitis C: a meta-analysis. J. Hepatol. 41:462-473.
7. Duff, K. C., P. J. Gilchrist, A. M. Saxena, and J. P. Bradshaw. 1994. Neutron diffraction reveals the site of amantadine blockade in the influenza A M2 ion channel. Virology 202:287-293.
8. Engler, A., T. Stangler, and D. Willbold. 2002. Structure of human immunodeficiency virus type 1 Vpr(34-51) peptide in micelle containing aqueous solution. Eur. J. Biochem. 269:3264-3269.
9. Galloux, M., S. Libersou, N. Morellet, S. Bouaziz, B. Da Costa, M. Ouldali, J. Lepault, and B. Delmas. 2007. Infectious bursal disease virus, a non-enveloped virus, possesses a capsid-associated peptide that deforms and perforates biological membranes. J. Biol. Chem. 282:20774-20784.
10. Gandhi, C. S., K. Shuck, J. D. Lear, G. R. Dieckmann, W. F. DeGrado, R. A. Lamb, and L. H. Pinto. 1999. Cu(II) inhibition of the proton translocation machinery of the influenza A virus M2 protein. J. Biol. Chem. 274:5474-5482.
11. Griffin, S., D. Clarke, C. McCormick, D. Rowlands, and M. Harris. 2005. Signal peptide cleavage and internal targeting signals direct the hepatitis C virus p7 protein to distinct intracellular membranes. J. Virol. 79:15525-15536.
12. Griffin, S., C. Stgelais, A. M. Owsianka, A. H. Patel, D. Rowlands, and M. Harris. 2008. Genotype-dependent sensitivity of hepatitis C virus to inhibitors of the p7 ion channel. Hepatology 48:1779-1790.
13. Griffin, S. D., L. P. Beales, D. S. Clarke, O. Worsfold, S. D. Evans, J. Jaeger, M. P. Harris, and D. J. Rowlands. 2003. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, amantadine. FEBS Lett. 535:34-38.
14. Griffin, S. D., R. Harvey, D. S. Clarke, W. S. Barclay, M. Harris, and D. J. Rowlands. 2004. A conserved basic loop in hepatitis C virus p7 protein is required for amantadine-sensitive ion channel activity in mammalian cells but is dispensable for localization to mitochondria. J. Gen. Virol. 85:451-461.
15. Harada, T., N. Tautz, and H. J. Thiel. 2000. E2-p7 region of the bovine viral diarrhea virus polyprotein: processing and functional studies. J. Virol. 74:9498-9506.
16. Isherwood, B. J., and A. H. Patel. 2005. Analysis of the processing and transmembrane topology of the E2p7 protein of hepatitis C virus. J. Gen. Virol. 86:667-676.
17. Jing, X., C. Ma, Y. Ohigashi, F. A. Oliveira, T. S. Jardetzky, L. H. Pinto, and R. A. Lamb. 2008. Functional studies indicate amantadine binds to the pore of the influenza A virus M2 proton-selective ion channel. Proc. Natl. Acad. Sci. USA 105:10967-10972.
18. Johnson, V. G., P. J. Nicholls, W. H. Habig, and R. J. Youle. 1993. The role of proline 345 in diphtheria toxin translocation. J. Biol. Chem. 268:3514-3519.
19. Jones, C. T., C. L. Murray, D. K. Eastman, J. Tassello, and C. M. Rice. 2007. Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J. Virol. 81:8374-8383.
20. Kato, T., T. Date, M. Miyamoto, A. Furusaka, K. Tokushige, M. Mizokami, and T. Wakita. 2003. Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon. Gastroenterology 125:1808-1817.
21. Lindenbach, B. D., M. J. Evans, A. J. Syder, B. Wolk, T. L. Tellinghuisen, C. C. Liu, T. Maruyama, R. O. Hynes, D. R. Burton, J. A. McKeating, and C. M. Rice. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
22. Meshkat, Z., M. Audsley, C. Beyer, E. J. Gowans, and G. Haqshenas. 2009. Reverse genetic analysis of a putative, influenza virus M2 HXXXW-like motif in the p7 protein of hepatitis C virus. J. Viral Hepat. 16:187-194.
23. Moradpour, D., F. Penin, and C. M. Rice. 2007. Replication of hepatitis C virus. Nat. Rev. Microbiol. 5:453-463.
24. Okada, A., T. Miura, and H. Takeuchi. 2001. Protonation of histidine and histidine-tryptophan interaction in the activation of the M2 ion channel from influenza a virus. Biochemistry 40:6053-6060.
25. Patargias, G., N. Zitzmann, R. Dwek, and W. B. Fischer. 2006. Proteinprotein interactions: modeling the hepatitis C virus ion channel p7. J. Med. Chem. 49:648-655.
26. Pavlovic, D., D. C. Neville, O. Argaud, B. Blumberg, R. A. Dwek, W. B. Fischer, and N. Zitzmann. 2003. The hepatitis C virus p7 protein forms an ion channel that is inhibited by long-alkyl-chain iminosugar derivatives. Proc. Natl. Acad. Sci. USA 100:6104-6108.
27. Pawlotsky, J. M. 2006. Therapy of hepatitis C: from empiricism to eradication. Hepatology 43:S207-20.
28. Perez-Berna, A. J., J. Guillen, M. R. Moreno, A. Bernabeu, G. Pabst, P. Laggner, and J. Villalain. 2008. Identification of the membrane-active regions of hepatitis C virus p7 protein: biophysical characterization of the loop region. J. Biol. Chem. 283:8089-8101.
29. Pielak, R. M., J. R. Schnell, and J. J. Chou. 2009. Mechanism of drug inhibition and drug resistance of influenza A M2 channel. Proc. Natl. Acad. Sci. USA 106:7379-7384.
30. Pinto, L. H., G. R. Dieckmann, C. S. Gandhi, C. G. Papworth, J. Braman, M. A. Shaughnessy, J. D. Lear, R. A. Lamb, and W. F. DeGrado. 1997. A functionally defined model for the M2 proton channel of influenza A virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. USA 94:11301-11306.
31. Premkumar, A., L. Wilson, G. D. Ewart, and P. W. Gage. 2004. Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride. FEBS Lett. 557:99-103.
32. Sakai, A., M. S. Claire, K. Faulk, S. Govindarajan, S. U. Emerson, R. H. Purcell, and J. Bukh. 2003. The p7 polypeptide of hepatitis C virus is critical for infectivity and contains functionally important genotype-specific sequences. Proc. Natl. Acad. Sci. USA 100:11646-11651.
33. Schnell, J. R., and J. J. Chou. 2008. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451:591-595.
34. Steinmann, E., F. Penin, S. Kallis, A. H. Patel, R. Bartenschlager, and T. Pietschmann. 2007. Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog. 3:e103.
35. Steinmann, E., T. Whitfield, S. Kallis, R. A. Dwek, N. Zitzmann, T. Pietschmann, and R. Bartenschlager. 2007. Antiviral effects of amantadine and iminosugar derivatives against hepatitis C virus. Hepatology 46:330-338.
36. StGelais, C., T. J. Tuthill, D. S. Clarke, D. J. Rowlands, M. Harris, and S. Griffin. 2007. Inhibition of hepatitis C virus p7 membrane channels in a liposome-based assay system. Antiviral Res. 76:48-58.
37. Stouffer, A. L., R. Acharya, D. Salom, A. S. Levine, L. Di Costanzo, C. S. Soto, V. Tereshko, V. Nanda, S. Stayrook, and W. F. DeGrado. 2008. Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451:596-599.
38. Takikawa, S., R. E. Engle, S. U. Emerson, R. H. Purcell, M. St Claire, and J. Bukh. 2006. Functional analyses of GB virus B p13 protein: development of a recombinant GB virus B hepatitis virus with a p7 protein. Proc. Natl. Acad. Sci. USA 103:3345-3350.
39. Tang, Y., F. Zaitseva, R. A. Lamb, and L. H. Pinto. 2002. The gate of the influenza virus M2 proton channel is formed by a single tryptophan residue. J. Biol. Chem. 277:39880-39886.
40. Wakita, T., T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H. G. Krausslich, M. Mizokami, R. Bartenschlager, and T. J. Liang. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
41. Wang, C., R. A. Lamb, and L. H. Pinto. 1995. Activation of the M2 ion channel of influenza virus: a role for the transmembrane domain histidine residue. Biophys. J. 69:1363-1371.
42. Xie, J., J. Zhao, P. B. Davis, and J. Ma. 2000. Conformation, independent of charge, in the R domain affects cystic fibrosis transmembrane conductance regulator channel openings. Biophys. J. 78:1293-1305.
43. Yanagi, M., M. St. Claire, M. Shapiro, S. U. Emerson, R. H. Purcell, and J. Bukh. 1998. Transcripts of a chimeric cDNA clone of hepatitis C virus genotype 1b are infectious in vivo. Virology 244:161-172.
44. Zhong, H., J. Lai, and K. W. Yau. 2003. Selective heteromeric assembly of cyclic nucleotide-gated channels. Proc. Natl. Acad. Sci. USA 100:5509-5513.
45. Zhong, J., P. Gastaminza, G. Cheng, S. Kapadia, T. Kato, D. R. Burton, S. F. Wieland, S. L. Uprichard, T. Wakita, and F. V. Chisari. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. USA 102:9294-9299.