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Redox Report
Communications in Free Radical Research
Volume 24, 2019 - Issue 1
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Research Articles

Hepatitis C virus core or NS3/4A protein expression preconditions hepatocytes against oxidative stress and endoplasmic reticulum stress

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References

  • World Health Organization [Internet]. 2017 [cited 2017 Jun 20]. Available from: http://www.who.int/mediacentre/factsheets/fs164/en//
  • Wiktor SZ, Scott JD. What is the impact of treatment for hepatitis C virus infection? Lancet. 2017;390(10090):107–109. doi: 10.1016/S0140-6736(17)31762-2
  • Moradpour D, Penin F, Rice CM. Replication of hepatitis C virus. Nat Rev Microbiol. 2007;5(6):453–463. doi: 10.1038/nrmicro1645
  • Bartenschlager R, Lohmann V. Replication of hepatitis C virus. J Gen Virol. 2000;81(Pt 7):1631–1648. doi: 10.1099/0022-1317-81-7-1631
  • Vassilaki N, Mavromara P. The HCV ARFP/F/core + 1 protein: production and functional analysis of an unconventional viral product. IUBMB Life. 2009;61(7):739–752. doi: 10.1002/iub.201
  • Lozano-Sepulveda SA, Bryan-Marrugo OL, Cordova-Fletes C, et al. Oxidative stress modulation in hepatitis C virus infected cells. World J Hepatol. 2015;7(29):2880–2889. doi: 10.4254/wjh.v7.i29.2880
  • Ke PY, Chen SS. Hepatitis C virus and cellular stress response: implications to molecular pathogenesis of liver diseases. Viruses. 2012;4:2251–2290. doi: 10.3390/v4102251
  • Fulda S, Gorman AM, Hori O, et al. Cellular stress responses: cell survival and cell death. Int J Cell Biol. 2010;2010:1–23.
  • Valgimigli M, Valgimigli L, Trerè D, et al. Oxidative stress EPR Measurement in human liver by radical-probe Technique. Correlation with Etiology, Histology and cell Proliferation. Free Radic Res. 2002;36(9):939–948. doi: 10.1080/107156021000006653
  • Ivanov A V, Bartosch B, Smirnova OA, et al. HCV and oxidative stress in the liver. Viruses. 2013;5(2):439–469. doi: 10.3390/v5020439
  • Farinati F, Cardin R LNDM, Della LG, et al. Iron storage, lipid peroxidation and glutathione turnover in chronic anti-HCV positive hepatitis. J Hepatol. 1995;22(4):449–456. doi: 10.1016/0168-8278(95)80108-1
  • Bureau C, Bernad J, Chaouche N, et al. Nonstructural 3 protein of hepatitis C virus triggers an oxidative Burst in human Monocytes via activation of NADPH Oxidase. J Biol Chem. 2001;276(25):23077–23083. doi: 10.1074/jbc.M100698200
  • Ivanov A V, Smirnova OA, Ivanova ON, et al. Hepatitis C virus proteins activate NRF2/ARE pathway by distinct ROS-dependent and independent mechanisms in HUH7 cells. PLoS One. 2011;6(9):1–11. doi: 10.1371/journal.pone.0024957
  • Pal S, Polyak SJ, Bano N, et al. Hepatitis C virus induces oxidative stress. DNA damage and modulates the DNA repair enzyme NEI(L1). J Gastroenterol Hepatol. 2010;25(3):627–634. doi: 10.1111/j.1440-1746.2009.06128.x
  • García-Mediavilla MV, Sánchez-Campos S, González-Pérez P, et al. Differential contribution of hepatitis C virus NS5A and core proteins to the induction of oxidative and nitrosative stress in human hepatocyte-derived cells. J Hepatol. 2005;43(4):606–613. doi: 10.1016/j.jhep.2005.04.019
  • Bukh J, Purcell RH, Miller RH. Sequence analysis of the core gene of 14 hepatitis C virus genotypes. Proc Natl Acad Sci U S A. 1994;91(17):8239–8243. doi: 10.1073/pnas.91.17.8239
  • Ivanov A V, Smirnova OA, Petrushanko IY, et al. Hcv core protein uses multiple mechanisms to induce oxidative stress in human hepatoma huh7 cells. Viruses. 2015;7(6):2745–2770. doi: 10.3390/v7062745
  • Gallinari P, Brennan D, Nardi C, et al. Multiple enzymatic activities associated with recombinant NS3 protein of hepatitis C virus. J Virol. 1998;72(8):6758–6769.
  • Lk BW, Sansonno D, Kr Usslich H-G, et al. Subcellular Localization, Stability, and trans-Cleavage Competence of the hepatitis C virus NS3-NS4A Complex expressed in Tetracycline-regulated cell Lines. J Virol. 2000;74(5):2293–2304. doi: 10.1128/JVI.74.5.2293-2304.2000
  • Ke P, 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(1):37–56. doi: 10.1172/JCI41474
  • Merquiol E, Uzi D, Mueller T, et al. Hcv Causes chronic endoplasmic reticulum stress Leading to adaptation and Interference with the Unfolded protein response. PLoS ONE. 2011;6(9):1–12. doi: 10.1371/journal.pone.0024660
  • Benali-Furet NL, Chami M, Houel L, et al. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene. 2005;24(31):4921–4933. doi: 10.1038/sj.onc.1208673
  • Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334:1081–1087. doi: 10.1126/science.1209038
  • Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007;8(7):519–529. doi: 10.1038/nrm2199
  • Chan S-W. Unfolded protein response in hepatitis C virus infection. Front Microbiol. 2014;5(May):233.
  • Szegezdi E, Logue SE, Gorman AM, et al. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep. 2006;7(9):880–885. doi: 10.1038/sj.embor.7400779
  • Criddle DN, Gillies S, Baumgartner-wilson HK, et al. Menadione-induced reactive oxygen species generation via redox Cycling Promotes apoptosis of Murine Pancreatic Acinar cells. J Biol Chem. 2006;281(52):40485–40492. doi: 10.1074/jbc.M607704200
  • Thort H, Smith MT, Hartzells P, Bellomo G, Jewelll A. The Metabolism of menadione (2-Methyl-1, 4-naphthoquinone) by isolated hepatocytes. J Biol Chem. 1982;257(20):12419–12425.
  • Laux I, Nel A. Evidence that oxidative stress-induced apoptosis by menadione involves Fas-dependent and Fas-independent pathways. Clin Immunol. 2001;101(3):335–344. doi: 10.1006/clim.2001.5129
  • Conde L, Rosa D, Schoemaker MH, et al. Superoxide anions and hydrogen peroxide induce hepatocyte death by different mechanisms : involvement of JNK and ERK MAP kinases. J Hepatol. 2006;44(5):918–929. doi: 10.1016/j.jhep.2005.07.034
  • Moshage H, Casini A, Lieber S. Acetaldehyde Selectively Stimulates collagen production in cultured Rat liver Fat-storing cells but not in hepatocytes. J Hepatol. 1990;12(3):511–518. doi: 10.1002/hep.1840120311
  • Schoemaker MH, de la Rosa L C, Buist-homan M, et al. Tauroursodeoxycholic Acid protects Rat hepatocytes from Bile Acid-induced apoptosis via activation of survival pathways. Hepatology. 2004;39(6):1563–1573. doi: 10.1002/hep.20246
  • Esposito G, Scarselli E, Cerino A, et al. A human antibody specific for hepatitis C virus core protein: synthesis in a bacterial system and characterization. Gene. 1995;164(2):203–209. doi: 10.1016/0378-1119(95)00435-9
  • Ryter SW, Choi AMK. Heme oxygenase-1: molecular mechanisms of gene expression in oxygen-related stress. Antioxid Redox Signal. 2002;4(4):625–632. doi: 10.1089/15230860260220120
  • Czaja MJ. Two types of autophagy are better than one during hepatocyte oxidative stress. Autophagy. 2011;7(1):96–97. doi: 10.4161/auto.7.1.13885
  • Kayesh MEH, Ezzikouri S, Sanada T, et al. Oxidative stress and Immune Responses during hepatitis C virus infection in Tupaia belangeri. Sci Rep. 2017;7(1):9848. doi: 10.1038/s41598-017-10329-7
  • Gardmo C, Kotokorpi P, Helander H, et al. Transfection of adult primary rat hepatocytes in culture. Biochem Pharmacol. 2005;69(12):1805–1813. doi: 10.1016/j.bcp.2005.03.028
  • Farquhar MJ, Mckeating JA. Primary hepatocytes as targets for hepatitis C virus replication. J Viral Hepat. 2008;15(12):849–854. doi: 10.1111/j.1365-2893.2008.01051.x
  • Banaudha K, Orenstein JM, Korolnek T, et al. Primary hepatocyte Culture supports hepatitis C virus replication: A model for infection-associated Hepatocarcinogenesis. Hepatology. 2010;51(6):1922–1932. doi: 10.1002/hep.23616
  • MASIARZ F LOS-Y, LAI MMC HWANGSB, J-H OU. Differential Subcellular Localization of hepatitis C virus Core gene products. Virology. 1995;213(2):455–461. doi: 10.1006/viro.1995.0018
  • Seo YL, Heo S, Jang KL. Hepatitis C virus core protein overcomes H2O2-induced apoptosis by downregulating p14 expression via DNA methylation. J Gen Virol. 2015;96(4):822–832. doi: 10.1099/vir.0.000032
  • Garcia-Ruiz C, Fernandez-Checa JC. Mitochondrial glutathione: hepatocellular survival–death switch. J Gastroenterol Hepatol. 2006;21(Suppl 3):3–6. doi: 10.1111/j.1440-1746.2006.04570.x
  • de la Rosa L C, Vrenken TE, Hannivoort RA, et al. Carbon monoxide blocks oxidative stress-induced hepatocyte apoptosis via inhibition of the p54 JNK isoform. Free Radic Biol Med. 2008;44(7):1323–1333. doi: 10.1016/j.freeradbiomed.2007.12.011
  • Geuken E, Buis C, Visser D, et al. Expression of heme oxygenase-1 in human livers before transplantation correlates with graft injury and function after transplantation. Am J Transpl. 2005;5(9):1875–1885. doi: 10.1111/j.1600-6143.2005.00960.x
  • Zhang M, An C, Gao Y, et al. Emerging roles of Nrf2 and phase II antioxidant enzymes in neuroprotection. Prog Neurobiol. 2013;100(1):30–47. doi: 10.1016/j.pneurobio.2012.09.003
  • Okuda M, Li K, Beard MR, et al. Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology. 2002;122(2):366–375. doi: 10.1053/gast.2002.30983
  • Gong G, Waris G, Tanveer R, Siddiqui A. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B. Proc Natl Acad Sci U S A. 2001;98(17):9599–9604. doi: 10.1073/pnas.171311298
  • Yao W, Cai H, Li X, et al. Endoplasmic reticulum stress Links hepatitis C virus RNA replication to Wild-Type PGC-1 a /liver-specific PGC-1 a Upregulation. J Virol. 2014;88(15):8361–8374. doi: 10.1128/JVI.01202-14
  • Paul D, Madan V, Bartenschlager R. Hepatitis C virus RNA replication and assembly : living on the Fat of the Land. Cell Host Microbe. 2014;16(5):569–579. doi: 10.1016/j.chom.2014.10.008
  • Tardif KD, Mori K, Siddiqui A. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an Intracellular Signaling pathway. J Virol. 2002;76(15):7453–7459. doi: 10.1128/JVI.76.15.7453-7459.2002
  • Lai C, Jeng K, Machida K, et al. Hepatitis C virus NS3 / 4A protein interacts with ATM, impairs DNA repair and enhances sensitivity to ionizing radiation. Virology. 2008;370(2):295–309. doi: 10.1016/j.virol.2007.08.037
  • Bansal R, Frelin L, Brenndörfer ED, et al. Hepatitis C virus nonstructural 3/4A protein dampens inflammation and contributes to slow fibrosis progression during chronic fibrosis in vivo. PLoS One. 2015;10(6):1–12. doi: 10.1371/journal.pone.0128466
  • Wang Y, Singh R, Xiang Y, et al. Macroautophagy and chaperone-mediated autophagy are required for hepatocyte resistance to oxidant stress. Hepatology. 2010;52(1):266–277. doi: 10.1002/hep.23645
  • Hou W, Han J, Lu C, et al. Autophagic degradation of active caspase-8 A crosstalk mechanism between autophagy and apoptosis autophagic degradation of active caspase-8. Autophagy. 2010;6(7):891–900. doi: 10.4161/auto.6.7.13038
  • Gao L, Gang L, Xianling G, et al. Activation of autophagy protects against cholestasis-induced hepatic injury. Cell Biosci. 2014;4(47):1–10.
  • Li S, Li J, Shen C, Zhang X, Sun S, Cho M, et al. Tert-butylhydroquinone (tBHQ) protects hepatocytes against lipotoxicity via inducing autophagy independently of Nrf2 activation. Biochim Biophys Acta. 2014;1841(1):22–33. doi: 10.1016/j.bbalip.2013.09.004