The elusive function of the hepatitis C virus p7 protein

Virology

Volumn 462-463, Issue 1, 2014, Pages 377-387

  Atoom, Ali M ^a   Taylor, Nathan G A ^a   Russell, Rodney S ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Assembly; HCV; Hepatitis C virus; P7; Viroporin

Indexed keywords

ALPHA INTERFERON; AMANTADINE; FAT DROPLET; GLYCOPROTEIN E1; IMINOSUGAR; ION CHANNEL; N [5 (1 METHYL 1H PYRAZOL 4 YL) 2 NAPHTHOYL]GUANIDINE; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5A; P7 PROTEIN; RIBAVIRIN; RIMANTADINE; SIGNAL PEPTIDASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

CHANNEL GATING; ENDOPLASMIC RETICULUM; HEPATITIS C; HEPATITIS C VIRUS; HEPATITIS C VIRUS SUBTYPE 1A; HEPATITIS C VIRUS SUBTYPE 2A; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS ENTRY; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS REPLICATION;

HEPATITIS C VIRUS;

ASSEMBLY; HCV; HEPATITIS C VIRUS; P7; VIROPORIN;

HEPACIVIRUS; HUMANS; VIRAL PROTEINS; VIRUS ASSEMBLY;

EID: 84905961801     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.04.018     Document Type: Review

References (112)

1. Andre P., Komurian-Pradel F., Deforges S., Perret M., Berland J.L., et al. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 2002, 76:6919-6928.
2. Appel N., Zayas M., Miller S., Krijnse-Locker J., Schaller T., et al. Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog. 2008, 4:e1000035.
3. Atkins E., Tatineni R., Li H., Gretch D., Harris M., et al. The stability of secreted, acid-labile H77/JFH-1 hepatitis C virus (HCV) particles is altered by patient isolate genotype 1a p7 sequences. Virology 2014, 448:117-124.
4. Atoom A.M., Jones D.M., Russell R.S. Evidence suggesting that HCV p7 protects E2 glycoprotein from premature degradation during virus production. Virus Res. 2013, 176:199-210.
5. Aweya J.J., Mak T.M., Lim S.G., Tan Y.J. The p7 protein of the hepatitis C virus induces cell death differently from the influenza A virus viroporin M2. Virus Res. 2013, 172:24-34.
6. Bartenschlager R., Penin F., Lohmann V., Andre P. Assembly of infectious hepatitis C virus particles. Trends Microbiol. 2011, 19:95-103.
7. Bartosch B., Dubuisson J., Cosset F.L. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J. Exp. Med. 2003, 197:633-642.
8. Bentham M.J., Foster T.L., McCormick C., Griffin S. Mutations in hepatitis C virus p7 reduce both the egress and infectivity of assembled particles via impaired proton channel function. J. Gen. Virol. 2013, 94:2236-2248.
9. Bergeron J.J., Brenner M.B., Thomas D.Y., Williams D.B. Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem. Sci. 1994, 19:124-128.
10. Blight K.J., McKeating J.A., Rice C.M. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 2002, 76:13001-13014.
11. Boson B., Granio O., Bartenschlager R., Cosset F.L. A concerted action of hepatitis C virus p7 and nonstructural protein 2 regulates core localization at the endoplasmic reticulum and virus assembly. PLoS Pathog. 2011, 7:e1002144.
12. Boulant S., Montserret R., Hope R.G., Ratinier M., Targett-Adams P., et al. Structural determinants that target the hepatitis C virus core protein to lipid droplets. J. Biol. Chem. 2006, 281:22236-22247.
13. Branza-Nichita N., Durantel D., Carrouee-Durantel S., Dwek R.A., Zitzmann N. Antiviral effect of N-butyldeoxynojirimycin against bovine viral diarrhea virus correlates with misfolding of E2 envelope proteins and impairment of their association into E1-E2 heterodimers. J. Virol. 2001, 75:3527-3536.
14. Brohm C., Steinmann E., Friesland M., Lorenz I.C., Patel A., et al. Characterization of determinants important for hepatitis C virus p7 function in morphogenesis by using trans-complementation. J. Virol. 2009, 83:11682-11693.
15. Carrere-Kremer S., Montpellier-Pala C., Cocquerel L., Wychowski C., Penin F., et al. Subcellular localization and topology of the p7 polypeptide of hepatitis C virus. J. Virol. 2002, 76:3720-3730.
16. Carrere-Kremer S., Montpellier C., Lorenzo L., Brulin B., Cocquerel L., et al. Regulation of hepatitis C virus polyprotein processing by signal peptidase involves structural determinants at the p7 sequence junctions. J. Biol. Chem. 2004, 279:41384-41392.
17. Castelain S., Bonte D., Penin F., Francois C., Capron D., et al. Hepatitis C Virus p7 membrane protein quasispecies variability in chronically infected patients treated with interferon and ribavirin, with or without amantadine. J. Med. Virol. 2007, 79:144-154.
18. Chandler D.E., Penin F., Schulten K., Chipot C. The p7 protein of hepatitis C virus forms structurally plastic, minimalist ion channels. PLoS Comput. Biol. 2012, 8:e1002702.
19. Chew C.F., Vijayan R., Chang J., Zitzmann N., Biggin P.C. Determination of pore-lining residues in the hepatitis C virus p7 protein. Biophys. J. 2009, 96:L10-12.
20. Clarke D., Griffin S., Beales L., Gelais C.S., Burgess S., et al. Evidence for the formation of a heptameric ion channel complex by the hepatitis C virus p7 protein in vitro. J. Biol. Chem. 2006, 281:37057-37068.
21. Cook G.A., Dawson L.A., Tian Y., Opella S.J. Three-dimensional structure and interaction studies of hepatitis C virus p7 in 1,2-dihexanoyl-sn-glycero-3-phosphocholine by solution nuclear magnetic resonance. Biochemistry 2013.
22. Dimitrova M., Imbert I., Kieny M.P., Schuster C. Protein-protein interactions between hepatitis C virus nonstructural proteins. J. Virol. 2003, 77:5401-5414.
23. Dubuisson J., Hsu H.H., Cheung R.C., Greenberg H.B., Russell D.G., et al. Formation and intracellular localization of hepatitis C virus envelope glycoprotein complexes expressed by recombinant vaccinia and Sindbis viruses. J. Virol. 1994, 68:6147-6160.
24. Durantel D., Branza-Nichita N., Carrouee-Durantel S., Butters T.D., Dwek R.A., et al. Study of the mechanism of antiviral action of iminosugar derivatives against bovine viral diarrhea virus. J. Virol. 2001, 75:8987-8998.
25. Elbers K., Tautz N., Becher P., Stoll D., Rumenapf T., et al. Processing in the pestivirus E2-NS2 region: identification of proteins p7 and E2p7. J. Virol. 1996, 70:4131-4135.
26. Feld J.J., Hoofnagle J.H. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005, 436:967-972.
27. Fischer P.B., Collin M., Karlsson G.B., James W., Butters T.D., et al. The alpha-glucosidase inhibitor N-butyldeoxynojirimycin inhibits human immunodeficiency virus entry at the level of post-CD4 binding. J. Virol. 1995, 69:5791-5797.
28. Flint M., Logvinoff C., Rice C.M., McKeating J.A. Characterization of infectious retroviral pseudotype particles bearing hepatitis C virus glycoproteins. J. Virol. 2004, 78:6875-6882.
29. Foster T.L., Verow M., Wozniak A.L., Bentham M.J., Thompson J., et al. Resistance mutations define specific antiviral effects for inhibitors of the hepatitis C virus p7 ion channel. Hepatology 2011, 54:79-90.
30. Foster T.L., Thompson G.S., Kalverda A.P., Kankanala J., Bentham M., et al. Structure-guided design affirms inhibitors of hepatitis C virus p7 as a viable class of antivirals targeting virion release. Hepatology 2014, 59:408-422.
31. Gastaminza P., Kapadia S.B., Chisari F.V. Differential biophysical properties of infectious intracellular and secreted hepatitis C virus particles. J. Virol. 2006, 80:11074-11081.
32. Gentzsch J., Brohm C., Steinmann E., Friesland M., Menzel N., et al. hepatitis c Virus p7 is critical for capsid assembly and envelopment. PLoS Pathog. 2013, 9:e1003355.
33. Gonzalez M.E., Carrasco L. Viroporins. FEBS Lett. 2003, 552:28-34.
34. Gottwein J.M., Scheel T.K., Jensen T.B., Lademann J.B., Prentoe J.C., et al. Development and characterization of hepatitis C virus genotype 1-7 cell culture systems: role of CD81 and scavenger receptor class B type I and effect of antiviral drugs. Hepatology 2009, 49:364-377.
35. Griffin S., Clarke D., McCormick C., Rowlands D., Harris M. Signal peptide cleavage and internal targeting signals direct the hepatitis C virus p7 protein to distinct intracellular membranes. J. Virol. 2005, 79:15525-15536.
36. Griffin S., Stgelais C., Owsianka A.M., Patel A.H., Rowlands D., et al. Genotype-dependent sensitivity of hepatitis C virus to inhibitors of the p7 ion channel. Hepatology 2008, 48:1779-1790.
37. Griffin S.D., Beales L.P., Clarke D.S., Worsfold O., Evans S.D., et al. The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett. 2003, 535:34-38.
38. Griffin S.D., Harvey R., Clarke D.S., Barclay W.S., Harris M., et al. 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. 2004, 85:451-461.
39. Han Q., Manna D., Belton K., Cole R., Konan K.V. Modulation of hepatitis C virus genome encapsidation by nonstructural protein 4B. J. Virol. 2013, 87:7409-7422.
40. Haqshenas G., Mackenzie J.M., Dong X., Gowans E.J. Hepatitis C virus p7 protein is localized in the endoplasmic reticulum when it is encoded by a replication-competent genome. J. Gen. Virol. 2007, 88:134-142.
41. Harada T., Tautz N., Thiel H.J. E2-p7 region of the bovine viral diarrhea virus polyprotein: processing and functional studies. J. Virol. 2000, 74:9498-9506.
42. Hijikata M., Mizushima H., Akagi T., Mori S., Kakiuchi N., et al. Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J. Virol. 1993, 67:4665-4675.
43. Hoffman B., Liu Q. Hepatitis C viral protein translation: mechanisms and implications in developing antivirals. Liver Int. 2011, 31:1449-1467.
44. Hsu M., Zhang J., Flint M., Logvinoff C., Cheng-Mayer C., et al. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7271-7276.
45. Hughes M., Gretton S., Shelton H., Brown D.D., McCormick C.J., et al. A conserved proline between domains II and III of hepatitis C virus NS5A influences both RNA replication and virus assembly. J. Virol. 2009, 83:10788-10796.
46. Hughes M., Griffin S., Harris M. Domain III of NS5A contributes to both RNA replication and assembly of hepatitis C virus particles. J. Gen. Virol. 2009, 90:1329-1334.
47. Jirasko V., Montserret R., Appel N., Janvier A., Eustachi L., et al. Structural and functional characterization of nonstructural protein 2 for its role in hepatitis C virus assembly. J. Biol. Chem. 2008, 283:28546-28562.
48. Jirasko V., Montserret R., Lee J.Y., Gouttenoire J., Moradpour D., et al. Structural and functional studies of nonstructural protein 2 of the hepatitis C virus reveal its key role as organizer of virion assembly. PLoS Pathog. 2010, 6:e1001233.
49. Jones C.T., Murray C.L., Eastman D.K., Tassello J., Rice C.M. Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus. J. Virol. 2007, 81:8374-8383.
50. Jones D.M., Patel A.H., Targett-Adams P., McLauchlan J. The hepatitis C virus NS4B protein can trans-complement viral RNA replication and modulates production of infectious virus. J. Virol. 2009, 83:2163-2177.
51. Jones D.M., Atoom A.M., Zhang X., Kottilil S., Russell R.S. A genetic interaction between the core and NS3 proteins of hepatitis C virus is essential for production of infectious virus. J. Virol. 2011, 85:12351-12361.
52. Kelly M.L., Cook J.A., Brown-Augsburger P., Heinz B.A., Smith M.C., et al. Demonstrating the intrinsic ion channel activity of virally encoded proteins. FEBS Lett. 2003, 552:61-67.
53. Khoury G., Ewart G., Luscombe C., Miller M., Wilkinson J. Antiviral efficacy of the novel compound BIT225 against HIV-1 release from human macrophages. Antimicrob. Agents Chemother. 2010, 54:835-845.
54. Kohlway A., Pirakitikulr N., Barrera F.N., Potapova O., Engelman D.M., et al. Hepatitis C virus RNA replication and virus particle assembly require specific dimerization of the NS4A protein transmembrane domain. J. Virol. 2013, 88:628-642.
55. Kolykhalov A.A., Mihalik K., Feinstone S.M., Rice C.M. Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3' nontranslated region are essential for virus replication in vivo. J. Virol. 2000, 74:2046-2051.
56. Kuiken C., Simmonds P. Nomenclature and numbering of the hepatitis C virus. Methods Mol. Biol. 2009, 510:33-53.
57. Lake-Bakaar G., Ruffini L., Kuzmic P. Effect of ribavirin and amantadine on early hepatitis C virus RNA rebound and clearance in serum during daily high-dose interferon. Dig. Dis. Sci. 2003, 48:126-139.
58. Lee A., Liu S., Wang T. Identification of novel human kinases that suppress hepatitis C virus infection. J. Viral Hepat. 2013, Nov 10.
59. Levrero M. Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene 2006, 25:3834-3847.
60. Liang X., Li Z.Y. Ion channels as antivirus targets. Virol. Sin. 2010, 25:267-280.
61. Lin C., Lindenbach B.D., Pragai B.M., McCourt D.W., Rice C.M. Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini. J. Virol. 1994, 68:5063-5073.
62. Lindenbach B.D., Evans M.J., Syder A.J., Wolk B., Tellinghuisen T.L., et al. Complete replication of hepatitis C virus in cell culture. Science 2005, 309:623-626.
63. Lohmann V., Korner F., Koch J., Herian U., Theilmann L., et al. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 1999, 285:110-113.
64. Lorenz I.C., Marcotrigiano J., Dentzer T.G., Rice C.M. Structure of the catalytic domain of the hepatitis C virus NS2-3 protease. Nature 2006, 442:831-835.
65. Luik P., Chew C., Aittoniemi J., Chang J., Wentworth P., et al. The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:12712-12716.
66. Luscombe C.A., Huang Z., Murray M.G., Miller M., Wilkinson J., et al. A novel Hepatitis C virus p7 ion channel inhibitor, BIT225, inhibits bovine viral diarrhea virus in vitro and shows synergism with recombinant interferon-alpha-2b and nucleoside analogues. Antivir. Res. 2010, 86:144-153.
67. Ma Y., Yates J., Liang Y., Lemon S.M., Yi M. NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly. J. Virol. 2008, 82:7624-7639.
68. Ma Y., Anantpadma M., Timpe J.M., Shanmugam S., Singh S.M., et al. Hepatitis C virus NS2 protein serves as a scaffold for virus assembly by interacting with both structural and nonstructural proteins. J. Virol. 2011, 85:86-97.
69. Masaki T., Suzuki R., Murakami K., Aizaki H., Ishii K., et al. Interaction of hepatitis C virus nonstructural protein 5A with core protein is critical for the production of infectious virus particles. J. Virol. 2008, 82:7964-7976.
70. McLauchlan J., Lemberg M.K., Hope G., Martoglio B. Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J. 2002, 21:3980-3988.
71. Meshkat Z., Audsley M., Beyer C., Gowans E.J., Haqshenas G. Reverse genetic analysis of a putative, influenza virus M2 HXXXW-like motif in the p7 protein of hepatitis C virus. J. Viral Hepat. 2009, 16:187-194.
72. Mihm U., Grigorian N., Welsch C., Herrmann E., Kronenberger B., et al. Amino acid variations in hepatitis C virus p7 and sensitivity to antiviral combination therapy with amantadine in chronic hepatitis C. Antivir. Ther. 2006, 11:507-519.
73. Miyanari Y., Atsuzawa K., Usuda N., Watashi K., Hishiki T., et al. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell Biol. 2007, 9:1089-1097.
74. Mizushima H., Hijikata M., Asabe S., Hirota M., Kimura K., et al. Two hepatitis C virus glycoprotein E2 products with different C termini. J. Virol. 1994, 68:6215-6222.
75. Montserret R., Saint N., Vanbelle C., Salvay A.G., Simorre J.P., et al. NMR structure and ion channel activity of the p7 protein from hepatitis C virus. J. Biol. Chem. 2010, 285:31446-31461.
76. Moradpour D., Penin F., Rice C.M. Replication of hepatitis C virus. Nat. Rev. Microbiol. 2007, 5:453-463.
77. Murray C.L., Jones C.T., Tassello J., Rice C.M. Alanine scanning of the hepatitis C virus core protein reveals numerous residues essential for production of infectious virus. J. Virol. 2007, 81:10220-10231.
78. Murray C.L., Jones C.T., Rice C.M. Architects of assembly: roles of Flaviviridae non-structural proteins in virion morphogenesis. Nat. Rev. Microbiol. 2008, 6:699-708.
79. Nieva J.L., Madan V., Carrasco L. Viroporins: structure and biological functions. Nat. Rev. Microbiol. 2012, 10:563-574.
80. OuYang B., Xie S., Berardi M.J., Zhao X., Dev J., et al. Unusual architecture of the p7 channel from hepatitis C virus. Nature 2013, 498:521-525.
81. Patargias G., Zitzmann N., Dwek R., Fischer W.B. Protein-protein interactions: modeling the hepatitis C virus ion channel p7. J. Med. Chem. 2006, 49:648-655.
82. Pavlovic D., Neville D.C., Argaud O., Blumberg B., Dwek R.A., et al. 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. 2003, 100:6104-6108.
83. Phan T., Beran R.K., Peters C., Lorenz I.C., Lindenbach B.D. Hepatitis C virus NS2 protein contributes to virus particle assembly via opposing epistatic interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J. Virol. 2009, 83:8379-8395.
84. Pietschmann T., Kaul A., Koutsoudakis G., Shavinskaya A., Kallis S., et al. Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:7408-7413.
85. Popescu C.I., Callens N., Trinel D., Roingeard P., Moradpour D., et al. NS2 protein of hepatitis C virus interacts with structural and non-structural proteins towards virus assembly. PLoS Pathog. 2011, 7:e1001278.
86. Premkumar A., Wilson L., Ewart G.D., Gage P.W. Cation-selective ion channels formed by p7 of hepatitis C virus are blocked by hexamethylene amiloride. FEBS Lett. 2004, 557:99-103.
87. Premkumar A., Dong X., Haqshenas G., Gage P.W., Gowans E.J. Amantadine inhibits the function of an ion channel encoded by GB virus B, but fails to inhibit virus replication. Antivir. Ther. 2006, 11:289-295.
88. Reed K.E., Rice C.M. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 2000, 242:55-84.
89. Ruch T.R., Machamer C.E. The coronavirus E protein: assembly and beyond. Viruses 2012, 4:363-382.
90. Russell R.S., Meunier J.C., Takikawa S., Faulk K., Engle R.E., et al. Advantages of a single-cycle production assay to study cell culture-adaptive mutations of hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4370-4375.
91. Sakai A., Claire M.S., Faulk K., Govindarajan S., Emerson S.U., et al. 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. 2003, 100:11646-11651.
92. Schnell J.R., Chou J.J. Structure and mechanism of the M2 proton channel of influenza A virus. Nature 2008, 451:591-595.
93. Shanmugam S., Yi M. Efficiency of E2-p7 processing modulates production of infectious hepatitis C virus. J. Virol. 2013, 87:11255-11266.
94. StGelais C., Tuthill T.J., Clarke D.S., Rowlands D.J., Harris M., et al. Inhibition of hepatitis C virus p7 membrane channels in a liposome-based assay system. Antivir. Res. 2007, 76:48-58.
95. StGelais C., Foster T.L., Verow M., Atkins E., Fishwick C.W., et al. Determinants of hepatitis C virus p7 ion channel function and drug sensitivity identified in vitro. J. Virol. 2009, 83:7970-7981.
96. Stapleford K.A., Lindenbach B.D. Hepatitis C virus NS2 coordinates virus particle assembly through physical interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes. J. Virol. 2011, 85:1706-1717.
97. Steinmann E., Penin F., Kallis S., Patel A.H., Bartenschlager R., et al. Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog. 2007, 3:e103.
98. Steinmann E., Whitfield T., Kallis S., Dwek R.A., Zitzmann N., et al. Antiviral effects of amantadine and iminosugar derivatives against hepatitis C virus. Hepatology 2007, 46:330-338.
99. Stocks C.E., Lobigs M. Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires determinants in C, the signal peptide, and prM. J. Virol. 1998, 72:2141-2149.
100. Tedbury P., Welbourn S., Pause A., King B., Griffin S., et al. The subcellular localization of the hepatitis C virus non-structural protein NS2 is regulated by an ion channel-independent function of the p7 protein. J. Gen. Virol. 2011, 92:819-830.
101. Thomas D.L. Global control of hepatitis C: where challenge meets opportunity. Nat. Med. 2013, 19:850-858.
102. Tscherne D.M., Jones C.T., Evans M.J., Lindenbach B.D., McKeating J.A., et al. Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J. Virol. 2006, 80:1734-1741.
103. Vieyres G., Brohm C., Friesland M., Gentzsch J., Wolk B., et al. Subcellular localization and function of an epitope-tagged p7 viroporin in hepatitis C virus-producing cells. J. Virol. 2013, 87:1664-1678.
104. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005, 11:791-796.
105. Wang K., Xie S., Sun B. Viral proteins function as ion channels. Biochim. Biophys. Acta 2011, 1808:510-515.
106. Wang Y.T., Hsu H.J., Fischer W.B. Computational modeling of the p7 monomer from HCV and its interaction with small molecule drugs. Springerplus 2013, 2:324.
107. Wozniak A.L., Griffin S., Rowlands D., Harris M., Yi M., et al. Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production. PLoS Pathog. 2010, 6:e1001087.
108. Yi M., Villanueva R.A., Thomas D.L., Wakita T., Lemon S.M. Production of infectious genotype 1a hepatitis C virus (Hutchinson strain) in cultured human hepatoma cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2310-2315.
109. Yi M., Ma Y., Yates J., Lemon S.M. Compensatory mutations in E1, p7, NS2, and NS3 enhance yields of cell culture-infectious intergenotypic chimeric hepatitis C virus. J. Virol. 2007, 81:629-638.
110. Yi M., Ma Y., Yates J., Lemon S.M. Trans-complementation of an NS2 defect in a late step in hepatitis C virus (HCV) particle assembly and maturation. PLoS Pathog. 2009, 5:e1000403.
111. Zeisel M.B., Felmlee DJ, Baumert T.F. Hepatitis C virus entry. Curr. Top. Microbiol. Immunol. 2013, 369:87-112.
112. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., et al. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9294-9299.