Unfolded protein response pathways regulate Hepatitis C virus replication via modulation of autophagy

Biochemical and Biophysical Research Communications

Volumn 432, Issue 2, 2013, Pages 326-332

  Shinohara, Yoshiyasu ^a,b   Imajo, Kento ^a   Yoneda, Masato ^a   Tomeno, Wataru ^a   Ogawa, Yuji ^a   Kirikoshi, Hiroyuki ^a   Funakoshi, Kengo ^b   Ikeda, Masanori ^b,c   Kato, Nobuyuki ^b,c   Nakajima, Atsushi ^a   Saito, Satoru ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c OKAYAMA UNIVERSITY   (Japan)

Author keywords

Autophagy; EIF2 alpha; Hepatitis C virus; JNK; Unfolding protein response; XBP 1

Indexed keywords

3 ETHOXY 5,6 DIBROMOSALICYLALDEHYDE; 3 METHYLADENINE; ALDEHYDE DERIVATIVE; ALPHA INTERFERON; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN IRE1; RAPAMYCIN; SALUBRINAL; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; AUTOPHAGY; CONTROLLED STUDY; GENOTYPE; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; REPLICON; UNFOLDED PROTEIN RESPONSE; VIRUS GENOME; VIRUS REPLICATION; VIRUS STRAIN;

AUTOPHAGY; CELL LINE, TUMOR; HEPACIVIRUS; HUMANS; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; VIRUS REPLICATION;

EUKARYOTA; HEPATITIS C VIRUS; RNA VIRUSES;

EID: 84875279443     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2013.01.103     Document Type: Article

References (38)

1. Hoofnagle J.H. Course and outcome of hepatitis C. Hepatology 2002, 36:21-29.
2. Rehermann B., Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 2005, 5:215-229.
3. Lohmann V., Körner F., Koch J., et al. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 1999, 285:110-113.
4. Blight K.J., Kolykhalov A.A., Rice C.M. Efficient initiation of HCV RNA replication in cell culture. Science 2000, 290:1972-1974.
5. Egger D., Wölk B., Gosert R., et al. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 2002, 76:5974-5984.
6. Gong G., Waris G., Tanveer R., et al. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kB. Proc. Natl. Acad. Sci. USA 2001, 98:9599-9604.
7. Tardif K.D., Mori K., Siddiqui A. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J. Virol. 2002, 76:7453-7459.
8. Ma Y., Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe?. Nat. Rev. Cancer 2004, 4:966-977.
9. Schr̈oder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
10. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
11. Lee A.H., Iwakoshi N.N., Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 2003, 23:7448-7459.
12. Wu J., Rutkowski D.T., Dubois M., et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 2007, 13:351-364.
13. Yamamoto K., Sato T., Matsui T., et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 2007, 13:365-376.
14. Ding W.X., Ni H.M., Gao W., et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am. J. Pathol. 2007, 171:513-524.
15. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
16. Shintani T., Klionsky D.J. Autophagy in health and disease: a double-edged sword. Science 2004, 306:990-995.
17. Dreux M., Chisari F.V. Viruses and the autophagy machinery. Cell Cycle 2010, 9:1295-1307.
18. 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:e24660.
19. Chan S.W., Egan P.A. Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J. 2005, 19:1510-1512.
20. Ke P.Y., Chen S.S. 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.
21. Li S., Ye L., Yu X., et al. Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 2009, 391:257-264.
22. Sir D., Chen W.L., Choi J., et al. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 2008, 48:1054-1061.
23. Ikeda M., Abe K., Dansako H., et al. Efficient replication of a full-length hepatitis C virus genome, strain O, in cell culture, and development of a luciferase reporter system. Biochem. Biophys. Res. Commun. 2005, 329:1350-1359.
24. Kato N., Sugiyama K., Namba K., et al. Establishment of a hepatitis C virus subgenomic replicon derived from human hepatocytes infected in vitro. Biochem. Biophys. Res. Commun. 2003, 306:756-766.
25. Mori K., Ikeda M., Ariumi Y., et al. Mechanism of action of ribavirin in a novel hepatitis C virus replication cell system. Virus Res. 2011, 151:61-70.
26. Stiffler J.D., Nguyen M., Sohn J.A., et al. Focal distribution of hepatitis C virus RNA in infected livers. PLoS One 2009, 4:e6661.
27. Mizushima N. Methods for monitoring autophagy. Int. J. Biochem. Cell Biol. 2004, 36:2491-2502.
28. Boyce M., Bryant K.F., Jousse C., et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 2005, 307:935-939.
29. Volkmann K., Lucas J.L., Vuga D., et al. Potent and selective inhibitors of the inositol-requiring enzyme 1 endoribonuclease. J. Biol. Chem. 2011, 286:12743-12755.
30. 2-terminal kinase/extracellular signal-regulated kinase activation in WI38 lung epithelial fibroblast cells. J. Pharmacol. Exp. Ther. 2009, 329:112-122.
31. Tardif K.D., Mori K., Kaufman R.J., et al. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 2004, 279:17158-17164.
32. Jackson W.T., Giddings T.H., Taylor M.P., et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005, 3:e156.
33. Prentice E., Jerome W.G., Yoshimori T., et al. Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 2004, 279:10136-10141.
34. Kouroku Y., Fujita E., Tanida I., et al. ER stress (PERK/eIF2α phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 2007, 14:230-239.
35. Ogata M., Hino S., Saito A., et al. Autophagy is activated for cell survival after endoplasmic reticulum stress, Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell. Biol. 2006, 26:9220-9231.
36. Yamamoto K., Yoshida H., Kokame K., Kaufman R.J., et al. Differential contributions of ATF6 and XBP1 in activating endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J. Biochem. 2004, 136:343-350.
37. Yoshida H., Matsui T., Hosokawa N., et al. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 2003, 4:265-271.
38. Lin J.H., Li H., Yasumura D., et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007, 318:944-949.