HCV and Oxidative Stress: Implications for HCV Life Cycle and HCV-Associated Pathogenesis

Oxidative Medicine and Cellular Longevity

Volumn 2016, Issue , 2016, Pages

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

^a PAUL EHRLICH INSTITUT   (Germany)

^b Deutsches Zentrum für Infektions forschung DZIF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUSES;

CAUSATIVE AGENTS; CHRONIC LIVER DISEASE; HEPATITIS C VIRUS; HEPATOCELLULAR CARCINOMA; LIVER REGENERATION; MULTIFACTORIAL PROCESS; REACTIVE OXYGEN SPECIES; VIRAL LIFE CYCLE;

LIFE CYCLE;

KELCH LIKE ECH ASSOCIATED PROTEIN 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TRANSCRIPTION FACTOR NRF2;

AUTOPHAGY; ENDOPLASMIC RETICULUM STRESS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; INSULIN RESISTANCE; LIFE CYCLE; LIVER REGENERATION; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; VIRUS REPLICATION; ANIMAL; CHRONIC HEPATITIS C; HEPACIVIRUS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; VIRUS REPLICATION;

EID: 84959431882     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2016/9012580     Document Type: Review

References (181)

1. D. Lavanchy, "The global burden of hepatitis C," Liver International, vol. 29, supplement 1, pp. 74-81, 2009.
2. R. Bartenschlager, F. Penin, V. Lohmann, and P. André, "Assembly of infectious hepatitis C virus particles," Trends in Microbiology, vol. 19, no. 2, pp. 95-103, 2011.
3. V. Madan and R. Bartenschlager, "Structural and functional properties of the hepatitis C virus p7 viroporin," Viruses, vol. 7, no. 8, pp. 4461-4481, 2015.
4. R. Bartenschlager and V. Lohmann, "Novel cell culture systems for the hepatitis C virus," Antiviral Research, vol. 52, no. 1, pp. 1-17, 2001.
5. D. Moradpour, R. Gosert, D. Egger, F. Penin, H. E. Blum, and K. Bienz, "Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex," Antiviral Research, vol. 60, no. 2, pp. 103-109, 2003.
6. D. Moradpour, F. Penin, and C. M. Rice, "Replication of hepatitis C virus," Nature ReviewsMicrobiology, vol. 5, no. 6, pp. 453-463, 2007.
7. D. Moradpour, V. Brass, E. Bieck et al., "Membrane association of the RNA-dependent RNA polymerase is essential for hepatitis C virus RNA replication," Journal of Virology, vol. 78, no. 23, pp. 13278-13284, 2004.
8. D. Paul, V. Madan, and R. Bartenschlager, "Hepatitis C virus RNA replication and assembly: living on the fat of the land," Cell Host & Microbe, vol. 16, no. 5, pp. 569-579, 2014.
9. T. Wakita, T. Pietschmann, T. Kato et al., "Production of infectious hepatitis C virus in tissue culture from a cloned viral genome," Nature Medicine, vol. 11, no. 7, pp. 791-796, 2005.
10. J. Zhong, P. Gastaminza, G. Cheng et al., "Robust hepatitis C virus infection in vitro," Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 26, pp. 9294-9299, 2005.
11. B. D. Lindenbach, M. J. Evans, A. J. Syder et al., "Complete replication of hepatitis C virus in cell culture," Science, vol. 309, no. 5734, pp. 623-626, 2005.
12. V. Lohmann, F. Körner, J.-O. Koch, U. Herian, L. Theilmann, and R. Bartenschlager, "Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line," Science, vol. 285, no. 5424, pp. 110-113, 1999.
13. G. Alvisi, V. Madan, and R. Bartenschlager, "Hepatitis C virus and host cell lipids: An intimate connection," RNA Biology, vol. 8, no. 2, pp. 258-269, 2011.
14. J.-Y. Lee, E. G. Acosta, I. K. Stoeck et al., "Apolipoprotein E likely contributes to a maturation step of infectious hepatitis C virus particles and interacts with viral envelope glycoproteins," Journal of Virology, vol. 88, no. 21, pp. 12422-12437, 2014.
15. W. J. A. Benga, S. E. Krieger, M. Dimitrova et al., "Apolipoprotein E interacts with hepatitis C virus nonstructural protein 5A and determines assembly of infectious particles," Hepatology, vol. 51, no. 1, pp. 43-53, 2010.
16. D. Ploen, M. L. Hafirassou, K. Himmelsbach et al., "TIP47 plays a crucial role in the life cycle of hepatitis C virus," Journal of Hepatology, vol. 58, no. 6, pp. 1081-1088, 2013.
17. D. Ploen, M. L. Hafirassou, K. Himmelsbach et al., "TIP47 is associated with the Hepatitis C virus and its interaction with Rab9 is required for release of viral particles," European Journal of Cell Biology, vol. 92, no. 12, pp. 374-382, 2013.
18. N. A. Counihan, S. M. Rawlinson, and B. D. Lindenbach, "Trafficking of hepatitis C virus core protein during virus particle assembly," PLoS Pathogens, vol. 7, no. 10, Article ID e1002302, 2011.
19. A. Filipe and J. McLauchlan, "Hepatitis C virus and lipid droplets: finding a niche," Trends inMolecularMedicine, vol. 21, no. 1, pp. 34-42, 2015.
20. Y. Miyanari, K. Atsuzawa, N. Usuda et al., "The lipid droplet is an important organelle for hepatitis C virus production," Nature Cell Biology, vol. 9, no. 9, pp. 1089-1097, 2007.
21. E. Herker, C. Harris, C. Hernandez et al., "Efficient hepatitis C virus particle formation requires diacylglycerol acyltransferase-1," Nature Medicine, vol. 16, no. 11, pp. 1295-1298, 2010.
22. G. Camus, E. Herker, A. A. Modi et al., "Diacylglycerol acyltransferase-1 localizes hepatitis C virus NS5A protein to lipid droplets and enhances NS5A interaction with the viral capsid core,"The Journal of Biological Chemistry, vol. 288, no. 14, pp. 9915-9923, 2013.
23. A. V. Ivanov, B. Bartosch,O. A. Smirnova,M. G. Isaguliants, and S. N. Kochetkov, "HCVand oxidative stress in the liver," Viruses, vol. 5, no. 2, pp. 439-469, 2013.
24. M. Marra, I. M. Sordelli, A. Lombardi et al., "Molecular targets and oxidative stress biomarkers in hepatocellular carcinoma: An overview," Journal of TranslationalMedicine, vol. 9, no. 1, article 171, 2011.
25. M. L. Reshi, Y.-C. Su, and J.-R. Hong, "RNA viruses: ROSmediated cell death," International Journal of Cell Biology, vol. 2014, Article ID467452, 16 pages, 2014.
26. T. Wang and S. A. Weinman, "Interactions between hepatitis C virus and mitochondria: impact on pathogenesis and innate immunity," Current Pathobiology Reports, vol. 1, no. 3, pp. 179-187, 2013.
27. K. Hino, Y. Hara, and S. Nishina, "Mitochondrial reactive oxygen species as a mystery voice in hepatitis C," Hepatology Research, vol. 44, no. 2, pp. 123-132, 2014.
28. C. Espinosa-Diez, V. Miguel, D. Mennerich et al., "Antioxidant responses and cellular adjustments to oxidative stress," Redox Biology, vol. 6, pp. 183-197, 2015.
29. M. A. O'Connell and J. D. Hayes, "The Keap1/Nrf2 pathway in health and disease: from the bench to the clinic," Biochemical Society Transactions, vol. 43, no. 4, pp. 687-689, 2015.
30. D. V. Chartoumpekis, N. Wakabayashi, and T. W. Kensler, "Keap1/Nrf2 pathway in the frontiers of cancer and non-cancer cell metabolism," Biochemical Society Transactions, vol. 43, no. 4, pp. 639-644, 2015.
31. T. W. Kensler, N. Wakabayashi, and S. Biswal, "Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway," Annual Review of Pharmacology and Toxicology, vol. 47, pp. 89-116, 2007.
32. B. Harder, T. Jiang, T. Wu et al., "Molecularmechanisms of Nrf2 regulation and how these influence chemical modulation for disease intervention," Biochemical Society Transactions, vol. 43, no. 4, pp. 680-686, 2015.
33. T. A. Beyer, W. Xu, D. Teupser et al., "Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance,"TheEMBOJournal, vol. 27,no. 1, pp. 212-223, 2008.
34. T. A. Beyer and S. Werner, "The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver," Cell Cycle, vol. 7, no. 7, pp. 874-878, 2008.
35. E. Seki, D. A. Brenner, andM. Karin, "Aliver full of JNK: signaling in regulation of cell function and disease pathogenesis, and clinical approaches," Gastroenterology, vol. 143, no. 2, pp. 307-320, 2012.
36. S. Guo, "Insulin signaling, resistance, and metabolic syndrome: insights from mouse models into disease mechanisms," Journal of Endocrinology, vol. 220, no. 2, pp. T1-T23, 2014.
37. J. Wardyn, A. Ponsford, and C. Sanderson, "Dissecting molecular cross-talk between Nrf2 and NF-B response pathways," Biochemical Society Transactions, vol. 43, no. 4, pp. 621-626, 2015.
38. U. A. Köhler, F. Böhm, F. Rolfs et al., "NF-B/RelA and Nrf2 cooperate to maintain hepatocyte integrity and to prevent development of hepatocellular adenoma," Journal ofHepatology, vol. 64, no. 1, pp. 94-102, 2016.
39. S. Masoudi, D. Ploen, K. Kunz, and E. Hildt, "The adjuvant component -tocopherol triggers via modulation of Nrf2 the expression and turnover of hypocretin in vitro and its implication to the development of narcolepsy," Vaccine, vol. 32, no. 25, pp. 2980-2988, 2014.
40. A. V. Ivanov,O. A. Smirnova, I. Y. Petrushanko et al., "HCVcore protein uses multiple mechanisms to induce oxidative stress in human hepatoma huh7 cells," Viruses, vol. 7, no. 6, pp. 2745-2770, 2015.
41. B. Schwer, S. Ren, T. Pietschmannet al., "TargetingofhepatitisC virus core protein to mitochondria through a novel C-terminal localization motif," Journal of Virology, vol. 78, no. 15, pp. 7958-7968, 2004.
42. R. Suzuki, S. Sakamoto, T. Tsutsumi et al., "Molecular determinants for subcellular localization of hepatitis C virus core protein," Journal of Virology, vol. 79, no. 2, pp. 1271-1281, 2005.
43. M. Okuda, K. Li, M. R. Beard et al., "Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein," Gastroenterology, vol. 122, no. 2, pp. 366-375, 2002.
44. M. Korenaga, T. Wang, Y. Li et al., "Hepatitis C virus core protein inhibitsmitochondrial electron transport and increases reactive oxygen species (ROS) production," The Journal of Biological Chemistry, vol. 280, no. 45, pp. 37481-37488, 2005.
45. D. M. D'Agostino, P. Zanovello, T. Watanabe, and V. Ciminale, "The microRNA regulatory network in normal-and HTLV-1-transformed T cells," Advances in Cancer Research, vol. 113, pp. 45-83, 2012.
46. V. C. Chu, S. Bhattacharya, A. Nomoto et al., "Persistent expression of hepatitis C virus non-structural proteins leads to increased autophagy and mitochondrial injury in human hepatoma cells," PLoSONE, vol. 6, no. 12,Article IDe28551,2011.
47. S. Griffin, D. Clarke, C. McCormick, D. Rowlands, and M. Harris, "Signal peptide cleavage and internal targeting signals direct the hepatitis C virus p7 protein to distinct intracellular membranes," Journal ofVirology, vol. 79,no. 24,pp. 15525-15536, 2005.
48. Y. Rouillé, F. Helle, D. Delgrange et al., "Subcellular localization of hepatitis C virus structural proteins in a cell culture system that efficiently replicates the virus," Journal of Virology, vol. 80, no. 6, pp. 2832-2841, 2006.
49. J. Wang, B. Zhou, Q. Lai et al., "Clinical and virological characteristics of chronic hepatitis B with concurrent hepatitis B e antigen and antibody detection," Journal of Viral Hepatitis, vol. 18, no. 9, pp. 646-652, 2011.
50. X.-D. Li, L. Sun, R. B. Seth, G. Pineda, and Z. J. Chen, "Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity," Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 49, pp. 17717-17722, 2005.
51. S. M. Horner, H. S. Park, and M. Gale, "Control of innate immune signaling and membrane targeting by the hepatitis C virus NS3/4A protease are governed by the NS3 Helix 0," Journal of Virology, vol. 86, no. 6, pp. 3112-3120, 2012.
52. M. Baril, M.-E. Racine, F. Penin, and D. Lamarre, "MAVS dimer is a crucial signaling component of innate immunity and the target of hepatitis C virusNS3/4A protease," Journal of Virology, vol. 83, no. 3, pp. 1299-1311, 2009.
53. N. L. Benali-Furet,M. Chami, L. Houel et al., "Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion," Oncogene, vol. 24, no. 31, pp. 4921-4933, 2005.
54. C. Piccoli, R. Scrima, G. Quarato et al., "Hepatitis C virus protein expression causes calcium-mediated mitochondrial bioenergetic dysfunction and nitro-oxidative stress," Hepatology, vol. 46, no. 1, pp. 58-65, 2007.
55. K. D. Tardif, G. Waris, and A. Siddiqui, "Hepatitis C virus, ER stress, and oxidative stress," Trends in Microbiology, vol. 13, no. 4, pp. 159-163, 2005.
56. I. Qadri, M. Iwahashi, J. M. Capasso et al., "Induced oxidative stress and activated expression of manganese superoxide dismutase during hepatitis C virus replication: role of JNK, p38 MAPK and AP-1," Biochemical Journal, vol. 378, no. 3, pp. 919-928, 2004.
57. N. Dionisio, M. V. Garcia-Mediavilla, S. Sanchez-Campos et al., "Hepatitis C virus NS5A and core proteins induce oxidative stress-mediated calcium signalling alterations in hepatocytes," Journal of Hepatology, vol. 50, no. 5, pp. 872-882, 2009.
58. M. Carvajal-Yepes, K. Himmelsbach, S. Schaedler et al., "Hepatitis C virus impairs the induction of cytoprotectiveNrf2 target genes by delocalization of small maf proteins," The Journal of Biological Chemistry, vol. 286, no. 11, pp. 8941-8951, 2011.
59. Y. Li, D. F. Boehning, T. Qian, V. L. Popov, and S. A. Weinman, "Hepatitis C virus core protein increases mitochondrial ROS production by stimulation of Ca2+ uniporter activity," The FASEB Journal, vol. 21, no. 10, pp. 2474-2485, 2007.
60. T. Wang, R. V. Campbell, M. K. Yi, S. M. Lemon, and S. A. Weinman, "Role of Hepatitis C virus core protein in viralinduced mitochondrial dysfunction," Journal of Viral Hepatitis, vol. 17, no. 11, pp. 784-793, 2010.
61. D. P. Lindsay, A. K. Camara, D. F. Stowe, R. Lubbe, and M. Aldakkak, "Differential effects of buffer pH on Ca2+-induced ROS emission with inhibited mitochondrial complexes I and III," Frontiers in Physiology, vol. 6, article 58, 2015.
62. C. L. Quinlan, I. V. Perevoshchikova, M. Hey-Mogensen, A. L. Orr, and M. D. Brand, "Sites of reactive oxygen species generation by mitochondria oxidizing different substrates," Redox Biology, vol. 1, no. 1, pp. 304-312, 2013.
63. Y. Amako, T. Munakata, M. Kohara et al., "Hepatitis C virus attenuates mitochondrial lipid -oxidation by downregulating mitochondrial trifunctional-protein expression," Journal of Virology, vol. 89, no. 8, pp. 4092-4101, 2015.
64. J.-W. Yu, L.-J. Sun, W. Liu, Y.-H. Zhao, P. Kang, and B.-Z. Yan, "Hepatitis C virus core protein induces hepaticmetabolism disorders through down-regulation of the SIRT1-AMPK signaling pathway," International Journal of Infectious Diseases, vol. 17, no. 7, pp. e539-e545, 2013.
65. A. S. Kathiria, L. D. Butcher, L. A. Feagins, R. F. Souza, C. R. Boland, and A. L. Theiss, "Prohibitin 1modulatesmitochondrial stress-related autophagy in human colonic epithelial cells," PLoS ONE, vol. 7, no. 2,Article ID e31231, 2012.
66. T. Tsutsumi, M. Matsuda, H. Aizaki et al., "Proteomics analysis of mitochondrial proteins reveals overexpression of a mitochondrial protein chaperon, prohibitin, in cells expressing hepatitis C virus core protein," Hepatology, vol. 50, no. 2, pp. 378-386, 2009.
67. S.-S. Dang, M.-Z. Sun, E. Yang et al., "Prohibitin is overexpressed in Huh-7-HCV and Huh-7. 5-HCV cells harboring in vitro transcribed full-length hepatitis C virus RNA," Virology Journal, vol. 8, article 424, 2011.
68. Y.-H. Paik, J. Kim, T. Aoyama, S. De Minicis, R. Bataller, and D. A. Brenner, "Role of NADPH oxidases in liver fibrosis," Antioxidants and Redox Signaling, vol. 20, no. 17, pp. 2854-2872, 2014.
69. K. Bedard and K.-H. Krause, "The NOX family of ROSgeneratingNADPHoxidases: physiology and pathophysiology," Physiological Reviews, vol. 87, no. 1, pp. 245-313, 2007.
70. M. Geiszt, J. B. Kopp, P. Várnai, and T. L. Leto, "Identification of Renox, an NAD(P)H oxidase in kidney," Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 14, pp. 8010-8014, 2000.
71. N. S. R. deMochel, S. Seronello, S. H. Wang et al., "Hepatocyte NAD(P)Hoxidases as an endogenous source of reactive oxygen species during hepatitis C virus infection," Hepatology, vol. 52, no. 1, pp. 47-59, 2010.
72. H. E. Boudreau, S. U. Emerson, A. Korzeniowska, M. A. Jendrysik, and T. L. Leto, "Hepatitis C virus (HCV) proteins induce NADPH oxidase 4 expression in a transforming growth factor -dependent manner: A newcontributor toHCVinduced oxidative stress," Journal of Virology, vol. 83, no. 24, pp. 12934-12946, 2009.
73. B. P. Tu and J. S. Weissman, "Oxidative protein folding in eukaryotes:mechanisms and consequences," The Journal of Cell Biology, vol. 164, no. 3, pp. 341-346, 2004.
74. E. Merquiol, D. Uzi, T. Mueller et al., "HCV causes chronic endoplasmic reticulum stress leading to adaptation and interference with the unfolded protein response," PLoS ONE, vol. 6, no. 9, Article IDe24660, 2011.
75. W. Yao, H. Cai, X. Li, T. Li, L. Hu, and T. Peng, "Endoplasmic reticulumstress links hepatitis C virus RNA replication to wildtype PGC-1/liver-specific PGC-1 upregulation," Journal of Virology, vol. 88, no. 15, pp. 8361-8374, 2014.
76. S.-W. Chan and P. A. Egan, "Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response," The FASEB Journal, vol. 19, no. 11, pp. 1510-1512, 2005.
77. Y. Zheng, B. Gao, L. Ye et al., "Hepatitis C virus non-structural protein NS4B can modulate an unfolded protein response," Journal of Microbiology, vol. 43, no. 6, pp. 529-536, 2005.
78. J. Jheng, J. Ho, and J. Horng, "ER stress, autophagy, and RNA viruses," Frontiers in Microbiology, vol. 5, article 388, 2014.
79. T. Anelli, L. Bergamelli,E. Margittai et al., "Ero1 regulates Ca2+ fluxes at the endoplasmic reticulum-mitochondria interface (MAM)," Antioxidants & Redox Signaling, vol. 16, no. 10, pp. 1077-1087, 2012.
80. J. Wang, R. Kang,H. Huang et al., "HepatitisCvirus coreprotein activates autophagy through EIF2AK3 andATF6UPR pathwaymediated MAP1LC3B and ATG12 expression," Autophagy, vol. 10, no. 5, pp. 766-784, 2014.
81. K. Nakai, H. Tanaka, K. Hanada et al., "Decreased expression of cytochromes P450 1A2, 2E1, and 3A4 and drug transporters Na+-taurocholate-cotransporting polypeptide, organic cation transporter 1, and organic anion-transporting peptide-C correlates with the progression of liver fibrosis in chronic hepatitis C patients," DrugMetabolism and Disposition, vol. 36, no. 9, pp. 1786-1793, 2008.
82. K. Linhart,H. Bartsch, andH. K. Seitz, "The roleof reactiveoxygen species (ROS) and cytochrome P-450 2E1 in the generation of carcinogenic etheno-DNA adducts," Redox Biology, vol. 3, pp. 56-62, 2014.
83. N. G. Avadhani, "Targeting of the same proteins to multiple subcellular destinations: mechanisms and physiological implications," The FEBS Journal, vol. 278, no. 22, article 4217, 2011.
84. M.-K. Kwak and T. W. Kensler, "Induction of 26S proteasome subunit PSMB5 by the bifunctional inducer 3-methylcholanthrene through the Nrf2-ARE, but not the AhR/Arnt-XRE, pathway," Biochemical and Biophysical Research Communications, vol. 345, no. 4, pp. 1350-1357, 2006.
85. D. Burdette,M. Olivarez, andG. Waris, "Activationof transcription factor Nrf2 by hepatitis C virus induces the cell-survival pathway," Journal of General Virology, vol. 91, no. 3, pp. 681-690, 2010.
86. Y. Jiang, H. Bao, Y. Ge et al., "Therapeutic targeting of GSK3 enhances the Nrf2 antioxidant response and confers hepatic cytoprotection in hepatitis C," Gut, vol. 64, no. 1, pp. 168-179, 2015.
87. A. V. Ivanov, O. A. Smirnova, O. N. Ivanova, O. V. Masalova, S. N. Kochetkov, andM. G. Isaguliants, "Hepatitis C virus proteins activate NRF2/ARE pathway by distinct ROS-dependent and independentmechanisms inHUH7 cells," PLoS ONE, vol. 6, no. 9, Article ID e24957, 2011.
88. S. Blackham, A. Baillie, F. Al-Hababi et al., "Gene expression profiling indicates the roles of host oxidative stress, apoptosis, lipid metabolism, and intracellular transport genes in the replication of hepatitis C virus," Journal of Virology, vol. 84, no. 10, pp. 5404-5414, 2010.
89. M. Y. Abdalla, B. E. Britigan, F. Wen et al., "Down-regulation of heme oxygenase-1 by hepatitis C virus infection in vivo and by the in vitro expression of hepatitis C core protein," Journal of Infectious Diseases, vol. 190, no. 6, pp. 1109-1118, 2004.
90. F. Wen, K. E. Brown, B. E. Britigan, and W. N. Schmidt, "HepatitisCcore protein inhibits induction of heme oxygenase-1 and sensitizes hepatocytes to cytotoxicity," Cell Biology and Toxicology, vol. 24, no. 2, pp. 175-188, 2008.
91. W. Tang, C. A. Lázaro, J. S. Campbell, W. T. Parks, M. G. Katze, and N. Fausto, "Responses of nontransformed human hepatocytes to conditional expression of full-length hepatitis C virus open reading frame," The American Journal of Pathology, vol. 171, no. 6, pp. 1831-1846, 2007.
92. C. Brault, P. Lévy, S. Duponchel et al., "Glutathione peroxidase 4 is reversibly induced by HCV to control lipid peroxidation and to increase virion infectivity," Gut, vol. 65, no. 1, pp. 144-154, 2014.
93. H. Huang, Y. Chen, and J. Ye, "Inhibition of hepatitis C virus replication by peroxidation of arachidonate and restoration by vitamin E," Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 47, pp. 18666-18670, 2007.
94. J. Choi, K. J. Lee, Y. Zheng, A. K. Yamaga,M. M. C. Lai, and J.-H. Ou, "Reactive oxygen species suppress hepatitis C virus RNA replication in human hepatoma cells," Hepatology, vol. 39, no. 1, pp. 81-89, 2004.
95. S. Ezzikouri, T. Nishimura, M. Kohara et al., "Inhibitory effects of Pycnogenol? on hepatitis C virus replication," Antiviral Research, vol. 113, pp. 93-102, 2015.
96. D. Ploen and E. Hildt, "Hepatitis C virus comes for dinner: how the hepatitis C virus interferes with autophagy," World Journal of Gastroenterology, vol. 21, no. 28, pp. 8492-8507, 2015.
97. T. Yorimitsu and D. J. Klionsky, "Eating the endoplasmic reticulum: quality control by autophagy," Trends in Cell Biology, vol. 17, no. 6, pp. 279-285, 2007.
98. B. Levine and J. Yuan, "Autophagy in cell death: An innocent convict?" The Journal of Clinical Investigation, vol. 115, no. 10, pp. 2679-2688, 2005.
99. N. Mizushima, B. Levine, A. M. Cuervo, and D. J. Klionsky, "Autophagy fights disease through cellular self-digestion," Nature, vol. 451, no. 7182, pp. 1069-1075, 2008.
100. K. Takeshige, M. Baba, S. Tsuboi, T. Noda, and Y. Ohsumi, "Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction," Journal of Cell Biology, vol. 119, no. 2, pp. 301-311, 1992.
101. V. Deretic and B. Levine, "Autophagy, immunity, and microbial adaptations," Cell Host & Microbe, vol. 5, no. 6, pp. 527-549, 2009.
102. S. Sengupta, T. R. Peterson, and D. M. Sabatini, "Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress," Molecular Cell, vol. 40, no. 2, pp. 310-322, 2010.
103. I. G. Ganley, H. Du Lam, J. Wang, X. Ding, S. Chen, and X. Jiang, "ULK1. ATG13. FIP200 complex complex mediates mTOR signaling and is essential for autophagy," The Journal of Biological Chemistry, vol. 284, no. 18, pp. 12297-12305, 2009.
104. N. Hosokawa, T. Hara, T. Kaizuka et al., "Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy," Molecular Biology of the Cell, vol. 20, no. 7, pp. 1981-1991, 2009.
105. J. Kim, M. Kundu, B. Viollet, and K.-L. Guan, "AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1," Nature Cell Biology, vol. 13, no. 2, pp. 132-141, 2011.
106. G. Kroemer, G. Mariño, and B. Levine, "Autophagy and the integrated stress response," Molecular Cell, vol. 40, no. 2, pp. 280-293, 2010.
107. N. Mizushima, T. Yoshimori, and Y. Ohsumi, "The role of Atg proteins in autophagosome formation," Annual Review of Cell and Developmental Biology, vol. 27, pp. 107-132, 2011.
108. E. Itakura and N. Mizushima, "Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins," Autophagy, vol. 6, no. 6, pp. 764-776, 2010.
109. K. Matsunaga, E. Morita, T. Saitoh et al., "Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L,"The Journal of Cell Biology, vol. 190, no. 4, pp. 511-521, 2010.
110. E. L. Axe, S. A. Walker, M. Manifava et al., "Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum," The Journal of Cell Biology, vol. 182, no. 4, pp. 685-701, 2008.
111. N. Fujita, T. Itoh, H. Omori, M. Fukuda, T. Noda, and T. Yoshimori, "The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy," Molecular Biology of the Cell, vol. 19, no. 5, pp. 2092-2100, 2008.
112. M. Hamasaki, N. Furuta, A. Matsuda et al., "Autophagosomes form at ER-mitochondria contact sites," Nature, vol. 495, no. 7441, pp. 389-393, 2013.
113. D. W. Hailey, A. S. Rambold, P. Satpute-Krishnan et al., "Mitochondria supply membranes for autophagosome biogenesis during starvation," Cell, vol. 141, no. 4, pp. 656-667, 2010.
114. W.-L. Yen, T. Shintani, U. Nair et al., "The conserved oligomeric Golgi complex is involved in double-membrane vesicle formation during autophagy," Journal of Cell Biology, vol. 188, no. 1, pp. 101-114, 2010.
115. B. Ravikumar, K. Moreau, L. Jahreiss, C. Puri, and D. C. Rubinsztein, "Plasma membrane contributes to the formation of pre-autophagosomal structures," Nature Cell Biology, vol. 12, no. 8, pp. 747-757, 2010.
116. E. Itakura, C. Kishi-Itakura, and N. Mizushima, "The hairpintype tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes," Cell, vol. 151, no. 6, pp. 1256-1269, 2012.
117. D. G. McEwan, D. Popovic, A. Gubas et al., "PLEKHM1 regulates autophagosome-lysosome fusion through HOPS complex and LC3/GABARAP proteins," Molecular Cell, vol. 57, no. 1, pp. 39-54, 2015.
118. L. M. Silva and J. U. Jung, "Modulation of the autophagy pathway by human tumor viruses," Seminars in Cancer Biology, vol. 23, no. 5, pp. 323-328, 2013.
119. G. Filomeni, D. de Zio, and F. Cecconi, "Oxidative stress and autophagy: the clash between damage and metabolic needs," Cell Death and Differentiation, vol. 22, no. 3, pp. 377-388, 2015.
120. G. Filomeni, E. Desideri, S. Cardaci, G. Rotilio, and M. R. Ciriolo, "Under the ROS: thiol network is the principal suspect for autophagy commitment," Autophagy, vol. 6, no. 7, pp. 999-1005, 2010.
121. K. Wang, "Autophagy and apoptosis in liver injury," Cell Cycle, vol. 14, no. 11, pp. 1631-1642, 2015.
122. R. Scherz-Shouval, E. Shvets, and Z. Elazar, "Oxidation as a post-translational modification that regulates autophagy," Autophagy, vol. 3, no. 4, pp. 371-373, 2007.
123. C. Zhang, L. Yang, X.-B. Wang et al., "Calyxin Y induces hydrogen peroxide-dependent autophagy and apoptosis via JNK activation in human non-small cell lung cancerNCI-H460 cells," Cancer Letters, vol. 340, no. 1, pp. 51-62, 2013.
124. Y. Chen, M. B. Azad, and S. B. Gibson, "Superoxide is themajor reactive oxygen species regulating autophagy," Cell Death and Differentiation, vol. 16, no. 7, pp. 1040-1052, 2009.
125. A.-L. Levonen, B. G. Hill, E. Kansanen, J. Zhang, and V. M. Darley-Usmar, "Redox regulation of antioxidants, autophagy, and the response to stress: implications for electrophile therapeutics," Free Radical Biology andMedicine, vol. 71, pp. 196-207, 2014.
126. E.-L. Eskelinen and P. Saftig, "Autophagy: A lysosomal degradation pathway with a central role in health and disease," Biochimica et Biophysica Acta-Molecular Cell Research, vol. 1793, no. 4, pp. 664-673, 2009.
127. T. Suzuki and M. Yamamoto, "Molecular basis of theKeap1-Nrf2 system," Free Radical Biology & Medicine B, vol. 88, pp. 93-100, 2015.
128. K. Itoh, T. Ishii, N. Wakabayashi, and M. Yamamoto, "Regulatory mechanisms of cellular response to oxidative stress," Free Radical Research, vol. 31, no. 4, pp. 319-324, 1999.
129. A. T. Dinkova-Kostova, W. D. Holtzclaw, R. N. Cole et al., "Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants," Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 18, pp. 11908-11913, 2002.
130. D. D. Zhang and M. Hannink, "Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress," Molecular and Cellular Biology, vol. 23, no. 22, pp. 8137-8151, 2003.
131. M. Komatsu, H. Kurokawa, S. Waguri et al., "The selective autophagy substrate p62 activates the stress responsive transcription factorNrf2 through inactivation of Keap1," Nature Cell Biology, vol. 12, no. 3, pp. 213-223, 2010.
132. A. Lau, X.-J. Wang, F. Zhao et al., "A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62,"Molecular and Cellular Biology, vol. 30, no. 13, pp. 3275-3285, 2010.
133. A. Jain, T. Lamark, E. Sjøttem et al., "p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription,"The Journal of Biological Chemistry, vol. 285, no. 29, pp. 22576-22591, 2010.
134. W. Fan, Z. Tang, D. Chen et al., "Keap1 facilitates p62-mediated ubiquitin aggregate clearance via autophagy," Autophagy, vol. 6, no. 5, pp. 614-621, 2010.
135. I. M. Copple, A. Lister, A. D. Obeng et al., "Physical and functional interaction of sequestosome 1 with Keap1 regulates the Keap1-Nrf2 cell defense pathway," The Journal of Biological Chemistry, vol. 285, no. 22, pp. 16782-16788, 2010.
136. T. Jiang, B. Harder,M. Rojo de laVega, P. K. Wong, E. Chapman, andD. D. Zhang, "p62 links autophagy andNrf2 signaling," Free Radical Biology & Medicine, vol. 88, pp. 199-204, 2015.
137. Y. Katsuragi, Y. Ichimura, and M. Komatsu, "p62/SQSTM1 functions as a signaling hub and an autophagy adaptor," The FEBS Journal, vol. 282, no. 24, pp. 4672-4678, 2015.
138. T. Johansen and T. Lamark, "Selective autophagy mediated by autophagic adapter proteins," Autophagy, vol. 7, no. 3, pp. 279-296, 2011.
139. Y. Ichimura, S. Waguri, Y.-S. Sou et al., "Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy," Molecular Cell, vol. 51, no. 5, pp. 618-631, 2013.
140. H. Digaleh, M. Kiaei, and F. Khodagholi, "Nrf2 and Nrf1 signaling and ER stress crosstalk: implication for proteasomal degradation and autophagy," Cellular and Molecular Life Sciences, vol. 70, no. 24, pp. 4681-4694, 2013.
141. T. Asselah, I. Bièche, A. Mansouri et al., "In vivo hepatic endoplasmic reticulum stress in patients with chronic hepatitis C," The Journal of Pathology, vol. 221, no. 3, pp. 264-274, 2010.
142. D. Sir, W.-L. Chen, J. Choi, T. Wakita, T. S. B. Yen, and J.-H. J. Ou, "Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response," Hepatology, vol. 48, no. 4, pp. 1054-1061, 2008.
143. P.-Y. Ke and S. S.-L. Chen, "Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro," The Journal of Clinical Investigation, vol. 121, no. 1, pp. 37-56, 2011.
144. K. D. Tardif, K. Mori, and A. Siddiqui, "Hepatitis C virus subgenomic replicons induce endoplasmic reticulumstress activating an intracellular signaling pathway," Journal of Virology, vol. 76, no. 15, pp. 7453-7459, 2002.
145. P.-Y. Ke and S. S.-L. Chen, "Autophagy: A novel guardian ofHCV against innate immune response," Autophagy, vol. 7, no. 5, pp. 533-535, 2011.
146. S. Li, L. Ye, X. Yu et al., "Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulumoverload response-dependent NF-B activation," Virology, vol. 391, no. 2, pp. 257-264, 2009.
147. W.-C. Su, T.-C. Chao, Y.-L. Huang, S.-C. Weng, K.-S. Jeng, and M. M. C. Lai, "Rab5 and class III phosphoinositide 3-kinase Vps34 are involved in hepatitis C virus NS4B-induced autophagy," Journal of Virology, vol. 85, no. 20, pp. 10561-10571, 2011.
148. S. Shrivastava, A. Raychoudhuri, R. Steele, R. Ray, and R. B. Ray, "Knockdown of autophagy enhances the innate immune response in hepatitis C virus-infected hepatocytes," Hepatology, vol. 53, no. 2, pp. 406-414, 2011.
149. I. P. Grégoire, C. Rabourdin-Combe, andM. Faure, "Autophagy and RNA virus interactomes reveal IRGMas a common target," Autophagy, vol. 8, no. 7, pp. 1136-1137, 2012.
150. S. Shrivastava, P. Devhare, N. Sujijantarat et al., "Knockdown of autophagy inhibits infectious hepatitis C virus release by the exosomal pathway," Journal of Virology, vol. 90, no. 3, pp. 1387-1396, 2016.
151. L. Wang, Y. Tian, J.-H. J. Ou, and G. G. Luo, "HCV induces the expression of Rubicon and UVRAG to temporally regulate the maturation of autophagosomes and viral replication," PLoS Pathogens, vol. 11, no. 3, Article ID e1004764, 2015.
152. L. Wang and J.-H. James Ou, "Hepatitis C virus and autophagy," Biological Chemistry, vol. 396, no. 11, pp. 1215-1222, 2015.
153. P.-Y. Ke and S. S.-L. Chen, "Autophagy in hepatitis C virus-host interactions: potential roles and therapeutic targets for liverassociated diseases," World Journal of Gastroenterology, vol. 20, no. 19, pp. 5773-5793, 2014.
154. I. Romero-Brey, A. Merz, A. Chiramel et al., "Threedimensional architecture and biogenesis of membrane structures associated with hepatitis C virus replication," PLoS Pathogens, vol. 8, no. 12, Article IDe1003056, 2012.
155. P. Ferraris, E. Blanchard, and P. Roingeard, "Ultrastructural and biochemical analyses of hepatitis C virus-associated host cell membranes,"The Journal of General Virology, vol. 91, no. 9, pp. 2230-2237, 2010.
156. D. Egger, B. Wölk, R. Gosert et al., "Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex," Journal of Virology, vol. 76, no. 12, pp. 5974-5984, 2002.
157. D. Paul, S. Hoppe, G. Saher, J. Krijnse-Locker, and R. Bartenschlager, "Morphological and biochemical characterization of the membranous hepatitis C virus replication compartment," Journal of Virology, vol. 87, no. 19, pp. 10612-10627, 2013.
158. I. Romero-Brey and R. Bartenschlager, "Membranous replication factories induced by plus-strand RNA viruses," Viruses, vol. 6, no. 7, pp. 2826-2857, 2014.
159. N. Mizushima, A. Yamamoto, M. Hatano et al., "Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells," The Journal of Cell Biology, vol. 152, no. 4, pp. 657-668, 2001.
160. C. Guévin, D. Manna, C. Bélanger, K. V. Konan, P. Mak, and P. Labonté, "Autophagy protein ATG5 interacts transiently with the hepatitis C virus RNA polymerase (NS5B) early during infection," Virology, vol. 405, no. 1, pp. 1-7, 2010.
161. M. Dreux, P. Gastaminza, S. F. Wieland, and F. V. Chisari, "The autophagy machinery is required to initiate hepatitis C virus replication," Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 14046-14051, 2009.
162. M. Dreux and F. V. Chisari, "Autophagy proteins promote hepatitis C virus replication," Autophagy, vol. 5, no. 8, pp. 1224-1225, 2009.
163. S. Shrivastava, J. B. Chowdhury, R. Steele, R. Ray, and R. B. Ray, "Hepatitis C virus upregulates Beclin1 for induction of autophagy and activates mTOR signaling," Journal of Virology, vol. 86, no. 16, pp. 8705-8712, 2012.
164. H. Li, X. Yang, G. Yang et al., "Hepatitis C virus NS5A hijacks ARFGAP1 to maintain a phosphatidylinositol 4-phosphateenriched microenvironment," Journal of Virology, vol. 88, no. 11, pp. 5956-5966, 2014.
165. D. Sir, C.-F. Kuo, Y. Tian et al., "Replication of hepatitis C virus RNA on autophagosomalmembranes," The Journal of Biological Chemistry, vol. 287, no. 22, pp. 18036-18043, 2012.
166. M. Ait-Goughoulte, T. Kanda, K. Meyer, J. S. Ryerse, R. B. Ray, and R. Ray, "HepatitisCvirus genotype 1a growth and induction of autophagy," Journal of Virology, vol. 82, no. 5, pp. 2241-2249, 2008.
167. 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, vol. 5, no. 7, pp. 937-945, 2009.
168. M. DreuxandF. V. Chisari, "Impactof the autophagymachinery on hepatitis C virus infection," Viruses, vol. 3, no. 8, pp. 1342-1357, 2011.
169. F. Elgner, C. Donnerhak, H. Ren et al., "Characterization of -taxilin as a novel factor controlling the release of hepatitis C virus,"TheBiochemical Journal, vol. 473, no. 2,pp. 145-155, 2016.
170. I. P. Grégoire, C. Richetta, L. Meyniel-Schicklin et al., "IRGM is a common target of RNA viruses that subvert the autophagy network," PLoS Pathogens, vol. 7, no. 12, Article ID e1002422, 2011.
171. A. C. Oliveira, E. R. Parise, R. M. Catarino et al., "Insulin resistance and not steatosis is associated with modifications in oxidative stressmarkers in chronic hepatitisC, non-3 genotype," Free Radical Research, vol. 43, no. 12, pp. 1187-1194, 2009.
172. H. Kamata, S.-I. Honda, S. Maeda, L. Chang, H. Hirata, and M. Karin, "Reactive oxygen species promote TNF-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases," Cell, vol. 120, no. 5, pp. 649-661, 2005.
173. J.-J. Ventura,P. Cogswell, R. A. Flavell, A. S. BaldwinJr., andR. J. Davis, "JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species," Genes & Development, vol. 18, no. 23, pp. 2905-2915, 2004.
174. Y. Zick, "Ser/Thr phosphorylation of IRS proteins: A molecular basis for insulin resistance," Science's STKE Signal Transduction Knowledge Environment, vol. 2005, no. 268, p. pe4, 2005.
175. K. Morino, K. F. Petersen, and G. I. Shulman, "Molecular mechanisms of insulin resistance in humans and their potential links with mitochondrial dysfunction," Diabetes, vol. 55, supplement 2, pp. S9-S15, 2006.
176. A. Shlomai, M. M. Rechtman, E. O. Burdelova et al., "The metabolic regulator PGC-1 links hepatitis C virus infection to hepatic insulin resistance," Journal of Hepatology, vol. 57, no. 4, pp. 867-873, 2012.
177. N. Kumashiro, Y. Tamura, T. Uchida et al., "Impact of oxidative stress and peroxisome proliferator-activated receptor coactivator-1 in hepatic insulin resistance," Diabetes, vol. 57, no. 8, pp. 2083-2091, 2008.
178. J. Lin, C. Handschin, and B. M. Spiegelman, "Metabolic control through the PGC-1 family of transcription coactivators," Cell Metabolism, vol. 1, no. 6, pp. 361-370, 2005.
179. J. Rhee, Y. Inoue, J. C. Yoon et al., "Regulation of hepatic fasting response by PPAR coactivator-1 (PGC-1): requirement for hepatocyte nuclear factor 4 in gluconeogenesis," Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 4012-4017, 2003.
180. N. Tanaka, K. Moriya, K. Kiyosawa, K. Koike, F. J. Gonzalez, and T. Aoyama, "PPAR activation is essential for HCV core protein-induced hepatic steatosis and hepatocellular carcinoma in mice,"The Journal of Clinical Investigation, vol. 118, no. 2, pp. 683-694, 2008.
181. 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," Journal of Virology, vol. 81, no. 15, pp. 8122-8130, 2007.