HCV-induced oxidative stress by inhibition of Nrf2 triggers autophagy and favors release of viral particles

Free Radical Biology and Medicine

Volumn 110, Issue , 2017, Pages 300-315

  Medvedev, Regina ^a   Ploen, Daniela ^a   Spengler, Catrina ^a   Elgner, Fabian ^a   Ren, Huimei ^a   Bunten, Sarah ^a   Hildt, Eberhard ^a,b  

^a PAUL EHRLICH INSTITUT   (Germany)

^b Deutsches Zentrum für Infektions forschung DZIF   (Germany)

Author keywords

Autophagy; Crosstalk; Hepatitis C virus; Nrf2 ARE signaling; P62; Particle release; Reactive oxygen species (ROS)

Indexed keywords

3 METHYLADENINE; AUTOPHAGY RELATED PROTEIN 5; BECLIN 1; GLUCOSE OXIDASE; HETERODIMER; MESSENGER RNA; PROTEASOME; REACTIVE OXYGEN METABOLITE; SCAVENGER; SEQUESTOSOME 1; TRANSCRIPTION FACTOR NRF2; VIRUS RNA; KEAP1 PROTEIN, HUMAN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NFE2L2 PROTEIN, HUMAN; PROTEIN BINDING; SQSTM1 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGY; CELL LYSATE; CONTROLLED STUDY; GENE OVEREXPRESSION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; LIVER CELL; LUCIFERASE ASSAY; LYSOSOME; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REPLICON; REPORTER GENE; SIGNAL TRANSDUCTION; VIRUS DETECTION; VIRUS GENOME; VIRUS INHIBITION; VIRUS PARTICLE; VIRUS RELEASE; VIRUS REPLICATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; ANTIOXIDANT RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEPACIVIRUS; HOST PATHOGEN INTERACTION; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE; VIRION; VIROLOGY;

ANTIOXIDANT RESPONSE ELEMENTS; AUTOPHAGY; CELL LINE, TUMOR; GENE EXPRESSION REGULATION; HEPACIVIRUS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN BINDING; REACTIVE OXYGEN SPECIES; SEQUESTOSOME-1 PROTEIN; SIGNAL TRANSDUCTION; VIRION; VIRUS RELEASE;

EID: 85021745081     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2017.06.021     Document Type: Article

References (70)

1. Gower, E., Estes, C., Blach, S., Razavi-Shearer, K., Razavi, H., Global epidemiology and genotype distribution of the hepatitis C virus infection. J. Hepatol. 61 (2014), S45–57.
2. Choo, Q.L., Kuo, G., Weiner, A.J., Overby, L.R., Bradley, D.W., Houghton, M., Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244 (1989), 359–362.
3. Appel, N., Schaller, T., Penin, F., Bartenschlager, R., From structure to function: new insights into hepatitis C virus RNA replication. J. Biol. Chem. 281 (2006), 9833–9836.
4. Moradpour, D., Gosert, R., Egger, D., Penin, F., Blum, H.E., Bienz, K., Membrane association of hepatitis C virus nonstructural proteins and identification of the membrane alteration that harbors the viral replication complex. Antivir. Res. 60 (2003), 103–109.
5. Bartenschlager, R., Lohmann, V., Novel cell culture systems for the hepatitis C virus. Antivir. Res. 52 (2001), 1–17.
6. Bartenschlager, R., Penin, F., Lohmann, V., André, P., Assembly of infectious hepatitis C virus particles. Trends Microbiol. 19 (2011), 95–103.
7. Lindenbach, B.D., Virion assembly and release. Curr. Top. Microbiol. Immunol. 369 (2013), 199–218.
8. Choi, J., Corder, N.L.B., Koduru, B., Wang, Y., Oxidative stress and hepatic Nox proteins in chronic hepatitis C and hepatocellular carcinoma. Free Radic. Biol. Med. 72 (2014), 267–284.
9. Ivanov, A.V., Bartosch, B., Smirnova, O.A., Isaguliants, M.G., Kochetkov, S.N., HCV and oxidative stress in the liver. Viruses 5 (2013), 439–469.
10. Fu, N., Yao, H., Nan, Y., Qiao, L., Role of oxidative stress in hepatitis C virus induced hepatocellular carcinoma. Curr. Cancer Drug Targets, 2016.
11. Kensler, T.W., Wakabayashi, N., Biswal, S., Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47 (2007), 89–116.
12. O'Connell, M.A., Hayes, J.D., The Keap1/Nrf2 pathway in health and disease: from the bench to the clinic. Biochem. Soc. Trans. 43 (2015), 687–689.
13. Harder, B., Jiang, T., Wu, T., Tao, S., Montserrat Rojo, de la Vega, Tian, W., Chapman, E., Zhang, D.D., Molecular mechanisms of Nrf2 regulation and how these influence chemical modulation for disease intervention. Biochem. Soc. Trans. 43 (2015), 680–686.
14. Wasserman, W.W., Fahl, W.E., Functional antioxidant responsive elements. Proc. Natl. Acad. Sci. USA 94 (1997), 5361–5366.
15. 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. 286 (2011), 8941–8951.
16. Mizushima, N., Levine, B., Cuervo, A.M., Klionsky, D.J., Autophagy fights disease through cellular self-digestion. Nature 451 (2008), 1069–1075.
17. Kazuhiko Takeshige, Misuzu Baba, Shigeru Tsuboi, Takeshi Noda, Yoshinori Ohsumi, Autophagy in Yeast Demonstrated with Proteinase-deficient Mutants and Conditions for its Induction, 1992.
18. Deretic, V., Levine, B., Autophagy, immunity, and microbial adaptations. Cell Host Microbe 5 (2009), 527–549.
19. Ariosa, A.R., Klionsky, D.J., Autophagy core machinery: overcoming spatial barriers in neurons. J. Mol. Med. 94 (2016), 1217–1227.
20. Taniguchi, K., Yamachika, S., He, F., Karin, M., p62/SQSTM1-Dr. Jekyll and Mr. Hyde that prevents oxidative stress but promotes liver cancer. FEBS Lett. 590 (2016), 2375–2397.
21. Johansen, T., Lamark, T., Selective autophagy mediated by autophagic adapter proteins. Autophagy 7 (2011), 279–296.
22. Dash, S., Chava, S., Aydin, Y., Chandra, P.K., Ferraris, P., Chen, W., Balart, L.A., Wu, T., Garry, R.F., Hepatitis C virus infection induces autophagy as a prosurvival mechanism to alleviate hepatic ER-stress response. Viruses, 8, 2016.
23. Elgner, F., Ren, H., Medvedev, R., Ploen, D., Himmelsbach, K., Boller, K., Hildt, E., The intra-cellular cholesterol transport inhibitor U18666A inhibits the exosome-dependent release of mature hepatitis C virus. J. Virol., 2016.
24. Ren, H., Elgner, F., Jiang, B., Himmelsbach, K., Medvedev, R., Ploen, D., Hildt, E., The autophagosomal SNARE protein syntaxin 17 is an essential factor for the hepatitis C virus life cycle. J. Virol. 90 (2016), 5989–6000.
25. Wang, L., Tian, Y., Ou, J.-hJ., HCV induces the expression of Rubicon and UVRAG to temporally regulate the maturation of autophagosomes and viral replication. PLoS Pathog., 11, 2015, e1004764.
26. Shrivastava, S., Devhare, P., Sujijantarat, N., Steele, R., Kwon, Y.-C., Ray, R., Ray, R.B., Knockdown of autophagy inhibits infectious hepatitis C virus release by the exosomal pathway. J. Virol. 90 (2016), 1387–1396.
27. Wang, J., Kang, R., Huang, H., Xi, X., Wang, B., Wang, J., Zhao, Z., Hepatitis C virus core protein activates autophagy through EIF2AK3 and ATF6 UPR pathway-mediated MAP1LC3B and ATG12 expression. Autophagy 10 (2014), 766–784.
28. Chu, V.C., Bhattacharya, S., Nomoto, A., Lin, J., Zaidi, S.K., Oberley, T.D., Weinman, S.A., Azhar, S., Huang, T.-T., Persistent expression of hepatitis C virus non-structural proteins leads to increased autophagy and mitochondrial injury in human hepatoma cells. PLoS One, 6, 2011, e28551.
29. Mohl, B.-P., Bartlett, C., Mankouri, J., Harris, M., Early events in the generation of autophagosomes are required for the formation of membrane structures involved in hepatitis C virus genome replication. J. Gen. Virol. 97 (2016), 680–693.
30. Hansen, M.D., Johnsen, I.B., Stiberg, K.A., Sherstova, T., Wakita, T., Richard, G.M., Kandasamy, R.K., Meurs, E.F., Anthonsen, M.W., Hepatitis C virus triggers Golgi fragmentation and autophagy through the immunity-related GTPase M. Proc. Natl. Acad. Sci. USA 114 (2017), E3462–E3471.
31. Filomeni, G., Desideri, E., Cardaci, S., Rotilio, G., Ciriolo, M.R., Under the ROS…thiol network is the principal suspect for autophagy commitment. Autophagy 6 (2010), 999–1005.
32. Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., Sou, Y.-S., Ueno, I., Sakamoto, A., Tong, K.I., Kim, M., Nishito, Y., Iemura, S.-i., Natsume, T., Ueno, T., Kominami, E., Motohashi, H., Tanaka, K., Yamamoto, M., The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12 (2010), 213–223.
33. Lau, A., Wang, X.-J., Zhao, F., Villeneuve, N.F., Wu, T., Jiang, T., Sun, Z., White, E., Zhang, D.D., A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 30 (2010), 3275–3285.
34. Jain, A., Lamark, T., Sjøttem, E., Larsen, K.B., Awuh, J.A., Øvervatn, A., McMahon, M., Hayes, J.D., Johansen, T., p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J. Biol. Chem. 285 (2010), 22576–22591.
35. Fan, W., Tang, Z., Chen, D., Moughon, D., Ding, X., Chen, S., Zhu, M., Zhong, Q., Keap1 facilitates p62-mediated ubiquitin aggregate clearance via autophagy. Autophagy 6 (2010), 614–621.
36. Copple, I.M., Lister, A., Obeng, A.D., Kitteringham, N.R., Jenkins, R.E., Layfield, R., Foster, B.J., Goldring, C.E., Park, B.K., Physical and functional interaction of sequestosome 1 with Keap1 regulates the Keap1-Nrf2 cell defense pathway. J. Biol. Chem. 285 (2010), 16782–16788.
37. T. Jiang, B. Harder, Vega, Montserrat Rojo de la, P.K. Wong, E. Chapman, D.D. Zhang, p62 links autophagy and Nrf2 signaling, Free Radic. Biol. Med., 2015.
38. Wakita, T., Pietschmann, T., Kato, T., Date, T., Miyamoto, M., Zhao, Z., Murthy, K., Habermann, A., Kräusslich, H.-G., Mizokami, M., Bartenschlager, R., Liang, T.J., Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11 (2005), 791–796.
39. 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. 9 (2007), 1089–1097.
40. Pietschmann, T., Kaul, A., Koutsoudakis, G., Shavinskaya, A., Kallis, S., Steinmann, E., Abid, K., Negro, F., Dreux, M., Cosset, F.-L., Bartenschlager, R., Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc. Natl. Acad. Sci. USA 103 (2006), 7408–7413.
41. Oikawa, D., Akai, R., Tokuda, M., Iwawaki, T., A transgenic mouse model for monitoring oxidative stress. Sci. Rep., 2, 2012, 229.
42. Blight, K.J., McKeating, J.A., Rice, C.M., Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76 (2002), 13001–13014.
43. Weiss, T.S., Pahernik, S., Scheruebl, I., Jauch, K.-W., Thasler, W.E., Cellular damage to human hepatocytes through repeated application of 5-aminolevulinic acid. J. Hepatol. 38 (2003), 476–482.
44. Dorko, K., Freeswick, P.D., Bartoli, F., Cicalese, L., Bardsley, B.A., Tzakis, A., Nussler, A.K., A new technique for isolating and culturing human hepatocytes from whole or split livers not used for transplantation. Cell Transplant. 3 (1994), 387–395.
45. Bürckstümmer, T., Kriegs, M., Lupberger, J., Pauli, E.K., Schmittel, S., Hildt, E., Raf-1 kinase associates with Hepatitis C virus NS5A and regulates viral replication. FEBS Lett. 580 (2006), 575–580.
46. Schaedler, S., Krause, J., Himmelsbach, K., Carvajal-Yepes, M., Lieder, F., Klingel, K., Nassal, M., Weiss, T.S., Werner, S., Hildt, E., Hepatitis B virus induces expression of antioxidant response element-regulated genes by activation of Nrf2. J. Biol. Chem. 285 (2010), 41074–41086.
47. Beyer, T.A., Xu, W., Teupser, D., Ulrich, auf dem Keller, Bugnon, P., Hildt, E., Thiery, J., Kan, Y.W., Werner, S., Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance. EMBO J. 27 (2008), 212–223.
48. Wang, X., Gu, C., He, W., Ye, X., Chen, H., Zhang, X., Hai, C., Glucose oxidase induces insulin resistance via influencing multiple targets in vitro and in vivo: the central role of oxidative stress. Biochimie 94 (2012), 1705–1717.
49. Kärber, G., Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche, Archiv f. experiment. Pathol. Pharmakol. 162 (1931), 480–483.
50. Spearman, C., The method of ‘right and wrong cases’ (‘constant stimuli’) without gauss's formulae. Br. J. Psychol. 1904–1920:2 (1908), 227–242.
51. G. Bjorkoy, T. Lamark, S. Pankiv, A. Øvervatn, A. Brech, T. Johansen, Chapter 12 monitoring autophagic degradation of p62/SQSTM1, in: Methods in Enzymology Autophagy in Mammalian Systems, Part B, Academic Press, 2009, pp. 181–197.
52. Kwak, M.-K., Kensler, T.W., 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. 345 (2006), 1350–1357.
53. Quinkert, D., Bartenschlager, R., Lohmann, V., Quantitative analysis of the hepatitis C virus replication complex. J. Virol. 79 (2005), 13594–13605.
54. Post, J., Ratnarajah, S., Lloyd, A.R., Immunological determinants of the outcomes from primary hepatitis C infection. Cell. Mol. Life Sci. 66 (2009), 733–756.
55. Osburn, W.O., Wakabayashi, N., Misra, V., Nilles, T., Biswal, S., Trush, M.A., Kensler, T.W., Nrf2 regulates an adaptive response protecting against oxidative damage following diquat-mediated formation of superoxide anion. Arch. Biochem. Biophys. 454 (2006), 7–15.
56. Ichimura, Y., Waguri, S., Sou, Y.-S., 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, M.-S., Yoshimori, T., Tanaka, K., Yamamoto, M., Komatsu, M., Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol. Cell 51 (2013), 618–631.
57. Bartosch, B., Thimme, R., Blum, H.E., Zoulim, F., Hepatitis C virus-induced hepatocarcinogenesis. J. Hepatol. 51 (2009), 810–820.
58. Dreux, M., Chisari, F.V., Autophagy proteins promote hepatitis C virus replication. Autophagy 5 (2009), 1224–1225.
59. Ploen, D., Hildt, E., Hepatitis C virus comes for dinner: how the hepatitis C virus interferes with autophagy. World J. Gastroenterol. 21 (2015), 8492–8507.
60. Sir, D., Kuo, C.-F., Tian, Y., Liu, H.M., Huang, E.J., Jung, J.U., Machida, K., Ou, J.J., Replication of hepatitis C virus RNA on autophagosomal membranes. J. Biol. Chem. 287 (2012), 18036–18043.
61. Dreux, M., Gastaminza, P., Wieland, S.F., Chisari, F.V., The autophagy machinery is required to initiate hepatitis C virus replication. Proc. Natl. Acad. Sci. USA 106 (2009), 14046–14051.
62. Filomeni, G., de Zio, D., Cecconi, F., Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 22 (2015), 377–388.
63. Ivanov, A.V., Smirnova, O.A., Petrushanko, I.Y., Ivanova, O.N., Karpenko, I.L., Alekseeva, E., Sominskaya, I., Makarov, A.A., Bartosch, B., Kochetkov, S.N., Isaguliants, M.G., HCV core protein uses multiple mechanisms to induce oxidative stress in human hepatoma huh7 cells. Viruses 7 (2015), 2745–2770.
64. de Mochel, Seronello, S., Wang, S.H., Ito, C., Zheng, J.X., Liang, T.J., Lambeth, J.D., Choi, J., Hepatocyte NAD(P)H oxidases as an endogenous source of reactive oxygen species during hepatitis C virus infection. Hepatology 52 (2010), 47–59.
65. Pawlotsky, J.-M., Feld, J.J., Zeuzem, S., Hoofnagle, J.H., From non-A, non-B hepatitis to hepatitis C virus cure. J. Hepatol. 62 (2015), S87–S99.
66. San Miguel, R., Gimeno-Ballester, V., Blázquez, A., Mar, J., Cost-effectiveness analysis of sofosbuvir-based regimens for chronic hepatitis C. Gut 64 (2015), 1277–1288.
67. Peymani, P., Yeganeh, B., Sabour, S., Geramizadeh, B., Fattahi, M.R., Keyvani, H., Azarpira, N., Coombs, K.M., Ghavami, S., Lankarani, K.B., New use of an old drug: chloroquine reduces viral and ALT levels in HCV non-responders (a randomized, triple-blind, placebo-controlled pilot trial). Can. J. Physiol. Pharmacol. 94 (2016), 613–619.
68. Shawki, S.M., Meshaal, S.S., El Dash, A.S., Zayed, N.A., Hanna, M.O.F., Increased DNA damage in hepatitis C virus-related hepatocellular carcinoma. DNA Cell Biol. 33 (2014), 884–890.
69. Tsukiyama-Kohara, K., Role of oxidative stress in hepatocarcinogenesis induced by hepatitis C virus. Int. J. Mol. Sci. 13 (2012), 15271–15278.
70. Barthel, S.R., Medvedev, R., Heinrich, T., Buchner, S.M., Kettern, N., Hildt, E., Hepatitis B virus inhibits insulin receptor signaling and impairs liver regeneration via intracellular retention of the insulin receptor. Cell. Mol. Life Sci. 73 (2016), 4121–4140.