HCV induces transforming growth factor β1 through activation of endoplasmic reticulum stress and the unfolded protein response

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Chusri, Pattranuch ^a,b   Kumthip, Kattareeya ^a,b   Hong, Jian ^a   Zhu, Chuanlong ^a,c   Duan, Xiaoqiong ^a,d   Jilg, Nikolaus ^a   Fusco, Dahlene N ^a   Brisac, Cynthia ^a   Schaefer, Esperance A ^a   Cai, Dachuan ^a,e   Peng, Lee F ^a   Maneekarn, Niwat ^b   Lin, Wenyu ^a   Chung, Raymond T ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Faculty of Medicine Chiang Mai University   (Thailand)

^c THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^d INSTITUTE OF BLOOD TRANSFUSION   (China)

^e THE SECOND AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ATF6 PROTEIN, HUMAN; EIF2AK3 PROTEIN, HUMAN; ERN1 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN KINASE R; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; RIBONUCLEASE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA1;

ANTAGONISTS AND INHIBITORS; ENDOPLASMIC RETICULUM STRESS; GENETICS; HEPACIVIRUS; HUMAN; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; RNA INTERFERENCE; TUMOR CELL LINE; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 6; CELL LINE, TUMOR; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; HEPACIVIRUS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSFORMING GROWTH FACTOR BETA1; UNFOLDED PROTEIN RESPONSE;

EID: 84959467728     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22487     Document Type: Article

References (32)

1. Alter, H. J. & Seeff, L. B. Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin Liver Dis 20, 17-35 (2000).
2. Lin, W., Weinberg, E. M. & Chung, R. T. Pathogenesis of accelerated fibrosis in HIV/HCV co-infection. J Infect Dis 207 Suppl 1, S13-18, doi: 10.1093/infdis/jis926 (2013).
3. Dubuisson, J., Penin, F. & Moradpour, D. Interaction of hepatitis C virus proteins with host cell membranes and lipids. Trends Cell Biol 12, 517-523 (2002).
4. Cocquerel, L., Meunier, J. C., 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 72, 2183-2191 (1998).
5. Egger, D. et al. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76, 5974-5984 (2002).
6. Gretton, S. N., Taylor, A. I. & McLauchlan, J. Mobility of the hepatitis C virus NS4B protein on the endoplasmic reticulum membrane and membrane-associated foci. J Gen Virol 86, 1415-1421, doi: 10.1099/vir.0.80768-0 (2005).
7. Bartenschlager, R., Frese, M. & Pietschmann, T. Novel insights into hepatitis C virus replication and persistence. Adv Virus Res 63, 71-180, doi: 10.1016/S0065-3527(04)63002-8 (2004).
8. Kapadia, S. B. & Chisari, F. V. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc Natl Acad Sci USA 102, 2561-2566, doi: 10.1073/pnas.0409834102 (2005).
9. Tardif, K. D., Mori, K. & Siddiqui, A. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J Virol 76, 7453-7459 (2002).
10. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8, 519-529, doi: 10.1038/nrm2199 (2007).
11. Ye, J. et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6, 1355-1364 (2000).
12. Mori, K. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101, 451-454 (2000).
13. Shamu, C. E. & Walter, P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J 15, 3028-3039 (1996).
14. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. & Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891 (2001).
15. Harding, H. P., Zhang, Y. & Ron, D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274, doi: 10.1038/16729 (1999).
16. Raven, J. F. & Koromilas, A. E. PERK and PKR: old kinases learn new tricks. Cell Cycle 7, 1146-1150 (2008).
17. Bissell, D. M., Roulot, D. & George, J. Transforming growth factor beta and the liver. Hepatology 34, 859-867, doi: 10.1053/jhep.2001.28457 (2001).
18. Nelson, D. R. et al. Transforming growth factor-beta 1 in chronic hepatitis C. J Viral Hepat 4, 29-35 (1997).
19. Grungreiff, K., Reinhold, D. & Ansorge, S. Serum concentrations of sIL-2R, IL-6, TGF-beta1, neopterin, and zinc in chronic hepatitis C patients treated with interferon-alpha. Cytokine 11, 1076-1080, doi: 10.1006/cyto.1999.0504 (1999).
20. Taniguchi, H. et al. Hepatitis C virus core protein upregulates transforming growth factor-beta 1 transcription. J Med Virol 72, 52-59, doi: 10.1002/jmv.10545 (2004).
21. Presser, L. D., Haskett, A. & Waris, G. Hepatitis C virus-induced furin and thrombospondin-1 activate TGF-beta1: role of TGFbeta1 in HCV replication. Virology 412, 284-296, doi: 10.1016/j.virol.2010.12.051 (2011).
22. Lin, W. et al. Hepatitis C virus regulates transforming growth factor beta1 production through the generation of reactive oxygen species in a nuclear factor kappaB-dependent manner. Gastroenterology 138, 2509-2518, 2518 e2501, doi: 10.1053/j. gastro.2010.03.008 (2010).
23. Lin, W. et al. HIV and HCV cooperatively promote hepatic fibrogenesis via induction of reactive oxygen species and NFkappaB. J Biol Chem 286, 2665-2674, doi: 10.1074/jbc.M110.168286 (2011).
24. Waris, G. & Siddiqui, A. Regulatory mechanisms of viral hepatitis B and C. J Biosci 28, 311-321 (2003).
25. Rossmanith, W. & Schulte-Hermann, R. Biology of transforming growth factor beta in hepatocarcinogenesis. Microsc Res Tech 52, 430-436, doi: 10.1002/1097-0029(20010215)52:4<430::AID-JEMT1028>3.0.CO; 2-3 (2001).
26. Sir, D. et al. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48, 1054-1061, doi: 10.1002/hep.22464 (2008).
27. Tardif, K. D., Waris, G. & Siddiqui, A. Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol 13, 159-163, doi: 10.1016/j. tim.2005.02.004 (2005).
28. Kumthip, K. et al. Hepatitis C virus NS5A disrupts STAT1 phosphorylation and suppresses type I interferon signaling. J Virol 86, 8581-8591, doi: 10.1128/JVI.00533-12 (2012).
29. Lin, W. et al. The spliceosome factor SART1 exerts its anti-HCV action through mRNA splicing. J Hepatol 62, 1024-1032, doi: 10.1016/j.jhep.2014.11.038 (2015).
30. Zhu, C. et al. EFTUD2 Is a Novel Innate Immune Regulator Restricting Hepatitis C Virus Infection through the RIG-I/MDA5 Pathway. J Virol 89, 6608-6618, doi: 10.1128/JVI.00364-15 (2015).
31. Lin, W. et al. Hepatitis C virus expression suppresses interferon signaling by degrading STAT1. Gastroenterology 128, 1034-1041 (2005).
32. Lin, W. et al. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J Virol 80, 9226-9235, doi: 10.1128/JVI.00459-06 (2006).