Hepatitis C virus RNA replication and assembly: Living on the fat of the land

Cell Host and Microbe

Volumn 16, Issue 5, 2014, Pages 569-579

  Paul, David ^a   Madan, Vanesa ^a   Bartenschlager, Ralf ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA; VIRUS PROTEIN;

BIOGENESIS; HEPATITIS C VIRUS; NONHUMAN; REGULATORY MECHANISM; REVIEW; RNA SYNTHESIS; RNA TRANSLATION; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS PARTICLE; VIRUS REPLICATION; BIOSYNTHESIS; CELL CULTURE; CYTOPLASM; GENETICS; HEPACIVIRUS; HOST PATHOGEN INTERACTION; HUMAN; INTRACELLULAR MEMBRANE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; VIRION;

HEPATITIS C VIRUS;

CELLS, CULTURED; CYTOPLASM; HEPACIVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTRACELLULAR MEMBRANES; LIPID METABOLISM; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS; VIRION; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 84910629145     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.10.008     Document Type: Review

References (118)

1. H. Ago, T. Adachi, A. Yoshida, M. Yamamoto, N. Habuka, K. Yatsunami, and M. Miyano Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus Structure 7 1999 1417 1426
2. N. Altan-Bonnet, and T. Balla Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms Trends Biochem. Sci. 37 2012 293 302
3. P. André, F. Komurian-Pradel, S. Deforges, M. Perret, J.L. Berland, M. Sodoyer, S. Pol, C. Bréchot, G. Paranhos-Baccalà, and V. Lotteau Characterization of low- and very-low-density hepatitis C virus RNA-containing particles J. Virol. 76 2002 6919 6928
4. N. Appel, M. Zayas, S. Miller, J. Krijnse-Locker, T. Schaller, P. Friebe, S. Kallis, U. Engel, and R. Bartenschlager Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly PLoS Pathog. 4 2008 e1000035
5. T.C. Appleby, R. Anderson, O. Fedorova, A.M. Pyle, R. Wang, X. Liu, K.M. Brendza, and J.R. Somoza Visualizing ATP-dependent RNA translocation by the NS3 helicase from HCV J. Mol. Biol. 405 2011 1139 1153
6. R. Bartenschlager, F. Penin, V. Lohmann, and P. André Assembly of infectious hepatitis C virus particles Trends Microbiol. 19 2011 95 103
7. R. Bartenschlager, V. Lohmann, and F. Penin The molecular and structural basis of advanced antiviral therapy for hepatitis C virus infection Nat. Rev. Microbiol. 11 2013 482 496
8. A. Bianco, V. Reghellin, L. Donnici, S. Fenu, R. Alvarez, C. Baruffa, F. Peri, M. Pagani, S. Abrignani, P. Neddermann, and R. De Francesco Metabolism of phosphatidylinositol 4-kinase IIIα-dependent PI4P Is subverted by HCV and is targeted by a 4-anilino quinazoline with antiviral activity PLoS Pathog. 8 2012 e1002576
9. A. Boyer, A. Dumans, E. Beaumont, L. Etienne, P. Roingeard, and J.C. Meunier The association of hepatitis C virus glycoproteins with apolipoproteins E and B early in assembly is conserved in lipoviral particles J. Biol. Chem. 289 2014 18904 18913
10. V. Brass, J.M. Berke, R. Montserret, H.E. Blum, F. Penin, and D. Moradpour Structural determinants for membrane association and dynamic organization of the hepatitis C virus NS3-4A complex Proc. Natl. Acad. Sci. USA 105 2008 14545 14550
11. S. Bressanelli, L. Tomei, A. Roussel, I. Incitti, R.L. Vitale, M. Mathieu, R. De Francesco, and F.A. Rey Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus Proc. Natl. Acad. Sci. USA 96 1999 13034 13039
12. S. Bressanelli, L. Tomei, F.A. Rey, and R. De Francesco Structural analysis of the hepatitis C virus RNA polymerase in complex with ribonucleotides J. Virol. 76 2002 3482 3492
13. G. Camus, E. Herker, A.A. Modi, J.T. Haas, H.R. Ramage, R.V. Farese Jr., and M. Ott Diacylglycerol acyltransferase-1 localizes hepatitis C virus NS5A protein to lipid droplets and enhances NS5A interaction with the viral capsid core J. Biol. Chem. 288 2013 9915 9923
14. M.T. Catanese, K. Uryu, M. Kopp, T.J. Edwards, L. Andrus, W.J. Rice, M. Silvestry, R.J. Kuhn, and C.M. Rice Ultrastructural analysis of hepatitis C virus particles Proc. Natl. Acad. Sci. USA 110 2013 9505 9510
15. K.S. Chang, J. Jiang, Z. Cai, and G. Luo Human apolipoprotein e is required for infectivity and production of hepatitis C virus in cell culture J. Virol. 81 2007 13783 13793
16. T.C. Chao, W.C. Su, J.Y. Huang, Y.C. Chen, K.S. Jeng, H.D. Wang, and M.M. Lai Proline-serine-threonine phosphatase-interacting protein 2 (PSTPIP2), a host membrane-deforming protein, is critical for membranous web formation in hepatitis C virus replication J. Virol. 86 2012 1739 1749
17. L. Chatel-Chaix, M.A. Germain, A. Motorina, É. Bonneil, P. Thibault, M. Baril, and D. Lamarre A host YB-1 ribonucleoprotein complex is hijacked by hepatitis C virus for the control of NS3-dependent particle production J. Virol. 87 2013 11704 11720
18. L. Coelmont, X. Hanoulle, U. Chatterji, C. Berger, J. Snoeck, M. Bobardt, P. Lim, I. Vliegen, J. Paeshuyse, and G. Vuagniaux DEB025 (Alisporivir) inhibits hepatitis C virus replication by preventing a cyclophilin A inducedcis-trans isomerisation in domain II of NS5A PLoS ONE 5 2010 e13687
19. K.E. Coller, N.S. Heaton, K.L. Berger, J.D. Cooper, J.L. Saunders, and G. Randall Molecular determinants and dynamics of hepatitis C virus secretion PLoS Pathog. 8 2012 e1002466
20. D.G. Cordek, T.J. Croom-Perez, J. Hwang, M.R. Hargittai, C.V. Subba-Reddy, Q. Han, M.F. Lodeiro, G. Ning, T.S. McCrory, and J.J. Arnold Expanding the proteome of an RNA virus by phosphorylation of an intrinsically disordered viral protein J. Biol. Chem. 289 2014 24397 24416
21. L. Corless, C.M. Crump, S.D. Griffin, and M. Harris Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles J. Gen. Virol. 91 2010 362 372
22. N.A. Counihan, S.M. Rawlinson, and B.D. Lindenbach Trafficking of hepatitis C virus core protein during virus particle assembly PLoS Pathog. 7 2011 e1002302
23. D. Da Costa, M. Turek, D.J. Felmlee, E. Girardi, S. Pfeffer, G. Long, R. Bartenschlager, M.B. Zeisel, and T.F. Baumert Reconstitution of the entire hepatitis C virus life cycle in nonhepatic cells J. Virol. 86 2012 11919 11925
24. D.L. Diamond, A.J. Syder, J.M. Jacobs, C.M. Sorensen, K.A. Walters, S.C. Proll, J.E. McDermott, M.A. Gritsenko, Q. Zhang, and R. Zhao Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics PLoS Pathog. 6 2010 e1000719
25. Q. Ding, M. von Schaewen, and A. Ploss The impact of hepatitis C virus entry on viral tropism Cell Host Microbe 16 2014 562 568 this issue
26. M. Dreux, P. Gastaminza, S.F. Wieland, and F.V. Chisari The autophagy machinery is required to initiate hepatitis C virus replication Proc. Natl. Acad. Sci. USA 106 2009 14046 14051
27. S. Dumont, W. Cheng, V. Serebrov, R.K. Beran, I. Tinoco Jr., A.M. Pyle, and C. Bustamante RNA translocation and unwinding mechanism of HCV NS3 helicase and its coordination by ATP Nature 439 2006 105 108
28. D. Egger, B. Wölk, R. Gosert, L. Bianchi, H.E. Blum, D. Moradpour, and K. Bienz Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex J. Virol. 76 2002 5974 5984
29. M.J. Evans, C.M. Rice, and S.P. Goff Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication Proc. Natl. Acad. Sci. USA 101 2004 13038 13043
30. E. Ferrari, Z. He, R.E. Palermo, and H.C. Huang Hepatitis C virus NS5B polymerase exhibits distinct nucleotide requirements for initiation and elongation J. Biol. Chem. 283 2008 33893 33901
31. P. Ferraris, E. Blanchard, and P. Roingeard Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes J. Gen. Virol. 91 2010 2230 2237
32. P. Ferraris, E. Beaumont, R. Uzbekov, D. Brand, J. Gaillard, E. Blanchard, and P. Roingeard Sequential biogenesis of host cell membrane rearrangements induced by hepatitis C virus infection Cell. Mol. Life Sci. 70 2013 1297 1306
33. T.L. Foster, P. Gallay, N.J. Stonehouse, and M. Harris Cyclophilin A interacts with domain II of hepatitis C virus NS5A and stimulates RNA binding in an isomerase-dependent manner J. Virol. 85 2011 7460 7464
34. L. Gao, H. Aizaki, J.W. He, and M.M. Lai Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft J. Virol. 78 2004 3480 3488
35. P. Gastaminza, G. Cheng, S. Wieland, J. Zhong, W. Liao, and F.V. Chisari Cellular determinants of hepatitis C virus assembly, maturation, degradation, and secretion J. Virol. 82 2008 2120 2129
36. P. Gastaminza, K.A. Dryden, B. Boyd, M.R. Wood, M. Law, M. Yeager, and F.V. Chisari Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture J. Virol. 84 2010 10999 11009
37. R. Gosert, D. Egger, V. Lohmann, R. Bartenschlager, H.E. Blum, K. Bienz, and D. Moradpour Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons J. Virol. 77 2003 5487 5492
38. H. Gouklani, R.A. Bull, C. Beyer, F. Coulibaly, E.J. Gowans, H.E. Drummer, H.J. Netter, P.A. White, and G. Haqshenas Hepatitis C virus nonstructural protein 5B is involved in virus morphogenesis J. Virol. 86 2012 5080 5088
39. J. Gouttenoire, V. Castet, R. Montserret, N. Arora, V. Raussens, J.M. Ruysschaert, E. Diesis, H.E. Blum, F. Penin, and D. Moradpour Identification of a novel determinant for membrane association in hepatitis C virus nonstructural protein 4B J. Virol. 83 2009 6257 6268
40. J. Gouttenoire, P. Roingeard, F. Penin, and D. Moradpour Amphipathic alpha-helix AH2 is a major determinant for the oligomerization of hepatitis C virus nonstructural protein 4B J. Virol. 84 2010 12529 12537
41. 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
42. D. Harrus, N. Ahmed-El-Sayed, P.C. Simister, S. Miller, M. Triconnet, C.H. Hagedorn, K. Mahias, F.A. Rey, T. Astier-Gin, and S. Bressanelli Further insights into the roles of GTP and the C terminus of the hepatitis C virus polymerase in the initiation of RNA synthesis J. Biol. Chem. 285 2010 32906 32918
43. E. Herker, C. Harris, C. Hernandez, A. Carpentier, K. Kaehlcke, A.R. Rosenberg, R.V. Farese Jr., and M. Ott Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1 Nat. Med. 16 2010 1295 1298
44. M.R. Herod, V. Schregel, C. Hinds, M. Liu, J. McLauchlan, and C.J. McCormick Genetic complementation of hepatitis C virus nonstructural protein functions associated with replication exhibits requirements that differ from those for virion assembly J. Virol. 88 2014 2748 2762
45. Y. Hirata, K. Ikeda, M. Sudoh, Y. Tokunaga, A. Suzuki, L. Weng, M. Ohta, Y. Tobita, K. Okano, and K. Ozeki Self-enhancement of hepatitis C virus replication by promotion of specific sphingolipid biosynthesis PLoS Pathog. 8 2012 e1002860
46. M. Honda, L.H. Ping, R.C. Rijnbrand, E. Amphlett, B. Clarke, D. Rowlands, and S.M. Lemon Structural requirements for initiation of translation by internal ribosome entry within genome-length hepatitis C virus RNA Virology 222 1996 31 42
47. S.M. Horner, H.M. Liu, H.S. Park, J. Briley, and M. Gale Jr. Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus Proc. Natl. Acad. Sci. USA 108 2011 14590 14595
48. H. Huang, F. Sun, D.M. Owen, W. Li, Y. Chen, M. Gale Jr., and J. Ye Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins Proc. Natl. Acad. Sci. USA 104 2007 5848 5853
49. J.T. Huang, C.P. Tseng, M.H. Liao, S.C. Lu, W.Z. Yeh, N. Sakamoto, C.M. Chen, and J.C. Cheng Hepatitis C virus replication is modulated by the interaction of nonstructural protein NS5B and fatty acid synthase J. Virol. 87 2013 4994 5004
50. K. Hueging, M. Doepke, G. Vieyres, D. Bankwitz, A. Frentzen, J. Doerrbecker, F. Gumz, S. Haid, B. Wölk, L. Kaderali, and T. Pietschmann Apolipoprotein E codetermines tissue tropism of hepatitis C virus and is crucial for viral cell-to-cell transmission by contributing to a postenvelopment step of assembly J. Virol. 88 2014 1433 1446
51. O. Isken, M. Baroth, C.W. Grassmann, S. Weinlich, D.H. Ostareck, A. Ostareck-Lederer, and S.E. Behrens Nuclear factors are involved in hepatitis C virus RNA replication RNA 13 2007 1675 1692
52. B. Jammart, M. Michelet, E.I. Pécheur, R. Parent, B. Bartosch, F. Zoulim, and D. Durantel Very-low-density lipoprotein (VLDL)-producing and hepatitis C virus-replicating HepG2 cells secrete no more lipoviroparticles than VLDL-deficient Huh7.5 cells J. Virol. 87 2013 5065 5080
53. J. Jiang, and G. Luo Apolipoprotein E but not B is required for the formation of infectious hepatitis C virus particles J. Virol. 83 2009 12680 12691
54. V. Jirasko, R. Montserret, J.Y. Lee, J. Gouttenoire, D. Moradpour, F. Penin, and R. Bartenschlager Structural and functional studies of nonstructural protein 2 of the hepatitis C virus reveal its key role as organizer of virion assembly PLoS Pathog. 6 2010 e1001233
55. D.M. Jones, A.H. Patel, P. Targett-Adams, and J. McLauchlan The hepatitis C virus NS4B protein can trans-complement viral RNA replication and modulates production of infectious virus J. Virol. 83 2009 2163 2177
56. C.L. Jopling, M. Yi, A.M. Lancaster, S.M. Lemon, and P. Sarnow Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA Science 309 2005 1577 1581
57. A. Kaul, S. Stauffer, C. Berger, T. Pertel, J. Schmitt, S. Kallis, M. Zayas, V. Lohmann, J. Luban, and R. Bartenschlager Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics PLoS Pathog. 5 2009 e1000546
58. P.Y. Ke, and S.S. Chen Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro J. Clin. Invest. 121 2011 37 56
59. I. Khan, D.S. Katikaneni, Q. Han, L. Sanchez-Felipe, K. Hanada, R.L. Ambrose, J.M. Mackenzie, and K.V. Konan Modulation of hepatitis C virus genome replication by glycosphingolipids and four-phosphate adaptor protein 2 J. Virol. 88 2014 12276 12295
60. A. Kohlway, N. Pirakitikulr, F.N. Barrera, O. Potapova, D.M. Engelman, A.M. Pyle, and B.D. Lindenbach Hepatitis C virus RNA replication and virus particle assembly require specific dimerization of the NS4A protein transmembrane domain J. Virol. 88 2014 628 642
61. A. Kohlway, N. Pirakitikulr, S.C. Ding, F. Yang, D. Luo, B.D. Lindenbach, and A.M. Pyle The linker region of NS3 plays a critical role in the replication and infectivity of hepatitis C virus J. Virol. 88 2014 10970 10974
62. S.M. Lambert, D.R. Langley, J.A. Garnett, R. Angell, K. Hedgethorne, N.A. Meanwell, and S.J. Matthews The crystal structure of NS5A domain 1 from genotype 1a reveals new clues to the mechanism of action for dimeric HCV inhibitors Protein Sci. 23 2014 723 734
63. J.Y. Lee, E.G. Acosta, I.K. Stoeck, G. Long, M.S. Hiet, B. Mueller, O.T. Fackler, S. Kallis, and R. Bartenschlager Apolipoprotein e likely contributes to a maturation step of infectious hepatitis C virus particles and interacts with viral envelope glycoproteins J. Virol. 88 2014 12422 12437
64. C.A. Lesburg, M.B. Cable, E. Ferrari, Z. Hong, A.F. Mannarino, and P.C. Weber Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site Nat. Struct. Biol. 6 1999 937 943
65. Q. Li, V. Pène, S. Krishnamurthy, H. Cha, and T.J. Liang Hepatitis C virus infection activates an innate pathway involving IKK-α in lipogenesis and viral assembly Nat. Med. 19 2013 722 729
66. 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
67. B.D. Lindenbach, P. Meuleman, A. Ploss, T. Vanwolleghem, A.J. Syder, J.A. McKeating, R.E. Lanford, S.M. Feinstone, M.E. Major, G. Leroux-Roels, and C.M. Rice Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro Proc. Natl. Acad. Sci. USA 103 2006 3805 3809
68. B.D. Lindenbach, B.M. Prágai, R. Montserret, R.K. Beran, A.M. Pyle, F. Penin, and C.M. Rice The C terminus of hepatitis C virus NS4A encodes an electrostatic switch that regulates NS5A hyperphosphorylation and viral replication J. Virol. 81 2007 8905 8918
69. Z. Liu, F. Yang, J.M. Robotham, and H. Tang Critical role of cyclophilin A and its prolyl-peptidyl isomerase activity in the structure and function of the hepatitis C virus replication complex J. Virol. 83 2009 6554 6565
70. V. Lohmann Hepatitis C virus RNA replication Curr. Top. Microbiol. Immunol. 369 2013 167 198
71. V. Lohmann, F. Körner, 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
72. V. Lohmann, H. Overton, and R. Bartenschlager Selective stimulation of hepatitis C virus and pestivirus NS5B RNA polymerase activity by GTP J. Biol. Chem. 274 1999 10807 10815
73. G. Long, M.S. Hiet, M.P. Windisch, J.Y. Lee, V. Lohmann, and R. Bartenschlager Mouse hepatic cells support assembly of infectious hepatitis C virus particles Gastroenterology 141 2011 1057 1066
74. R.A. Love, O. Brodsky, M.J. Hickey, P.A. Wells, and C.N. Cronin Crystal structure of a novel dimeric form of NS5A domain I protein from hepatitis C virus J. Virol. 83 2009 4395 4403
75. M. Lundin, H. Lindström, C. Grönwall, and M.A. Persson Dual topology of the processed hepatitis C virus protein NS4B is influenced by the NS5A protein J. Gen. Virol. 87 2006 3263 3272
76. V. Madan, D. Paul, V. Lohmann, and R. Bartenschlager Inhibition of HCV replication by cyclophilin antagonists is linked to replication fitness and occurs by inhibition of membranous web formation Gastroenterology 146 2014 1361 1372 e1-e9
77. T. Masaki, S. Matsunaga, H. Takahashi, K. Nakashima, Y. Kimura, M. Ito, M. Matsuda, A. Murayama, T. Kato, and H. Hirano Involvement of hepatitis C virus NS5A hyperphosphorylation mediated by casein kinase I-α in infectious virus production J. Virol. 88 2014 7541 7555
78. N. Menzel, W. Fischl, K. Hueging, D. Bankwitz, A. Frentzen, S. Haid, J. Gentzsch, L. Kaderali, R. Bartenschlager, and T. Pietschmann MAP-kinase regulated cytosolic phospholipase A2 activity is essential for production of infectious hepatitis C virus particles PLoS Pathog. 8 2012 e1002829
79. A. Merz, G. Long, M.S. Hiet, B. Brügger, P. Chlanda, P. Andre, F. Wieland, J. Krijnse-Locker, and R. Bartenschlager Biochemical and morphological properties of hepatitis C virus particles and determination of their lipidome J. Biol. Chem. 286 2011 3018 3032
80. B. Mesmin, J. Bigay, J. Moser von Filseck, S. Lacas-Gervais, G. Drin, and B. Antonny A four-step cycle driven by PI(4)P hydrolysis directs sterol/PI(4)P exchange by the ER-Golgi tether OSBP Cell 155 2013 830 843
81. J.C. Meunier, R.S. Russell, R.E. Engle, K.N. Faulk, R.H. Purcell, and S.U. Emerson Apolipoprotein c1 association with hepatitis C virus J. Virol. 82 2008 9647 9656
82. Y. Miyanari, K. Atsuzawa, N. Usuda, K. Watashi, T. Hishiki, M. Zayas, R. Bartenschlager, T. Wakita, M. Hijikata, and K. Shimotohno The lipid droplet is an important organelle for hepatitis C virus production Nat. Cell Biol. 9 2007 1089 1097
83. D. Moradpour, and F. Penin Hepatitis C virus proteins: from structure to function Curr. Top. Microbiol. Immunol. 369 2013 113 142
84. R.T. Mosley, T.E. Edwards, E. Murakami, A.M. Lam, R.L. Grice, J. Du, M.J. Sofia, P.A. Furman, and M.J. Otto Structure of hepatitis C virus polymerase in complex with primer-template RNA J. Virol. 86 2012 6503 6511
85. C.J. Neufeldt, M.A. Joyce, A. Levin, R.H. Steenbergen, D. Pang, J. Shields, D.L. Tyrrell, and R.W. Wozniak Hepatitis C virus-induced cytoplasmic organelles use the nuclear transport machinery to establish an environment conducive to virus replication PLoS Pathog. 9 2013 e1003744
86. M. Niepmann Hepatitis C virus RNA translation Curr. Top. Microbiol. Immunol. 369 2013 143 166
87. M.F. Palomares-Jerez, H. Nemesio, and J. Villalaín Interaction with membranes of the full C-terminal domain of protein NS4B from hepatitis C virus Biochim. Biophys. Acta 1818 2012 2536 2549
88. A.M. Paredes, and K.J. Blight A genetic interaction between hepatitis C virus NS4B and NS3 is important for RNA replication J. Virol. 82 2008 10671 10683
89. C.Y. Park, H.J. Jun, T. Wakita, J.H. Cheong, and S.B. Hwang Hepatitis C virus nonstructural 4B protein modulates sterol regulatory element-binding protein signaling via the AKT pathway J. Biol. Chem. 284 2009 9237 9246
90. D. Paul, and R. Bartenschlager Architecture and biogenesis of plus-strand RNA virus replication factories World J Virol 2 2013 32 48
91. D. Paul, I. Romero-Brey, J. Gouttenoire, S. Stoitsova, J. Krijnse-Locker, D. Moradpour, and R. Bartenschlager NS4B self-interaction through conserved C-terminal elements is required for the establishment of functional hepatitis C virus replication complexes J. Virol. 85 2011 6963 6976
92. D. Paul, S. Hoppe, G. Saher, J. Krijnse-Locker, and R. Bartenschlager Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment J. Virol. 87 2013 10612 10627
93. T. Phan, R.K. Beran, C. Peters, I.C. Lorenz, and B.D. Lindenbach 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. 83 2009 8379 8395
94. C.I. Popescu, N. Callens, D. Trinel, P. Roingeard, D. Moradpour, V. Descamps, G. Duverlie, F. Penin, L. Héliot, Y. Rouillé, and J. Dubuisson NS2 protein of hepatitis C virus interacts with structural and non-structural proteins towards virus assembly PLoS Pathog. 7 2011 e1001278
95. E.M. Quezada, and C.M. Kane The Stimulatory Mechanism of Hepatitis C Virus NS5A Protein on the NS5B Catalyzed Replication Reaction In Vitro Open Biochem J 7 2013 11 14
96. C.T. Ranjith-Kumar, L. Gutshall, R.T. Sarisky, and C.C. Kao Multiple interactions within the hepatitis C virus RNA polymerase repress primer-dependent RNA synthesis J. Mol. Biol. 330 2003 675 685
97. S. Reiss, I. Rebhan, P. Backes, I. Romero-Brey, H. Erfle, P. Matula, L. Kaderali, M. Poenisch, H. Blankenburg, and M.S. Hiet Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment Cell Host Microbe 9 2011 32 45
98. I. Romero-Brey, A. Merz, A. Chiramel, J.Y. Lee, P. Chlanda, U. Haselman, R. Santarella-Mellwig, A. Habermann, S. Hoppe, and S. Kallis Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication PLoS Pathog. 8 2012 e1003056
99. C. Romero-López, A. Barroso-Deljesus, A. García-Sacristán, C. Briones, and A. Berzal-Herranz End-to-end crosstalk within the hepatitis C virus genome mediates the conformational switch of the 3'X-tail region Nucleic Acids Res. 42 2014 567 582
100. P.S. Roulin, M. Lötzerich, F. Torta, L.B. Tanner, F.J.M. van Kuppeveld, M.R. Wenk, and U.F. Greber Rhinovirus uses a phosphatidylinositol 4-phosphate/cholesterol counter-current for the formation of replication compartments at the ER-Golgi interface Cell Host Microbe 16 2014 677 690 this issue
101. N. Scrima, C. Caillet-Saguy, M. Ventura, D. Harrus, T. Astier-Gin, and S. Bressanelli Two crucial early steps in RNA synthesis by the hepatitis C virus polymerase involve a dual role of residue 405 J. Virol. 86 2012 7107 7117
102. S.T. Shi, K.J. Lee, H. Aizaki, S.B. Hwang, and M.M. Lai Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2 J. Virol. 77 2003 4160 4168
103. Y. Shirota, H. Luo, W. Qin, S. Kaneko, T. Yamashita, K. Kobayashi, and S. Murakami Hepatitis C virus (HCV) NS5A binds RNA-dependent RNA polymerase (RdRP) NS5B and modulates RNA-dependent RNA polymerase activity J. Biol. Chem. 277 2002 11149 11155
104. P. Simister, M. Schmitt, M. Geitmann, O. Wicht, U.H. Danielson, R. Klein, S. Bressanelli, and V. Lohmann Structural and functional analysis of hepatitis C virus strain JFH1 polymerase J. Virol. 83 2009 11926 11939
105. P. Simmonds The origin of hepatitis C virus Curr. Top. Microbiol. Immunol. 369 2013 1 15
106. D. Sir, C.F. Kuo, Y. Tian, H.M. Liu, E.J. Huang, J.U. Jung, K. Machida, and J.H. Ou Replication of hepatitis C virus RNA on autophagosomal membranes J. Biol. Chem. 287 2012 18036 18043
107. R.M. Smith, C.M. Walton, C.H. Wu, and G.Y. Wu Secondary structure and hybridization accessibility of hepatitis C virus 3′-terminal sequences J. Virol. 76 2002 9563 9574
108. K. Tamai, M. Shiina, N. Tanaka, T. Nakano, A. Yamamoto, Y. Kondo, E. Kakazu, J. Inoue, K. Fukushima, and K. Sano Regulation of hepatitis C virus secretion by the Hrs-dependent exosomal pathway Virology 422 2012 377 385
109. I. Tanida, M. Fukasawa, T. Ueno, E. Kominami, T. Wakita, and K. Hanada Knockdown of autophagy-related gene decreases the production of infectious hepatitis C virus particles Autophagy 5 2009 937 945
110. T.L. Tellinghuisen, J. Marcotrigiano, and C.M. Rice Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase Nature 435 2005 374 379
111. T.L. Tellinghuisen, K.L. Foss, and J. Treadaway Regulation of hepatitis C virion production via phosphorylation of the NS5A protein PLoS Pathog. 4 2008 e1000032
112. D. Verdegem, A. Badillo, J.M. Wieruszeski, I. Landrieu, A. Leroy, R. Bartenschlager, F. Penin, G. Lippens, and X. Hanoulle Domain 3 of NS5A protein from the hepatitis C virus has intrinsic α-helical propensity and is a substrate of cyclophilin A J. Biol. Chem. 286 2011 20441 20454
113. 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
114. H. Wang, J.W. Perry, A.S. Lauring, P. Neddermann, R. De Francesco, and A.W. Tai Oxysterol-binding protein is a phosphatidylinositol 4-kinase effector required for HCV replication membrane integrity and cholesterol trafficking Gastroenterology 146 2014 1373 1385 e1-e11
115. G. Waris, D.J. Felmlee, F. Negro, and A. Siddiqui Hepatitis C virus induces proteolytic cleavage of sterol regulatory element binding proteins and stimulates their phosphorylation via oxidative stress J. Virol. 81 2007 8122 8130
116. S. Weinlich, S. Hüttelmaier, A. Schierhorn, S.E. Behrens, A. Ostareck-Lederer, and D.H. Ostareck IGF2BP1 enhances HCV IRES-mediated translation initiation via the 3'UTR RNA 15 2009 1528 1542
117. D. Yamane, D.R. McGivern, T. Masaki, and S.M. Lemon Liver injury and disease pathogenesis in chronic hepatitis C Curr. Top. Microbiol. Immunol. 369 2013 263 288
118. J. Ye, C. Wang, R. Sumpter Jr., M.S. Brown, J.L. Goldstein, and M. Gale Jr. Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation Proc. Natl. Acad. Sci. USA 100 2003 15865 15870