Last stop before exit - Hepatitis C assembly and release as antiviral drug targets

Viruses

Volumn 2, Issue 8, 2010, Pages 1782-1803

  Tews, Birke Andrea ^a   Popescu, Costin Ioan ^a,b   Dubuisson, Jean ^a  

^a UNIV LILLE   (France)

^b INSTITUTE OF BIOCHEMISTRY OF THE ROMANIAN ACADEMY   (Romania)

Author keywords

Antivirals; Assembly; Hepatitis C; Release

Indexed keywords

ANTIVIRUS AGENT; APOLIPOPROTEIN B; APOLIPOPROTEIN E; BIT 225; BMS 790052; CASTANOSPERMINE 6 BUTYRATE; FLAVONOID; GLYCOPROTEIN E1; GLYCOPROTEIN E2; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; N [5 (1 METHYL 1H PYRAZOL 4 YL)NAPHTHALENE 2 CARBONYL]GUANIDINE; N NONYL DEOXYGALACTONOJIRIMYCIN; NARIGENIN; NONSTRUCTURAL PROTEIN 2; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5B; PROTEIN P7; PTEROSTILBENE; TOREMIFENE; UNCLASSIFIED DRUG; UT 231B; VERY LOW DENSITY LIPOPROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ANTIVIRAL ACTIVITY; CARBOXY TERMINAL SEQUENCE; DRUG APPROVAL; DRUG SCREENING; DRUG TARGETING; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; INNATE IMMUNITY; LIFE CYCLE; MOLECULAR CLONING; NONHUMAN; REVIEW; RNA SYNTHESIS; VIRION; VIRUS ASSEMBLY; VIRUS CORE; VIRUS GENOME; VIRUS ISOLATION; VIRUS MORPHOGENESIS; VIRUS PARTICLE; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 79952169634     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v2081782     Document Type: Review

References (124)

1. Shepard, C.W.; Finelli, L.; Alter, M.J. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 2005, 5, 558-567.
2. Lemon, S.M.; Walker, C.; Alter, M.J.; Yi, M. Hepatitis C Virus; 5 ed.; Lippincott Williams & Wilkins: Philadelphia, PA, U. S. A., 2007; pp. 1253-1304.
3. Varaklioti, A.; Vassilaki, N.; Georgopoulou, U.; Mavromara, P. Alternate translation occurs within the core coding region of the hepatitis C viral genome. J. Biol. Chem. 2002, 277, 17713-17721.
4. Gottwein, J.M.; Scheel, T.K.; Jensen, T.B.; Lademann, J.B.; Prentoe, J.C.; Knudsen, M.L.; Hoegh, A.M.; Bukh, J. 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.
5. Burlone, M.E.; Budkowska, A. Hepatitis C virus cell entry: role of lipoproteins and cellular receptors. J. Gen. Virol. 2009, 90, 1055-1070.
6. Blanchard, E.; Belouzard, S.; Goueslain, L.; Wakita, T.; Dubuisson, J.; Wychowski, C.; Rouillé, Y. Hepatitis C virus entry depends on clathrin-mediated endocytosis. J. Virol. 2006, 80, 6964-6972.
7. Meertens, L.; Bertaux, C.; Dragic, T. Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles. J. Virol. 2006, 80, 11571-11578.
8. Moradpour, D.; Gosert, R.; Egger, D.; Penin, F.; Blum, H.E.; Bienz, K. Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex. Antiviral. Res. 2003, 60, 103-109.
9. Gosert, R.; Egger, D.; Lohmann, V.; Bartenschlager, R.; Blum, H.E.; Bienz, K.; Moradpour, D. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J. Virol. 2003, 77, 5487-5492.
10. Egger, D.; Wolk, B.; Gosert, R.; Bianchi, L.; Blum, H.E.; Moradpour, D.; Bienz, K. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 2002, 76, 5974-5984.
11. Blight, K.J.; Kolykhalov, A.A.; Rice, C.M. Efficient initiation of HCV RNA replication in cell culture. Science 2000, 290, 1972-1974.
12. Lohmann, V.; Korner, F.; Koch, J.; Herian, U.; Theilmann, L.; Bartenschlager, R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 1999, 285, 110-113.
13. Murray, C.L.; Jones, C.T.; Rice, C.M. Architects of assembly: roles of Flaviviridae non-structural proteins in virion morphogenesis. Nat. Rev. Micro. 2008, 6, 699-708.
14. Barba, G.; Harper, F.; Harada, T.; Kohara, M.; Goulinet, S.; Matsuura, Y.; Eder, G.; Schaff, Z.; Chapman, M.J.; Miyamura, T.; Brechot, C. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc. Natl. Acad. Sci. U. S. A. 1997, 94, 1200-1205.
15. Moradpour, D.; Englert, C.; Wakita, T.; Wands, J.R. Characterization of cell lines allowing tightly regulated expression of hepatitis C virus core protein. Virology 1996, 222, 51-63.
16. Martin, S.; Parton, R.G. Lipid droplets: a unified view of a dynamic organelle. Nat. Rev. Mol. Cell. Biol. 2006, 7, 373-378.
17. Miyanari, Y.; Atsuzawa, K.; Usuda, N.; Watashi, K.; Hishiki, T.; Zayas, M.; Bartenschlager, R.; Wakita, T.; Hijikata, M.; Shimotohno, K. The lipid droplet is an important organelle for hepatitis C virus production. Nat. Cell. Biol. 2007, 9, 1089-1097.
18. Santolini, E.; Migliaccio, G.; La Monica, N. Biosynthesis and biochemical properties of the hepatitis C virus core protein. J. Virol. 1994, 68, 3631-3641.
19. Hussy, P.; Langen, H.; Mous, J.; Jacobsen, H. Hepatitis C virus core protein: carboxy-terminal boundaries of two processed species suggest cleavage by a signal peptide peptidase. Virology 1996, 224, 93-104.
20. 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.
21. Boulant, S.; Vanbelle, C.; Ebel, C.; Penin, F.; Lavergne, J.P. Hepatitis C virus core protein is a dimeric alpha-helical protein exhibiting membrane protein features. J. Virol. 2005, 79, 11353-11365.
22. Hope, R.G.; Murphy, D.J.; McLauchlan, J. The domains required to direct core proteins of hepatitis C virus and GB virus-B to lipid droplets share common features with plant oleosin proteins. J. Biol. Chem. 2002, 277, 4261-4270.
23. McLauchlan, J. Properties of the hepatitis C virus core protein: a structural protein that modulates cellular processes. J. Viral. Hepat. 2000, 7, 2-14.
24. Cristofari, G.; Ivanyi-Nagy, R.; Gabus, C.; Boulant, S.; Lavergne, J.P.; Penin, F.; Darlix, J.L. The hepatitis C virus Core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro. Nucleic Acids Res. 2004, 32, 2623-2631.
25. Shimoike, T.; Mimori, S.; Tani, H.; Matsuura, Y.; Miyamura, T. Interaction of hepatitis C virus core protein with viral sense RNA and suppression of its translation. J. Virol. 1999, 73, 9718-9725.
26. Nolandt, O.; Kern, V.; Muller, H.; Pfaff, E.; Theilmann, L.; Welker, R.; Krausslich, H.G. Analysis of hepatitis C virus core protein interaction domains. J. Gen. Virol. 1997, 78 (Pt 6), 1331-1340.
27. Boulant, S.; Montserret, R.; Hope, R.G.; Ratinier, M.; Targett-Adams, P.; Lavergne, J.P.; Penin, F.; McLauchlan, J. Structural determinants that target the hepatitis C virus core protein to lipid droplets. J. Biol. Chem. 2006, 281, 22236-22247.
28. Boulant, S.; Targett-Adams, P.; McLauchlan, J. Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J. Gen. Virol. 2007, 88, 2204-2213.
29. Shavinskaya, A.; Boulant, S.; Penin, F.; McLauchlan, J.; Bartenschlager, R. The lipid droplet binding domain of hepatitis C virus core protein is a major determinant for efficient virus assembly. J. Biol. Chem. 2007, 282, 37158-37169.
30. Boulant, S.; Douglas, M.W.; Moody, L.; Budkowska, A.; Targett-Adams, P.; McLauchlan, J. Hepatitis C virus core protein induces lipid droplet redistribution in a microtubule- and dyneindependent manner. Traffic 2008, 9, 1268-1282.
31. Masaki, T.; Suzuki, R.; Murakami, K.; Aizaki, H.; Ishii, K.; Murayama, A.; Date, T.; Matsuura, Y.; Miyamura, T.; Wakita, T.; Suzuki, T. 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.
32. Appel, N.; Zayas, M.; Miller, S.; Krijnse-Locker, J.; Schaller, T.; Friebe, P.; Kallis, S.; Engel, U.; Bartenschlager, R. Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly. PLoS Pathog. 2008, 4, e1000035.
33. Tellinghuisen, T.L.; Foss, K.L.; Treadaway, J. Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog. 2008, 4, e1000032.
34. Hanoulle, X.; Badillo, A.; Verdegem, D.; Penin, F.; Lippens, G. The Domain 2 of the HCV NS5A Protein is Intrinsically Unstructured. Protein Pept. Lett. 2010, 17, 1012-1018.
35. Brass, V.; Bieck, E.; Montserret, R.; Wölk, B.; Hellings, J.A.; Blum, H.E.; Penin, F.; Moradpour, D. An amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 2002, 277, 8130-8139.
36. Penin, F.; Brass, V.; Appel, N.; Ramboarina, S.; Montserret, R.; Ficheux, D.; Blum, H.E.; Bartenschlager, R.; Moradpour, D. Structure and function of the membrane anchor domain of hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 2004, 279, 40835-40843.
37. Hanoulle, X.; Verdegem, D.; Badillo, A.; Wieruszeski, J.-M.; Penin, F.; Lippens, G. Domain 3 of non-structural protein 5A from hepatitis C virus is natively unfolded. Biochem. Biophys. Res. Commun. 2009, 381, 634-638.
38. Tellinghuisen, T.L.; Marcotrigiano, J.; Rice, C.M. Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase. Nature 2005, 435, 374-379.
39. Pietschmann, T.; Zayas, M.; Meuleman, P.; Long, G.; Appel, N.; Koutsoudakis, G.; Kallis, S.; Leroux-Roels, G.; Lohmann, V.; Bartenschlager, R. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog. 2009, 5, e1000475.
40. Bukh, J.; Pietschmann, T.; Lohmann, V.; Krieger, N.; Faulk, K.; Engle, R.E.; Govindarajan, S.; Shapiro, M.; St Claire, M.; Bartenschlager, R. Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 14416-14421.
41. 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.
42. Evans, M.J.; Rice, C.M.; Goff, S.P. Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 13038-13043.
43. Lemon, S.M.; McKeating, J.A.; Pietschmann, T.; Frick, D.N.; Glenn, J.S.; Tellinghuisen, T.L.; Symons, J.; Furman, P.A. Development of novel therapies for hepatitis C. Antiviral Res. 2010, 86, 79-92.
44. Masaki, T.; Suzuki, R.; Murakami, K.; Aizaki, H.; Ishii, K.; Murayama, A.; Date, T.; Matsuura, Y.; Miyamura, T.; Wakita, T.; Suzuki, T. 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.
45. Tellinghuisen, T.L.; Foss, K.L.; Treadaway, J. Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog. 2008, 4, e1000032.
46. 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.
47. 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.
48. Phan, T.; Beran, R.; Peters, C.; Lorenz, I.; Lindenbach, B. Hepatitis C virus NS2 protein contributes to virus particle assembly via opposing epistatic interactions with the E1-E2 glycoprotein and NS3-4A enzyme complexes. J. Virol. 2009, 83, 8379-95.
49. Jirasko, V.; Montserret, R.; Appel, N.; Janvier, A.; Eustachi, L.; Brohm, C.; Steinmann, E.; Pietschmann, T.; Penin, F.; Bartenschlager, R. Structural and functional characterization of nonstructural protein 2 for its role in hepatitis C virus assembly. J. Biol. Chem. 2008, 283, 28546-28562.
50. Dentzer, T.G.; Lorenz, I.C.; Evans, M.J.; Rice, C.M. Determinants of the hepatitis C virus nonstructural protein 2 protease domain required for production of infectious virus. J. Virol. 2009, 83, 12702-12713.
51. 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.
52. Brohm, C.; Steinmann, E.; Friesland, M.; Lorenz, I.C.; Patel, A.; Penin, F.; Bartenschlager, R.; Pietschmann, T. Characterization of determinants important for hepatitis C virus p7 function in morphogenesis by using trans-complementation. J. Virol. 2009, 83, 11682-11693.
53. 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.
54. Carrere-Kremer, S.; Montpellier-Pala, C.; Cocquerel, L.; Wychowski, C.; Penin, F.; Dubuisson, J. Subcellular localization and topology of the p7 polypeptide of hepatitis C virus. J. Virol. 2002, 76, 3720-3730.
55. Luik, P.; Chew, C.; Aittoniemi, J.; Chang, J.; Wentworth, P.; Dwek, R.; Biggin, P.; Vénien-Bryan, C.; Zitzmann, N. The 3-dimensional structure of a hepatitis C virus p7 ion channel by electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 12712-6.
56. Griffin, S.D.; Beales, L.P.; Clarke, D.S.; Worsfold, O.; Evans, S.D.; Jaeger, J.; Harris, M.P.; Rowlands, D.J. 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.
57. Pavlovic, D.; Neville, D.C.; Argaud, O.; Blumberg, B.; Dwek, R.A.; Fischer, W.B.; Zitzmann, N. 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.
58. 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.
59. Griffin, S.D.; Harvey, R.; Clarke, D.S.; Barclay, W.S.; Harris, M.; Rowlands, D.J. 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.
60. Clarke, D.; Griffin, S.; Beales, L.; Gelais, C.S.; Burgess, S.; Harris, M.; Rowlands, D. 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.
61. Steinmann, E.; Penin, F.; Kallis, S.; Patel, A.H.; Bartenschlager, R.; Pietschmann, T. Hepatitis C virus p7 protein is crucial for assembly and release of infectious virions. PLoS Pathog. 2007, 3, e103.
62. Bartosch, B.; Vitelli, A.; Granier, C.; Goujon, C.; Dubuisson, J.; Pascale, S.; Scarselli, E.; Cortese, R.; Nicosia, A.; Cosset, F.L. Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J. Biol. Chem. 2003, 278, 41624-41630.
63. Hsu, M.; Zhang, J.; Flint, M.; Logvinoff, C.; Cheng-Mayer, C.; Rice, C.M.; McKeating, J.A. Hepatitis C virus glycoproteins mediate pH-dependent cell entry of pseudotyped retroviral particles. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 7271-7276.
64. Wakita, T.; Pietschmann, T.; Kato, T.; Date, T.; Miyamoto, M.; Zhao, Z.; Murthy, K.; Habermann, A.; Krausslich, H.G.; Mizokami, M.; Bartenschlager, R.; Liang, T.J. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005, 11, 791-796.
65. Goffard, A.; Dubuisson, J. Glycosylation of hepatitis C virus envelope proteins. Biochimie 2003, 85, 295-301.
66. Krey, T.; d'Alayer, J.; Kikuti, C.M.; Saulnier, A.; Damier-Piolle, L.; Petitpas, I.; Johansson, D.X.; Tawar, R.G.; Baron, B.; Robert, B.; England, P.; Persson, M.A.A.; Martin, A.; Rey, F.A. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLoS Pathog. 2010, 6, e1000762.
67. Cocquerel, L.; Duvet, S.; Meunier, J.C.; Pillez, A.; Cacan, R.; Wychowski, C.; Dubuisson, J. The transmembrane domain of hepatitis C virus glycoprotein E1 is a signal for static retention in the endoplasmic reticulum. J. Virol. 1999, 73, 2641-2649.
68. Cocquerel, L.; Meunier, J.C.; Pillez, A.; Wychowski, C.; Dubuisson, J. A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. J. Virol. 1998, 72, 2183-2191.
69. Rouille, Y.; Helle, F.; Delgrange, D.; Roingeard, P.; Voisset, C.; Blanchard, E.; Belouzard, S.; McKeating, J.; Patel, A.H.; Maertens, G.; Wakita, T.; Wychowski, C.; Dubuisson, J. Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus. J. Virol. 2006, 80, 2832-2841.
70. Lavie, M.; Goffard, A.; Dubuisson, J. Assembly of a functional HCV glycoprotein heterodimer. Curr. Issues Mol. Biol. 2007, 9, 71-86.
71. Deleersnyder, V.; Pillez, A.; Wychowski, C.; Blight, K.; Xu, J.; Hahn, Y.S.; Rice, C.M.; Dubuisson, J. Formation of native hepatitis C virus glycoprotein complexes. J. Virol. 1997, 71, 697-704.
72. Op De Beeck, A.; Voisset, C.; Bartosch, B.; Ciczora, Y.; Cocquerel, L.; Keck, Z.; Foung, S.; Cosset, F.L.; Dubuisson, J. Characterization of functional hepatitis C virus envelope glycoproteins. J. Virol. 2004, 78, 2994-3002.
73. Vieyres, G.; Thomas, X.; Descamps, V.; Duverlie, G.; Patel, A.H.; Dubuisson, J. Characterization of the Envelope Glycoproteins Associated with Infectious Hepatitis C Virus. J. Virol. 2010, in press.
74. Icard, V.; Diaz, O.; Scholtes, C.; Perrin-Cocon, L.; Ramière, C.; Bartenschlager, R.; Penin, F.; Lotteau, V.; André, P. Secretion of hepatitis C virus envelope glycoproteins depends on assembly of apolipoprotein B positive lipoproteins. PLoS ONE 2009, 4, e4233.
75. Pecheur, E.I.; Diaz, O.; Molle, J.; Icard, V.; Bonnafous, P.; Lambert, O.; Andre, P. Morphological characterization and fusion properties of triglyceride-rich lipoproteins obtained from cells transduced with hepatitis C virus glycoproteins. J. Biol. Chem. 2010, 285, 25802-11.
76. Andre, P.; Komurian-Pradel, F.; Deforges, S.; Perret, M.; Berland, J.L.; Sodoyer, M.; Pol, S.; Brechot, C.; Paranhos-Baccala, G.; Lotteau, V. Characterization of low- and very-low-density hepatitis C virus RNA-containing particles. J. Virol. 2002, 76, 6919-6928.
77. Chang, K.S.; Jiang, J.; Cai, Z.; Luo, G. Human apolipoprotein e is required for infectivity and production of hepatitis C virus in cell culture. J. Virol. 2007, 81, 13783-13793.
78. Lindenbach, B.D.; Meuleman, P.; Ploss, A.; Vanwolleghem, T.; Syder, A.J.; McKeating, J.A.; Lanford, R.E.; Feinstone, S.M.; Major, M.E.; Leroux-Roels, G.; Rice, C.M. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 3805-3809.
79. Sundaram, M.; Yao, Z. Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion. Nutr. Metab. (Lond.) 2010, 7, 35.
80. Huang, H.; Sun, F.; Owen, D.M.; Li, W.; Chen, Y.; Gale, M., Jr.; Ye, J. Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 5848-5853.
81. Nahmias, Y.; Goldwasser, J.; Casali, M.; van Poll, D.; Wakita, T.; Chung, R.T.; Yarmush, M.L. Apolipoprotein B-dependent hepatitis C virus secretion is inhibited by the grapefruit flavonoid naringenin. Hepatology 2008, 47, 1437-1445.
82. Gastaminza, P.; Cheng, G.; Wieland, S.; Zhong, J.; Liao, W.; Chisari, F.V. Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion. J. Virol. 2008, 82, 2120-2129.
83. Jiang, J.; Luo, G. Apolipoprotein E but Not B Is Required for the Formation of infectious Hepatitis C Virus Particles. J. Virol. 2009, 83, 12680-91.
84. Benga, W.J.A.; Krieger, S.E.; Dimitrova, M.; Zeisel, M.B.; Parnot, M.; Lupberger, J.; Hildt, E.; Luo, G.; McLauchlan, J.; Baumert, T.F.; Schuster, C. Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles. Hepatology 2010, 51, 43-53.
85. Sánchez-San Martín, C.; Liu, C.Y.; Kielian, M. Dealing with low pH: entry and exit of alphaviruses and flaviviruses. Trends Microbiol. 2009, 17, 514-521.
86. 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.
87. Tscherne, D.M.; Jones, C.T.; Evans, M.J.; Lindenbach, B.D.; McKeating, J.A.; Rice, C.M. Timeand temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J. Virol. 2006, 80, 1734-1741.
88. Choo, Q.L.; Kuo, G.; Weiner, A.J.; Overby, L.R.; Bradley, D.W.; Houghton, M. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 1989, 244, 359-362.
89. Penin, F.; Dubuisson, J.; Rey, F.A.; Moradpour, D.; Pawlotsky, J.M. Structural biology of hepatitis C virus. Hepatology 2004, 39, 5-19.
90. Buckwold, V.E.; Beer, B.E.; Donis, R.O. Bovine viral diarrhea virus as a surrogate model of hepatitis C virus for the evaluation of antiviral agents. Antiviral Res. 2003, 60, 1-15.
91. 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.
92. Drummer, H.E.; Maerz, A.; Poumbourios, P. Cell surface expression of functional hepatitis C virus E1 and E2 glycoproteins. FEBS Lett. 2003, 546, 385-390.
93. Lindenbach, B.D.; Evans, M.J.; Syder, A.J.; Wölk, B.; Tellinghuisen, T.L.; Liu, C.C.; Maruyama, T.; Hynes, R.O.; Burton, D.R.; McKeating, J.A.; Rice, C.M. Complete replication of hepatitis C virus in cell culture. Science 2005, 309, 623-626.
94. Zhong, J.; Gastaminza, P.; Cheng, G.; Kapadia, S.; Kato, T.; Burton, D.R.; Wieland, S.F.; Uprichard, S.L.; Wakita, T.; Chisari, F.V. Robust hepatitis C virus infection in vitro. Proc. Natl Acad. Sci. U. S. A. 2005, 102, 9294-9299.
95. Meuleman, P.; Libbrecht, L.; De Vos, R.; de Hemptinne, B.; Gevaert, K.; Vandekerckhove, J.; Roskams, T.; Leroux-Roels, G. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatology 2005, 41, 847-856.
96. Mercer, D.F.; Schiller, D.E.; Elliott, J.F.; Douglas, D.N.; Hao, C.; Rinfret, A.; Addison, W.R.; Fischer, K.P.; Churchill, T.A.; Lakey, J.R.; Tyrrell, D.L.; Kneteman, N.M. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 2001, 7, 927-933.
97. Sarrazin, C.; Zeuzem, S. Resistance to direct antiviral agents in patients with hepatitis C virus infection. Gastroenterology 2010, 138, 447-462.
98. Zeisel, M.B.; Barth, H.; Schuster, C.; Baumert, T.F. Hepatitis C virus entry: molecular mechanisms and targets for antiviral therapy. Front. Biosci. 2009, 14, 3274-3285.
99. Thompson, A.J.; McHutchison, J.G. Antiviral resistance and specifically targeted therapy for HCV (STAT-C). J. Viral. Hepat. 2009, 16, 377-387.
100. Foy, E.; Li, K.; Wang, C.; Sumpter, R., Jr.; Ikeda, M.; Lemon, S.M.; Gale, M., Jr. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 2003, 300, 1145-1148.
101. Salzwedel, K.; Martin, D.E.; Sakalian, M. Maturation inhibitors: a new therapeutic class targets the virus structure. AIDS Rev. 2007, 9, 162-172.
102. Flajolet, M.; Rotondo, G.; Daviet, L.; Bergametti, F.; Inchauspe, G.; Tiollais, P.; Transy, C.; Legrain, P. A genomic approach of the hepatitis C virus generates a protein interaction map. Gene 2000, 242, 369-379.
103. Kota, S.; Scampavia, L.; Spicer, T.; Beeler, A.B.; Takahashi, V.; Snyder, J.K.; Porco, J.A.; Hodder, P.; Strosberg, A.D. A time-resolved fluorescence-resonance energy transfer assay for identifying inhibitors of hepatitis C virus core dimerization. Assay Drug Dev. Technol. 2010, 8, 96-105.
104. Griffin, S.; Stgelais, C.; Owsianka, A.M.; Patel, A.H.; Rowlands, D.; Harris, M. Genotypedependent sensitivity of hepatitis C virus to inhibitors of the p7 ion channel. Hepatology 2008, 48, 1779-1790.
105. Luscombe, C.A.; Huang, Z.; Murray, M.G.; Miller, M.; Wilkinson, J.; Ewart, G.D. 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. Antiviral Res. 2010, 86, 144-153.
106. Steinmann, E.; Whitfield, T.; Kallis, S.; Dwek, R.A.; Zitzmann, N.; Pietschmann, T.; Bartenschlager, R. Antiviral effects of amantadine and iminosugar derivatives against hepatitis C virus. Hepatology 2007, 46, 330-338.
107. Durantel, D.; Branza-Nichita, N.; Carrouee-Durantel, S.; Butters, T.D.; Dwek, R.A.; Zitzmann, N. Study of the mechanism of antiviral action of iminosugar derivatives against bovine viral iarrhea virus. J. Virol. 2001, 75, 8987-8998.
108. Bartenschlager, R. The NS3/4A proteinase of the hepatitis C virus: unravelling structure and function of an unusual enzyme and a prime target for antiviral therapy. J. Viral. Hepat. 1999, 6, 165-181.
109. Kim, D.W.; Gwack, Y.; Han, J.H.; Choe, J. C-terminal domain of the hepatitis C virus NS3 protein contains an RNA helicase activity. Biochem. Biophys. Res. Commun. 1995, 215, 160-166.
110. Gao, M.; Nettles, R.E.; Belema, M.; Snyder, L.B.; Nguyen, V.N.; Fridell, R.A.; Serrano-Wu, M.H.; Langley, D.R.; Sun, J.H.; O'Boyle, D.R., 2nd; Lemm, J.A.; Wang, C.; Knipe, J.O.; Chien, C.; Colonno, R.J.; Grasela, D.M.; Meanwell, N.A.; Hamann, L.G. Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 2010, 465, 96-100.
111. Helenius, A.; Aebi, M. Intracellular functions of N-linked glycans. Science 2001, 291, 2364-2369.
112. Branza-Nichita, N.; Petrescu, A.J.; Negroiu, G.; Dwek, R.A.; Petrescu, S.M. N-glycosylation processing and glycoprotein folding-lessons from the tyrosinase-related proteins. Chem. Rev. 2000, 100, 4697-4712.
113. Dwek, R.A.; Butters, T.D.; Platt, F.M.; Zitzmann, N. Targeting glycosylation as a therapeutic approach. Nat. Rev. Drug. Discov. 2002, 1, 65-75.
114. 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.
115. Wu, S.F.; Lee, C.J.; Liao, C.L.; Dwek, R.A.; Zitzmann, N.; Lin, Y.L. Antiviral effects of an iminosugar derivative on flavivirus infections. J. Virol. 2002, 76, 3596-3604.
116. Zitzmann, N.; Mehta, A.S.; Carrouée, S.; Butters, T.D.; Platt, F.M.; McCauley, J.; Blumberg, B.S.; Dwek, R.A.; Block, T.M. Imino sugars inhibit the formation and secretion of bovine viral diarrhea virus, a pestivirus model of hepatitis C virus: implications for the development of broad spectrum anti-hepatitis virus agents. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 11878-11882.
117. Takkenberg, B.; de Bruijne, J.; Weegink, C.; Jansen, P.; Reesink, H. Novel therapies in hepatitis B and C. Curr. Gastroenterol. Rep. 2008, 10, 81-90.
118. Pawlotsky, J.-M.; Chevaliez, S.; McHutchison, J.G. The hepatitis C virus life cycle as a target for new antiviral therapies. Gastroenterology 2007, 132, 1979-1998.
119. Cuchel, M.; Bloedon, L.T.; Szapary, P.O.; Kolansky, D.M.; Wolfe, M.L.; Sarkis, A.; Millar, J.S.; Ikewaki, K.; Siegelman, E.S.; Gregg, R.E.; Rader, D.J. Inhibition of microsomal triglyceride transfer protein in familial hypercholesterolemia. N. Engl. J. Med. 2007, 356, 148-156.
120. Samaha, F.F.; McKenney, J.; Bloedon, L.T.; Sasiela, W.J.; Rader, D.J. Inhibition of microsomal triglyceride transfer protein alone or with ezetimibe in patients with moderate hypercholesterolemia. Nat. Clin. Pract. Cardiovasc. Med. 2008, 5, 497-505.
121. Ishizaka, N.; Ishizaka, Y.; Takahashi, E.; Tooda, E.; Hashimoto, H.; Nagai, R.; Yamakado, M. Association between hepatitis C virus seropositivity, carotid-artery plaque, and intima-media thickening. Lancet 2002, 359, 133-135.
122. Mirandola, S.; Bowman, D.; Hussain, M.M.; Alberti, A. Hepatic steatosis in hepatitis C is a storage disease due to HCV interaction with microsomal triglyceride transfer protein (MTP). Nutr. Metab. (Lond.) 2010, 7, 13.
123. Gastaminza, P.; Whitten-Bauer, C.; Chisari, F.V. Unbiased probing of the entire hepatitis C virus life cycle identifies clinical compounds that target multiple aspects of the infection. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 291-296.
124. Chockalingam, K.; Simeon, R.L.; Rice, C.M.; Chen, Z. A cell protection screen reveals potent inhibitors of multiple stages of the hepatitis C virus life cycle. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 3764-3769.