Hepatitis C virus comes for dinner: How the hepatitis C virus interferes with autophagy

World Journal of Gastroenterology

Volumn 21, Issue 28, 2015, Pages 8492-8507

  Ploen, Daniela ^a   Hildt, Eberhard ^a,b  

^a PAUL EHRLICH INSTITUT   (Germany)

^b Standort Hannover Braunschweig   (Germany)

Author keywords

Autophagy; Hepatitis; Hepatitis C virus; Morphogenesis; Replication

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; BIOLOGICAL MARKER; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PROTEIN IRE1; SNARE PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ADAPTIVE IMMUNITY; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC LIVER DISEASE; CONJUGATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HEPATITIS C VIRUS; HUMAN; INNATE IMMUNITY; INTRACELLULAR MEMBRANE; LIGHT CHAIN; LIPOPHAGOCYTOSIS; LIVER CELL; MEMBRANE VESICLE; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; REVIEW; RNA REPLICATION; SIGNAL TRANSDUCTION; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS PARTICLE; VIRUS REPLICATION; ANIMAL; CHRONIC HEPATITIS C; CYTOPLASM VESICLE; GROWTH, DEVELOPMENT AND AGING; HEPACIVIRUS; HOST PATHOGEN INTERACTION; METABOLISM; PATHOGENICITY; PATHOLOGY; VIROLOGY; VIRUS ACTIVATION;

ANIMALS; AUTOPHAGY; CELL SURVIVAL; CYTOPLASMIC VESICLES; ENDOPLASMIC RETICULUM STRESS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; VIRUS ACTIVATION; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84937917960     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i28.8492     Document Type: Review

References (175)

1. Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology 2015; 61: 77-87 [PMID: 25069599 DOI: 10.1002/hep.27259]
2. Pawlotsky JM. New hepatitis C therapies: the toolbox, strategies, and challenges. Gastroenterology 2014; 146: 1176-1192 [PMID: 24631495 DOI: 10.1053/j.gastro.2014.03.003]
3. Kim do Y, Ahn SH, Han KH. Emerging therapies for hepatitis C. Gut Liver 2014; 8: 471-479 [PMID: 25228970 DOI: 10.5009/gnl14083]
4. Kronenberger B, Zeuzem S. New developments in HCV therapy. J Viral Hepat 2012; 19 Suppl 1: 48-51 [PMID: 22233414 DOI: 10.1111/j.1365-2893.2011.01526.x]
5. Peiffer KH, Akhras S, Himmelsbach K, Hassemer M, Finkernagel M, Carra G, Nuebling M, Chudy M, Niekamp H, Glebe D, Sarrazin C, Zeuzem S, Hildt E. Intracellular accumulation of subviral HBsAg particles and diminished Nrf2 activation in HBV genotype G expressing cells lead to an increased ROI level. J Hepatol 2015; 62: 791-798 [PMID: 25445396 DOI: 10.1016/j.jhep.2014.11.028]
6. Thomas DL. Global control of hepatitis C: where challenge meets opportunity. Nat Med 2013; 19: 850-858 [PMID: 23836235 DOI: 10.1038/nm.3184]
7. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005; 436: 967-972 [PMID: 16107837 DOI: 10.1038/nature04082]
8. Koh C, Liang TJ. What is the future of ribavirin therapy for hepatitis C? Antiviral Res 2014; 104: 34-39 [PMID: 24468277 DOI: 10.1016/j.antiviral.2014.01.005]
9. Kong W, Engel K, Wang J. Mammalian nucleoside transporters. Curr Drug Metab 2004; 5: 63-84 [PMID: 14965251]
10. Panigrahi R, Chandra PK, Ferraris P, Kurt R, Song K, Garry RF, Reiss K, Coe IR, Furihata T, Balart LA, Wu T, Dash S. Persistent hepatitis C virus infection impairs ribavirin antiviral activity through clathrin-mediated trafficking of equilibrative nucleoside transporter 1. J Virol 2015; 89: 626-642 [PMID: 25339775 DOI: 10.1128/JVI.02492-14]
11. Dreux M, Gastaminza P, Wieland SF, Chisari FV. The autophagy machinery is required to initiate hepatitis C virus replication. Proc Natl Acad Sci USA 2009; 106: 14046-14051 [PMID: 19666601 DOI: 10.1073/pnas.0907344106]
12. Ait-Goughoulte M, Kanda T, Meyer K, Ryerse JS, Ray RB, Ray R. Hepatitis C virus genotype 1a growth and induction of autophagy. J Virol 2008; 82: 2241-2249 [PMID: 18077704 DOI: 10.1128/JVI.02093-07]
13. Sir D, Kuo CF, Tian Y, Liu HM, Huang EJ, Jung JU, Machida K, Ou JH. Replication of hepatitis C virus RNA on autophagosomal membranes. J Biol Chem 2012; 287: 18036-18043 [PMID: 22496373 DOI: 10.1074/jbc.M111.320085]
14. Sir D, Chen WL, Choi J, Wakita T, Yen TS, Ou JH. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 2008; 48: 1054-1061 [PMID: 18688877 DOI: 10.1002/hep.22464]
15. Shrivastava S, Bhanja Chowdhury J, Steele R, Ray R, Ray RB. Hepatitis C virus upregulates Beclin1 for induction of autophagy and activates mTOR signaling. J Virol 2012; 86: 8705-8712 [PMID: 22674982 DOI: 10.1128/JVI.00616-12]
16. Su WC, Chao TC, Huang YL, Weng SC, Jeng KS, Lai MM. Rab5 and class III phosphoinositide 3-kinase Vps34 are involved in hepatitis C virus NS4B-induced autophagy. J Virol 2011; 85: 10561-10571 [PMID: 21835792 DOI: 10.1128/JVI.00173-11]
17. Tanida I, Fukasawa M, Ueno T, Kominami E, Wakita T, Hanada K. Knockdown of autophagy-related gene decreases the production of infectious hepatitis C virus particles. Autophagy 2009; 5: 937-945 [PMID: 19625776]
18. Grégoire IP, Richetta C, Meyniel-Schicklin L, Borel S, Pradezynski F, Diaz O, Deloire A, Azocar O, Baguet J, Le Breton M, Mangeot PE, Navratil V, Joubert PE, Flacher M, Vidalain PO, André P, Lotteau V, Biard-Piechaczyk M, Rabourdin-Combe C, Faure M. IRGM is a common target of RNA viruses that subvert the autophagy network. PLoS Pathog 2011; 7: e1002422 [PMID: 22174682 DOI: 10.1371/journal.ppat.1002422]
19. Stoeckl L, Funk A, Kopitzki A, Brandenburg B, Oess S, Will H, Sirma H, Hildt E. Identification of a structural motif crucial for infectivity of hepatitis B viruses. Proc Natl Acad Sci USA 2006; 103: 6730-6734 [PMID: 16618937 DOI: 10.1073/pnas.0509765103]
20. Shrivastava S, Raychoudhuri A, Steele R, Ray R, Ray RB. Knockdown of autophagy enhances the innate immune response in hepatitis C virus-infected hepatocytes. Hepatology 2011; 53: 406-414 [PMID: 21274862 DOI: 10.1002/hep.24073]
21. Ke PY, Chen SS. Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J Clin Invest 2011; 121: 37-56 [PMID: 21135505 DOI: 10.1172/JCI41474]
22. Ke PY, Chen SS. Autophagy in hepatitis C virus-host interactions: potential roles and therapeutic targets for liver-associated diseases. World J Gastroenterol 2014; 20: 5773-5793 [PMID: 24914338 DOI: 10.3748/wjg.v20.i19.5773]
23. Das GC, Hollinger FB. Molecular pathways for glucose homeostasis, insulin signaling and autophagy in hepatitis C virus induced insulin resistance in a cellular model. Virology 2012; 434: 5-17 [PMID: 22862962 DOI: 10.1016/j.virol.2012.07.003]
24. Bao L, Chandra PK, Moroz K, Zhang X, Thung SN, Wu T, Dash S. Impaired autophagy response in human hepatocellular carcinoma. Exp Mol Pathol 2014; 96: 149-154 [PMID: 24369267 DOI: 10.1016/j.yexmp.2013.12.002]
25. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451: 1069-1075 [PMID: 18305538 DOI: 10.1038/nature06639]
26. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40: 280-293 [PMID: 20965422 DOI: 10.1016/j.molcel.2010.09.023]
27. Alers S, Löffler AS, Wesselborg S, Stork B. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 2012; 32: 2-11 [PMID: 22025673 DOI: 10.1128/MCB.06159-11]
28. Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol 2013; 14: 759-774 [PMID: 24201109 DOI: 10.1038/nrm3696]
29. Yen WL, Shintani T, Nair U, Cao Y, Richardson BC, Li Z, Hughson FM, Baba M, Klionsky DJ. The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy. J Cell Biol 2010; 188: 101-114 [PMID: 20065092 DOI: 10.1083/jcb.200904075]
30. Reggiori F, Shintani T, Nair U, Klionsky DJ. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy 2005; 1: 101-109 [PMID: 16874040]
31. Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC. Plasma membrane contributes to the formation of preautophagosomal structures. Nat Cell Biol 2010; 12: 747-757 [PMID: 20639872 DOI: 10.1038/ncb2078]
32. Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 2008; 19: 2092-2100 [PMID: 18321988 DOI: 10.1091/mbc.E07-12-1257]
33. Fader CM, Colombo MI. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 2009; 16: 70-78 [PMID: 19008921 DOI: 10.1038/cdd.2008.168; ]
34. Silva LM, Jung JU. Modulation of the autophagy pathway by human tumor viruses. Semin Cancer Biol 2013; 23: 323-328 [PMID: 23727156 DOI: 10.1016/j.semcancer.2013.05.005]
35. Schroeder B, Schulze RJ, Weller SG, Sletten AC, Casey CA, McNiven MA. The small GTPase Rab7 as a central regulator of hepatocellular lipophagy. Hepatology 2015; 61: 1896-1907 [PMID: 25565581 DOI: 10.1002/hep.27667]
36. Itakura E, Kishi-Itakura C, Mizushima N. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell 2012; 151: 1256-1269 [PMID: 23217709 DOI: 10.1016/j.cell.2012.11.001]
37. Itakura E, Mizushima N. Syntaxin 17: the autophagosomal SNARE. Autophagy 2013; 9: 917-919 [PMID: 23466629 DOI: 10.4161/auto.24109]
38. Hegedu{combining double acute accent}s K, Takáts S, Kovács AL, Juhász G. Evolutionarily conserved role and physiological relevance of a STX17/Syx17 (syntaxin 17)-containing SNARE complex in autophagosome fusion with endosomes and lysosomes. Autophagy 2013; 9: 1642-1646 [PMID: 24113031 DOI: 10.4161/auto.25684]
39. Malhi H, Kaufman RJ. Endoplasmic reticulum stress in liver disease. J Hepatol 2011; 54: 795-809 [PMID: 21145844 DOI: 10.1016/j.jhep.2010.11.005]
40. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002; 415: 92-96 [PMID: 11780124 DOI: 10.1038/415092a]
41. Yoshida H, Oku M, Suzuki M, Mori K. pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 2006; 172: 565-575 [PMID: 16461360 DOI: 10.1083/jcb.200508145]
42. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 2002; 3: 99-111 [PMID: 12110171]
43. Jiang H, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, Wek RC. Phosphorylation of the Subunit of Eukaryotic Initiation Factor 2 Is Required for Activation of NF- B in Response to Diverse Cellular Stresses. Mol Cell Biol 2003; 23: 5651-5663 [PMID: 12897138 DOI: 10.1128/MCB.23.16.5651-566 3.2003]
44. Nakajima S, Kitamura M. Bidirectional regulation of NF-κB by reactive oxygen species: a role of unfolded protein response. Free Radic Biol Med 2013; 65: 162-174 [PMID: 23792277 DOI: 10.1016/j.freeradbiomed.2013.06.020]
45. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 2006; 38: 317-332 [PMID: 16290097 DOI: 10.1016/j.biocel.2005.09.018]
46. Digaleh H, Kiaei M, Khodagholi F. Nrf2 and Nrf1 signaling and ER stress crosstalk: implication for proteasomal degradation and autophagy. Cell Mol Life Sci 2013; 70: 4681-4694 [PMID: 23800989 DOI: 10.1007/s00018-013-1409-y]
47. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007; 47: 89-116 [PMID: 16968214 DOI: 10.1146/annurev.pharmtox.46.120604.141046]
48. Kwak M, Wakabayashi N, Greenlaw JL, Yamamoto M, Kensler TW. Antioxidants Enhance Mammalian Proteasome Expression through the Keap1-Nrf2 Signaling Pathway. Mol Cell Biol 2003; 23: 8786-8794 [PMID: 14612418 DOI: 10.1128/MCB.23.23.8786-8794.2003]
49. Kwak MK, Kensler TW. Induction of 26S proteasome subunit PSMB5 by the bifunctional inducer 3-methylcholanthrene through the Nrf2-ARE, but not the AhR/Arnt-XRE, pathway. Biochem Biophys Res Commun 2006; 345: 1350-1357 [PMID: 16723119 DOI: 10.1016/j.bbrc.2006.05.043]
50. Kensler TW, Wakabayashi N. Nrf2: friend or foe for chemoprevention? Carcinogenesis 2010; 31: 90-99 [PMID: 19793802 DOI: 10.1093/carcin/bgp231]
51. Riley BE, Kaiser SE, Kopito RR. Autophagy inhibition engages Nrf2-p62 Ub-associated signaling. Autophagy 2011; 7: 338-340 [PMID: 21252622 DOI: 10.4161/auto.7.3.14780]
52. Ichimura Y, Waguri S, Sou YS, Kageyama S, Hasegawa J, Ishimura R, Saito T, Yang Y, Kouno T, Fukutomi T, Hoshii T, Hirao A, Takagi K, Mizushima T, Motohashi H, Lee MS, Yoshimori T, Tanaka K, Yamamoto M, Komatsu M. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell 2013; 51: 618-631 [PMID: 24011591 DOI: 10.1016/j.molcel.2013.08.003]
53. Simmonds P. Genetic diversity and evolution of hepatitis C virus - 15 years on. J Gen Virol 2004; 85: 3173-3188 [PMID: 15483230 DOI: 10.1099/vir.0.80401-0]
54. Lindenbach BD, Rice CM. The ins and outs of hepatitis C virus entry and assembly. Nat Rev Microbiol 2013; 11: 688-700 [PMID: 24018384 DOI: 10.1038/nrmicro3098]
55. Pietschmann T, Lohmann V, Rutter G, Kurpanek K, Bartenschlager R. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J Virol 2001; 75: 1252-1264 [PMID: 11152498 DOI: 10.1128/JVI.75.3.1252-1264.2001]
56. André P, Perlemuter G, Budkowska A, Bréchot C, Lotteau V. Hepatitis C virus particles and lipoprotein metabolism. Semin Liver Dis 2005; 25: 93-104 [PMID: 15732001 DOI: 10.1055/s-2005-864785]
57. Andre P, Komurian-Pradel F, Deforges S, Perret M, Berland JL, 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 [PMID: 12072493 DOI: 10.1128/JVI.76.14.6919-6928.2002]
58. Lindenbach BD, Meuleman P, Ploss A, Vanwolleghem T, Syder AJ, McKeating JA, Lanford RE, Feinstone SM, Major ME, Leroux-Roels G, Rice CM. Cell culture-grown hepatitis C virus is infectious in vivo and can be recultured in vitro. Proc Natl Acad Sci USA 2006; 103: 3805-3809 [PMID: 16484368 DOI: 10.1073/pnas.0511218103]
59. Lindenbach BD, Evans MJ, Syder AJ, Wölk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. Complete replication of hepatitis C virus in cell culture. Science 2005; 309: 623-626 [PMID: 15947137 DOI: 10.1126/science.1114016]
60. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, Wieland SF, Uprichard SL, Wakita T, Chisari FV. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 2005; 102: 9294-9299 [PMID: 15939869 DOI: 10.1073/pnas.0503596102]
61. Gastaminza P, Dryden KA, Boyd B, Wood MR, Law M, Yeager M, Chisari FV. Ultrastructural and biophysical characterization of hepatitis C virus particles produced in cell culture. J Virol 2010; 84: 10999-11009 [PMID: 20686033 DOI: 10.1128/JVI.00526-10]
62. Chang KS, 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 [PMID: 17913825 DOI: 10.1128/JVI.01091-07]
63. Bradley D, McCaustland K, Krawczynski K, Spelbring J, Humphrey C, Cook EH. Hepatitis C virus: buoyant density of the factor VIII-derived isolate in sucrose. J Med Virol 1991; 34: 206-208 [PMID: 1655970]
64. Hijikata M, Shimizu YK, Kato H, Iwamoto A, Shih JW, Alter HJ, Purcell RH, Yoshikura H. Equilibrium centrifugation studies of hepatitis C virus: evidence for circulating immune complexes. J Virol 1993; 67: 1953-1958 [PMID: 8383220]
65. Agnello V, Abel G, Elfahal M, Knight GB, Zhang QX. Hepatitis C virus and other flaviviridae viruses enter cells via low density lipoprotein receptor. Proc Natl Acad Sci USA 1999; 96: 12766-12771 [PMID: 10535997]
66. Germi R, Crance JM, Garin D, Guimet J, Lortat-Jacob H, Ruigrok RW, Zarski JP, Drouet E. Cellular glycosaminoglycans and low density lipoprotein receptor are involved in hepatitis C virus adsorption. J Med Virol 2002; 68: 206-215 [PMID: 12210409 DOI: 10.1002/jmv.10196]
67. Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, Kinoshita-Toyoda A, Toida T, Van Kuppevelt TH, Depla E, Von Weizsacker F, Blum HE, Baumert TF. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 2003; 278: 41003-41012 [PMID: 12867431 DOI: 10.1074/jbc.M302267200]
68. Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G, Traboni C, Nicosia A, Cortese R, Vitelli A. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 2002; 21: 5017-5025 [PMID: 12356718]
69. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S. Binding of hepatitis C virus to CD81. Science 1998; 282: 938-941 [PMID: 9794763 DOI: 10.1126/science.282.5390.938]
70. Bertaux C, Dragic T, Bertaux C, Dragic T. Different domains of CD81 mediate distinct stages of hepatitis C virus pseudoparticle entry. J Virol 2006; 80: 4940-4988 [PMID: 16641285 DOI: 10.1128/JVI.80.10.4940-4948.2006]
71. Shi Q, Jiang J, Luo G. Syndecan-1 serves as the major receptor for attachment of hepatitis C virus to the surfaces of hepatocytes. J Virol 2013; 87: 6866-6875 [PMID: 23576506 DOI: 10.1128/JVI.03475-12]
72. Lefèvre M, Felmlee DJ, Parnot M, Baumert TF, Schuster C. Syndecan 4 is involved in mediating HCV entry through interaction with lipoviral particle-associated apolipoprotein E. PLoS One 2014; 9: e95550 [PMID: 24751902 DOI: 10.1371/journal.pone.0095550]
73. Xu Y, Martinez P, Séron K, Luo G, Allain F, Dubuisson J, Belouzard S. Characterization of hepatitis C virus interaction with heparan sulfate proteoglycans. J Virol 2015; 89: 3846-3858 [PMID: 25609801 DOI: 10.1128/JVI.03647-14]
74. Jiang J, Cun W, Wu X, Shi Q, Tang H, Luo G. Hepatitis C virus attachment mediated by apolipoprotein E binding to cell surface heparan sulfate. J Virol 2012; 86: 7256-7267 [PMID: 22532692 DOI: 10.1128/JVI.07222-11]
75. Khan AG, Whidby J, Miller MT, Scarborough H, Zatorski AV, Cygan A, Price AA, Yost SA, Bohannon CD, Jacob J, Grakoui A, Marcotrigiano J. Structure of the core ectodomain of the hepatitis C virus envelope glycoprotein 2. Nature 2014; 509: 381-384 [PMID: 24553139 DOI: 10.1038/nature13117]
76. Lavie M, Sarrazin S, Montserret R, Descamps V, Baumert TF, Duverlie G, Séron K, Penin F, Dubuisson J. Identification of conserved residues in hepatitis C virus envelope glycoprotein E2 that modulate virus dependence on CD81 and SRB1 entry factors. J Virol 2014; 88: 10584-10597 [PMID: 24990994 DOI: 10.1128/JVI.01402-14]
77. Douam F, Lavillette D, Cosset FL. The mechanism of HCV entry into host cells. Prog Mol Biol Transl Sci 2015; 129: 63-107 [PMID: 25595801 DOI: 10.1016/bs.pmbts.2014.10.003]
78. Evans MJ, von Hahn T, Tscherne DM, Syder AJ, Panis M, Wölk B, Hatziioannou T, McKeating JA, Bieniasz PD, Rice CM. Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 2007; 446: 801-805 [PMID: 17325668 DOI: 10.1038/nature05654]
79. Liu S, Yang W, Shen L, Turner JR, Coyne CB, Wang T. Tight junction proteins claudin-1 and occludin control hepatitis C virus entry and are downregulated during infection to prevent superinfection. J Virol 2009; 83: 2011-2014 [PMID: 19052094 DOI: 10.1128/JVI.01888-08]
80. Dorner M, Horwitz JA, Robbins JB, Barry WT, Feng Q, Mu K, Jones CT, Schoggins JW, Catanese MT, Burton DR, Law M, Rice CM, Ploss A. A genetically humanized mouse model for hepatitis C virus infection. Nature 2011; 474: 208-211 [PMID: 21654804 DOI: 10.1038/nature10168]
81. Dorner M, Horwitz JA, Donovan BM, Labitt RN, Budell WC, Friling T, Vogt A, Catanese MT, Satoh T, Kawai T, Akira S, Law M, Rice CM, Ploss A. Completion of the entire hepatitis C virus life cycle in genetically humanized mice. Nature 2013; 501: 237-241 [PMID: 23903655 DOI: 10.1038/nature12427]
82. 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 [PMID: 16809302 DOI: 10.1128/JVI.00024-06]
83. 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 [PMID: 17005647 DOI: 10.1128/JVI.01717-06]
84. Koutsoudakis G, Kaul A, Steinmann E, Kallis S, Lohmann V, Pietschmann T, Bartenschlager R. Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 2006; 80: 5308-5320 [PMID: 16699011 DOI: 10.1128/JVI.02460-05]
85. Lupberger J, Zeisel MB, Xiao F, Thumann C, Fofana I, Zona L, Davis C, Mee CJ, Turek M, Gorke S, Royer C, Fischer B, Zahid MN, Lavillette D, Fresquet J, Cosset FL, Rothenberg SM, Pietschmann T, Patel AH, Pessaux P, Doffoël M, Raffelsberger W, Poch O, McKeating JA, Brino L, Baumert TF. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 2011; 17: 589-595 [PMID: 21516087 DOI: 10.1038/nm.2341]
86. Zona L, Lupberger J, Sidahmed-Adrar N, Thumann C, Harris HJ, Barnes A, Florentin J, Tawar RG, Xiao F, Turek M, Durand SC, Duong FH, Heim MH, Cosset FL, Hirsch I, Samuel D, Brino L, Zeisel MB, Le Naour F, McKeating JA, Baumert TF. HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe 2013; 13: 302-313 [PMID: 23498955 DOI: 10.1016/j.chom.2013.02.006]
87. Sainz B, Barretto N, Martin DN, Hiraga N, Imamura M, Hussain S, Marsh KA, Yu X, Chayama K, Alrefai WA, Uprichard SL. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat Med 2012; 18: 281-285 [PMID: 22231557 DOI: 10.1038/nm.2581]
88. Martin DN, Uprichard SL. Identification of transferrin receptor 1 as a hepatitis C virus entry factor. Proc Natl Acad Sci USA 2013; 110: 10777-10782 [PMID: 23754414 DOI: 10.1073/pnas.1301764110]
89. Moradpour D, Penin F, Rice CM. Replication of hepatitis C virus. Nat Rev Microbiol 2007; 5: 453-463 [PMID: 17487147 DOI: 10.1038/nrmicro1645]
90. Romero-Brey I, Merz A, Chiramel A, Lee JY, Chlanda P, Haselman U, Santarella-Mellwig R, Habermann A, Hoppe S, Kallis S, Walther P, Antony C, Krijnse-Locker J, Bartenschlager R. Three-dimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication. PLoS Pathog 2012; 8: e1003056 [PMID: 23236278 DOI: 10.1371/journal.ppat.1003056]
91. Ferraris P, Blanchard E, Roingeard P. Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes. J Gen Virol 2010; 91: 2230-2237 [PMID: 20484561 DOI: 10.1099/vir.0.022186-0]
92. Paul D, Hoppe S, Saher G, Krijnse-Locker J, Bartenschlager R. Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment. J Virol 2013; 87: 10612-10627 [PMID: 23885072 DOI: 10.1128/JVI.01370-13]
93. Egger D, Wölk B, Gosert R, Bianchi L, Blum HE, 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 [PMID: 12021330 DOI: 10.1128/JVI.76.12.5974-5984.2002]
94. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P, Kaderali L, Poenisch M, Blankenburg H, Hiet MS, Longerich T, Diehl S, Ramirez F, Balla T, Rohr K, Kaul A, Bühler S, Pepperkok R, Lengauer T, Albrecht M, Eils R, Schirmacher P, Lohmann V, Bartenschlager R. Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 2011; 9: 32-45 [PMID: 21238945 DOI: 10.1016/j.chom.2010.12.002]
95. Li H, Yang X, Yang G, Hong Z, Zhou L, Yin P, Xiao Y, Chen L, Chung RT, Zhang L. Hepatitis C virus NS5A hijacks ARFGAP1 to maintain a phosphatidylinositol 4-phosphate-enriched microenvironment. J Virol 2014; 88: 5956-5966 [PMID: 24623438 DOI: 10.1128/JVI.03738-13]
96. Park CY, Jun HJ, Wakita T, Cheong JH, Hwang SB. Hepatitis C virus nonstructural 4B protein modulates sterol regulatory element-binding protein signaling via the AKT pathway. J Biol Chem 2009; 284: 9237-9246 [PMID: 19204002 DOI: 10.1074/jbc.M808773200]
97. Lesburg CA, Cable MB, Ferrari E, Hong Z, Mannarino AF, Weber PC. Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site. Nat Struct Biol 1999; 6: 937-943 [PMID: 10504728 DOI: 10.1038/13305]
98. Appleby TC, Perry JK, Murakami E, Barauskas O, Feng J, Cho A, Fox D, Wetmore DR, McGrath ME, Ray AS, Sofia MJ, Swaminathan S, Edwards TE. Viral replication. Structural basis for RNA replication by the hepatitis C virus polymerase. Science 2015; 347: 771-775 [PMID: 25678663 DOI: 10.1126/science.1259210]
99. Lohmann V. Hepatitis C virus RNA replication. Curr Top Microbiol Immunol 2013; 369: 167-198 [PMID: 23463201 DOI: 10.1007/978-3-642-27340-7-7]
100. Roberts AP, Lewis AP, Jopling CL. miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res 2011; 39: 7716-7729 [PMID: 21653556 DOI: 10.1093/nar/gkr426]
101. Hu J, Xu Y, Hao J, Wang S, Li C, Meng S. MiR-122 in hepatic function and liver diseases. Protein Cell 2012; 3: 364-371 [PMID: 22610888 DOI: 10.1007/s13238-012-2036-3]
102. Fischer G, Aumüller T. Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes. Rev Physiol Biochem Pharmacol 2003; 148: 105-150 [PMID: 12698322 DOI: 10.1007/s10254-003-0011-3]
103. Yang F, Robotham JM, Nelson HB, Irsigler A, Kenworthy R, Tang H. Cyclophilin A is an essential cofactor for hepatitis C virus infection and the principal mediator of cyclosporine resistance in vitro. J Virol 2008; 82: 5269-5278 [PMID: 18385230 DOI: 10.1128/JVI.02614-07]
104. Watashi K, Hijikata M, Hosaka M, Yamaji M, Shimotohno K. Cyclosporin A suppresses replication of hepatitis C virus genome in cultured hepatocytes. Hepatology 2003; 38: 1282-1288 [PMID: 14578868 DOI: 10.1053/jhep.2003.50449]
105. Chatterji U, Bobardt M, Tai A, Wood M, Gallay PA. Cyclophilin and NS5A inhibitors, but not other anti-hepatitis C virus (HCV) agents, preclude HCV-mediated formation of double-membrane-vesicle viral factories. Antimicrob Agents Chemother 2015; 59: 2496-2507 [PMID: 25666154 DOI: 10.1128/AAC.04958-14]
106. 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 [PMID: 17721513 DOI: 10.1038/ncb1631]
107. Huang H, Sun F, Owen DM, Li W, Chen Y, Gale M, Ye J. Hepatitis C virus production by human hepatocytes dependent on assembly and secretion of very low-density lipoproteins. Proc Natl Acad Sci USA 2007; 104: 5848-5853 [PMID: 17376867 DOI: 10.1073/pnas.0700760104]
108. Bickel PE, Tansey JT, Welte MA. PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta 2009; 1791: 419-440 [PMID: 19375517 DOI: 10.1016/j.bbalip.2009.04.002]
109. Boulant S, Douglas MW, Moody L, Budkowska A, Targett-Adams P, McLauchlan J. Hepatitis C virus core protein induces lipid droplet redistribution in a microtubule- and dynein-dependent manner. Traffic 2008; 9: 1268-1282 [PMID: 18489704 DOI: 10.1111/j.1600-0854.2008.00767.x]
110. Camus G, Herker E, Modi AA, Haas JT, Ramage HR, Farese RV, Ott M. Diacylglycerol acyltransferase-1 localizes hepatitis C virus NS5A protein to lipid droplets and enhances NS5A interaction with the viral capsid core. J Biol Chem 2013; 288: 9915-9923 [PMID: 23420847 DOI: 10.1074/jbc.M112.434910]
111. 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 [PMID: 17942391 DOI: 10.1074/jbc.M707329200]
112. Menzel N, Fischl W, Hueging K, Bankwitz D, Frentzen A, Haid S, Gentzsch J, Kaderali L, Bartenschlager R, Pietschmann T. MAP-kinase regulated cytosolic phospholipase A2 activity is essential for production of infectious hepatitis C virus particles. PLoS Pathog 2012; 8: e1002829 [PMID: 22911431 DOI: 10.1371/journal.ppat.1002829]
113. Salloum S, Wang H, Ferguson C, Parton RG, Tai AW. Rab18 binds to hepatitis C virus NS5A and promotes interaction between sites of viral replication and lipid droplets. PLoS Pathog 2013; 9: e1003513 [PMID: 23935497 DOI: 10.1371/journal.ppat.1003513]
114. Sato S, Fukasawa M, Yamakawa Y, Natsume T, Suzuki T, Shoji I, Aizaki H, Miyamura T, Nishijima M. Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein. J Biochem 2006; 139: 921-930 [PMID: 16751600 DOI: 10.1093/jb/mvj104]
115. Bulankina AV, Deggerich A, Wenzel D, Mutenda K, Wittmann JG, Rudolph MG, Burger KN, Höning S. TIP47 functions in the biogenesis of lipid droplets. J Cell Biol 2009; 185: 641-655 [PMID: 19451273 DOI: 10.1083/jcb.200812042]
116. Díaz E, Pfeffer SR. TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 1998; 93: 433-443 [PMID: 9590177]
117. Hickenbottom SJ, Kimmel AR, Londos C, Hurley JH. Structure of a lipid droplet protein; the PAT family member TIP47. Structure 2004; 12: 1199-1207 [PMID: 15242596 DOI: 10.1016/j.str.2004.04.021]
118. Benga WJ, Krieger SE, Dimitrova M, Zeisel MB, Parnot M, Lupberger J, Hildt E, Luo G, McLauchlan J, Baumert TF, Schuster C. Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles. Hepatology 2010; 51: 43-53 [PMID: 20014138 DOI: 10.1002/hep.23278]
119. Cun W, Jiang J, Luo G. The C-terminal alpha-helix domain of apolipoprotein E is required for interaction with nonstructural protein 5A and assembly of hepatitis C virus. J Virol 2010; 84: 11532-11541 [PMID: 20719944 DOI: 10.1128/JVI.01021-10]
120. Jiang J, Luo G. Apolipoprotein E but not B is required for the formation of infectious hepatitis C virus particles. J Virol 2009; 83: 12680-12691 [PMID: 19793818 DOI: 10.1128/JVI.01476-09]
121. Ploen D, Hafirassou ML, Himmelsbach K, Sauter D, Biniossek ML, Weiss TS, Baumert TF, Schuster C, Hildt E. TIP47 plays a crucial role in the life cycle of hepatitis C virus. J Hepatol 2013; 58: 1081-1088 [PMID: 23354285 DOI: 10.1016/j.jhep.2013.01.022]
122. Vogt DA, Camus G, Herker E, Webster BR, Tsou CL, Greene WC, Yen TS, Ott M. Lipid droplet-binding protein TIP47 regulates hepatitis C Virus RNA replication through interaction with the viral NS5A protein. PLoS Pathog 2013; 9: e1003302 [PMID: 23593007 DOI: 10.1371/journal.ppat.1003302]
123. 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 [PMID: 18369481 DOI: 10.1371/journal.ppat.1000035]
124. 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 [PMID: 18524832 DOI: 10.1128/JVI.00826-08]
125. Tellinghuisen TL, Foss KL, Treadaway J. Regulation of hepatitis C virion production via phosphorylation of the NS5A protein. PLoS Pathog 2008; 4: e1000032 [PMID: 18369478 DOI: 10.1371/journal.ppat.1000032]
126. Jirasko V, Montserret R, Lee JY, Gouttenoire J, Moradpour D, Penin F, Bartenschlager R. 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 [PMID: 21187906 DOI: 10.1371/journal.ppat.1001233]
127. Popescu CI, Callens N, Trinel D, Roingeard P, Moradpour D, Descamps V, Duverlie G, Penin F, Héliot L, Rouillé Y, Dubuisson J. NS2 protein of hepatitis C virus interacts with structural and non-structural proteins towards virus assembly. PLoS Pathog 2011; 7: e1001278 [PMID: 21347350 DOI: 10.1371/journal.ppat.1001278]
128. Ariumi Y, Kuroki M, Maki M, Ikeda M, Dansako H, Wakita T, Kato N. The ESCRT system is required for hepatitis C virus production. PLoS One 2011; 6: e14517 [PMID: 21264300 DOI: 10.1371/journal.pone.0014517]
129. Corless L, Crump CM, Griffin SD, Harris M. Vps4 and the ESCRT-III complex are required for the release of infectious hepatitis C virus particles. J Gen Virol 2010; 91: 362-372 [PMID: 19828764 DOI: 10.1099/vir.0.017285-0]
130. Bartenschlager R, Penin F, Lohmann V, André P. Assembly of infectious hepatitis C virus particles. Trends Microbiol 2011; 19: 95-103 [PMID: 21146993 DOI: 10.1016/j.tim.2010.11.005]
131. Coller KE, Heaton NS, Berger KL, Cooper JD, Saunders JL, Randall G. Molecular determinants and dynamics of hepatitis C virus secretion. PLoS Pathog 2012; 8: e1002466 [PMID: 22241992 DOI: 10.1371/journal.ppat.1002466]
132. Vieyres G, Thomas X, Descamps V, Duverlie G, Patel AH, Dubuisson J. Characterization of the envelope glycoproteins associated with infectious hepatitis C virus. J Virol 2010; 84: 10159-10168 [PMID: 20668082 DOI: 10.1128/JVI.01180-10]
133. Counihan NA, Rawlinson SM, Lindenbach BD. Trafficking of hepatitis C virus core protein during virus particle assembly. PLoS Pathog 2011; 7: e1002302 [PMID: 22028650 DOI: 10.1371/journal.ppat.1002302]
134. Ploen D, Hafirassou ML, Himmelsbach K, Schille SA, Biniossek ML, Baumert TF, Schuster C, Hildt E. TIP47 is associated with the hepatitis C virus and its interaction with Rab9 is required for release of viral particles. Eur J Cell Biol 2013; 92: 374-382 [PMID: 24480419 DOI: 10.1016/j.ejcb.2013.12.003]
135. Poenisch M, Metz P, Blankenburg H, Ruggieri A, Lee JY, Rupp D, Rebhan I, Diederich K, Kaderali L, Domingues FS, Albrecht M, Lohmann V, Erfle H, Bartenschlager R. Identification of HNRNPK as regulator of hepatitis C virus particle production. PLoS Pathog 2015; 11: e1004573 [PMID: 25569684 DOI: 10.1371/journal.ppat.1004573]
136. Tardif KD, Mori K, Siddiqui A. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J Virol 2002; 76: 7453-7459 [PMID: 12097557 DOI: 10.1128/JVI.76.15.7453-7459.2002]
137. Ke PY, Chen SS. Autophagy: a novel guardian of HCV against innate immune response. Autophagy 2011; 7: 533-535 [PMID: 21242722 DOI: 10.4161/auto.7.5.14732]
138. Asselah T, Bièche I, Mansouri A, Laurendeau I, Cazals-Hatem D, Feldmann G, Bedossa P, Paradis V, Martinot-Peignoux M, Lebrec D, Guichard C, Ogier-Denis E, Vidaud M, Tellier Z, Soumelis V, Marcellin P, Moreau R. In vivo hepatic endoplasmic reticulum stress in patients with chronic hepatitis C. J Pathol 2010; 221: 264-274 [PMID: 20527020 DOI: 10.1002/path.2703]
139. Cocquerel L, Meunier JC, 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 [PMID: 9499075]
140. Choukhi A, Ung S, Wychowski C, Dubuisson J. Involvement of endoplasmic reticulum chaperones in the folding of hepatitis C virus glycoproteins. J Virol 1998; 72: 3851-3858 [PMID: 9557669]
141. Bartosch B, Thimme R, Blum HE, Zoulim F. Hepatitis C virus-induced hepatocarcinogenesis. J Hepatol 2009; 51: 810-820 [PMID: 19545926 DOI: 10.1016/j.jhep.2009.05.008]
142. Carvajal-Yepes M, Himmelsbach K, Schaedler S, Ploen D, Krause J, Ludwig L, Weiss T, Klingel K, Hildt E. Hepatitis C virus impairs the induction of cytoprotective Nrf2 target genes by delocalization of small Maf proteins. J Biol Chem 2011; 286: 8941-8951 [PMID: 21216956 DOI: 10.1074/jbc.M110.186684]
143. Beyer TA, Xu W, Teupser D, auf dem Keller U, Bugnon P, Hildt E, Thiery J, Kan YW, Werner S. Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance. EMBO J 2008; 27: 212-223 [PMID: 18059474 DOI: 10.1038/sj.emboj.7601950]
144. Li S, Ye L, Yu X, Xu B, Li K, Zhu X, Liu H, Wu X, Kong L. Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 2009; 391: 257-264 [PMID: 19628242 DOI: 10.1016/j.virol.2009.06.039]
145. Li L, Kim E, Yuan H, Inoki K, Goraksha-Hicks P, Schiesher RL, Neufeld TP, Guan KL. Regulation of mTORC1 by the Rab and Arf GTPases. J Biol Chem 2010; 285: 19705-19709 [PMID: 20457610 DOI: 10.1074/jbc.C110.102483]
146. Simonsen A, Tooze SA. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 2009; 186: 773-782 [PMID: 19797076 DOI: 10.1083/jcb.200907014]
147. Stone M, Jia S, Heo WD, Meyer T, Konan KV. Participation of rab5, an early endosome protein, in hepatitis C virus RNA replication machinery. J Virol 2007; 81: 4551-4563 [PMID: 17301141 DOI: 10.1128/JVI.01366-06]
148. Grégoire IP, Rabourdin-Combe C, Faure M. Autophagy and RNA virus interactomes reveal IRGM as a common target. Autophagy 2012; 8: 1136-1137 [PMID: 22722598 DOI: 10.4161/auto.20339]
149. Vescovo T, Refolo G, Romagnoli A, Ciccosanti F, Corazzari M, Alonzi T, Fimia GM. Autophagy in HCV infection: keeping fat and inflammation at bay. Biomed Res Int 2014; 2014: 265353 [PMID: 25162004 DOI: 10.1155/2014/265353]
150. Romero-Brey I, Bartenschlager R. Membranous replication factories induced by plus-strand RNA viruses. Viruses 2014; 6: 2826-2857 [PMID: 25054883 DOI: 10.3390/v6072826]
151. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol 2001; 152: 657-668 [PMID: 11266458]
152. Guévin C, Manna D, Bélanger C, Konan KV, Mak P, Labonté P. Autophagy protein ATG5 interacts transiently with the hepatitis C virus RNA polymerase (NS5B) early during infection. Virology 2010; 405: 1-7 [PMID: 20580051 DOI: 10.1016/j.virol.2010.05.032]
153. Dreux M, Chisari FV. Autophagy proteins promote hepatitis C virus replication. Autophagy 2009; 5: 1224-1225 [PMID: 19844160]
154. Dreux M, Chisari FV. Impact of the autophagy machinery on hepatitis C virus infection. Viruses 2011; 3: 1342-1357 [PMID: 21994783 DOI: 10.3390/v3081342]
155. Taguwa S, Kambara H, Fujita N, Noda T, Yoshimori T, Koike K, Moriishi K, Matsuura Y. Dysfunction of autophagy participates in vacuole formation and cell death in cells replicating hepatitis C virus. J Virol 2011; 85: 13185-13194 [PMID: 21994453 DOI: 10.1128/JVI.06099-11]
156. Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe 2009; 5: 527-549 [PMID: 19527881 DOI: 10.1016/j.chom.2009.05.016]
157. Orvedahl A, Levine B. Eating the enemy within: autophagy in infectious diseases. Cell Death Differ 2009; 16: 57-69 [PMID: 18772897 DOI: 10.1038/cdd.2008.130]
158. Chiramel AI, Brady NR, Bartenschlager R. Divergent roles of autophagy in virus infection. Cells 2013; 2: 83-104 [PMID: 24709646 DOI: 10.3390/cells2010083]
159. Delgado MA, Deretic V. Toll-like receptors in control of immunological autophagy. Cell Death Differ 2009; 16: 976-983 [PMID: 19444282 DOI: 10.1038/cdd.2009.40]
160. Into T, Inomata M, Takayama E, Takigawa T. Autophagy in regulation of Toll-like receptor signaling. Cell Signal 2012; 24: 1150-1162 [PMID: 22333395 DOI: 10.1016/j.cellsig.2012.01.020]
161. Münz C. Antigen processing by macroautophagy for MHC presentation. Front Immunol 2011; 2: 42 [PMID: 22566832 DOI: 10.3389/fimmu.2011.00042]
162. Katze MG, Fornek JL, Palermo RE, Walters KA, Korth MJ. Innate immune modulation by RNA viruses: emerging insights from functional genomics. Nat Rev Immunol 2008; 8: 644-654 [PMID: 18654572 DOI: 10.1038/nri2377]
163. Kawai T, Akira S. Innate immune recognition of viral infection. Nat Immunol 2006; 7: 131-137 [PMID: 16424890 DOI: 10.1038/ni1303]
164. Alisi A, Mele R, Spaziani A, Tavolaro S, Palescandolo E, Balsano C. Thr 446 phosphorylation of PKR by HCV core protein deregulates G2/M phase in HCC cells. J Cell Physiol 2005; 205: 25-31 [PMID: 15880455 DOI: 10.1002/jcp.20363]
165. Dansako H, Naganuma A, Nakamura T, Ikeda F, Nozaki A, Kato N. Differential activation of interferon-inducible genes by hepatitis C virus core protein mediated by the interferon stimulated response element. Virus Res 2003; 97: 17-30 [PMID: 14550584]
166. Delhem N, Sabile A, Gajardo R, Podevin P, Abadie A, Blaton MA, Kremsdorf D, Beretta L, Brechot C. Activation of the interferon-inducible protein kinase PKR by hepatocellular carcinoma derived-hepatitis C virus core protein. Oncogene 2001; 20: 5836-5845 [PMID: 11593389 DOI: 10.1038/sj.onc.1204744]
167. Gale MJ, Korth MJ, Tang NM, Tan SL, Hopkins DA, Dever TE, Polyak SJ, Gretch DR, Katze MG. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 1997; 230: 217-227 [PMID: 9143277 DOI: 10.1006/viro.1997.8493]
168. Gale M, Blakely CM, Kwieciszewski B, Tan SL, Dossett M, Tang NM, Korth MJ, Polyak SJ, Gretch DR, Katze MG. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol Cell Biol 1998; 18: 5208-5218 [PMID: 9710605]
169. François C, Duverlie G, Rebouillat D, Khorsi H, Castelain S, Blum HE, Gatignol A, Wychowski C, Moradpour D, Meurs EF. Expression of hepatitis C virus proteins interferes with the antiviral action of interferon independently of PKR-mediated control of protein synthesis. J Virol 2000; 74: 5587-5596 [PMID: 10823866]
170. Pavio N, Taylor DR, Lai MM. Detection of a Novel Unglycosylated Form of Hepatitis C Virus E2 Envelope Protein That Is Located in the Cytosol and Interacts with PKR. J Virol 2002; 76: 1265-1272 [PMID: 11773402 DOI: 10.1128/JVI.76.3.1265-1272.2002]
171. Pavio N, Romano PR, Graczyk TM, Feinstone SM, Taylor DR. Protein Synthesis and Endoplasmic Reticulum Stress Can Be Modulated by the Hepatitis C Virus Envelope Protein E2 through the Eukaryotic Initiation Factor 2 Kinase PERK. J Virol 2003; 77: 3578-3585 [PMID: 12610133 DOI: 10.1128/JVI.77.6.3578-3585.2003]
172. Garaigorta U, Chisari FV. Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation. Cell Host Microbe 2009; 6: 513-522 [PMID: 20006840 DOI: 10.1016/j.chom.2009.11.004]
173. Lee HK, Iwasaki A. Autophagy and antiviral immunity. Curr Opin Immunol 2008; 20: 23-29 [PMID: 18262399 DOI: 10.1016/j.coi.2008.01.001]
174. Dabo S, Meurs EF. dsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection. Viruses 2012; 4: 2598-2635 [PMID: 23202496 DOI: 10.3390/v4112598]
175. Chandra PK, Bao L, Song K, Aboulnasr FM, Baker DP, Shores N, Wimley WC, Liu S, Hagedorn CH, Fuchs SY, Wu T, Balart LA, Dash S. HCV infection selectively impairs type I but not type III IFN signaling. Am J Pathol 2014; 184: 214-229 [PMID: 24215913 DOI: 10.1016/j.ajpath.2013.10.005]