Interferon alpha and ribavirin collaboratively regulate p38 mitogen-activated protein kinase signaling in hepatoma cells

Cytokine

Volumn 61, Issue 3, 2013, Pages 801-807

  He, Sheng Fei ^a   Wang, Wen ^a   Ren, Hao ^a   Zhao, Lan Juan ^a   Qi, Zhong Tian ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

HCV; Hepatoma cells; IFN ; P38 MAPK; Ribavirin

Indexed keywords

ALPHA INTERFERON; INTERFERON RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE P38; RIBAVIRIN; SMALL INTERFERING RNA; TYPE 1 INTERFERON RECEPTOR 2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DRUG SYNERGISM; HEPACIVIRUS; HUMANS; INTERFERON-ALPHA; LIVER NEOPLASMS; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECEPTOR, INTERFERON ALPHA-BETA; RIBAVIRIN; RNA, SMALL INTERFERING; TRANSFECTION;

HEPATITIS C VIRUS;

EID: 84875378152     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2013.01.007     Document Type: Article

References (41)

1. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., Schreiber R.D. How cells respond to interferons. Annu Rev Biochem 1998, 67:227-264.
2. Platanias L.C., Fish E.N. Signaling pathways activated by interferons. Exp Hematol 1999, 27:1583-1592.
3. van Boxel-Dezaire A.H., Rani M.R., Stark G.R. Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 2006, 25:361-372.
4. de Weerd N.A., Samarajiwa S.A., Hertzog P.J. Type 1 interferon receptors: biochemistry and biological functions. J Biol Chem 2007, 282:20053-20057.
5. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005, 5:375-386.
6. Feld J.J., Hoofnagle J.H. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005, 436:967-972.
7. Fried M.W., Shiffman M.L., Reddy K.R., Smith C., Marinos G., Gonçales F.L., et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002, 347:975-982.
8. Avolio S., Summa V. Advances in the development of macrocyclic inhibitors of hepatitis C virus NS3-4A protease. Curr Top Med Chem 2010, 10:1403-1422.
9. Erhardt A., Hassan M., Heintges T., Häussinger D. Hepatitis C virus core protein induces cell proliferation and activates ERK, JNK, and p38 MAP kinases together with the MAP kinase phosphatase MKP-1 in a HepG2 Tet-Off cell line. Virology 2002, 292:272-284.
10. Tsutsumi T., Suzuki T., Moriya K., Shintani Y., Fujie H., Miyoshi H., et al. Hepatitis C virus core protein activates ERK and p38 MAPK in cooperation with ethanol in transgenic mice. Hepatology 2003, 38:820-828.
11. Sundström S., Ota S., Dimberg L.Y., Masucci M.G., Bergqvist A. Hepatitis C virus core protein induces an anergic state characterized by decreased interleukin-2 production and perturbation of mitogen-activated protein kinase responses. J Virol 2005, 79:2230-2239.
12. Moorman J.P., Fitzgerald S.M., Prayther D.C., Lee S.A., Chi D.S., Krishnaswamy G. Induction of p38- and gC1qR-dependent IL-8 expression in pulmonary fibroblasts by soluble hepatitis C core protein. Respir Res 2005, 6:105.
13. Hassan M., Selimovic D., Ghozlan H., Abdel-kader O. Hepatitis C virus core protein triggers hepatic angiogenesis by a mechanism including multiple pathways. Hepatology 2009, 49:1469-1482.
14. Yang S.H., Lee C.G., Lee C.W., Choi E.J., Yoon S.K., Ahn K.S., et al. Hepatitis C virus core inhibits the Fas-mediated p38 mitogen activated kinase signaling pathway in hepatocytes. Mol Cells 2002, 13:452-462.
15. Balasubramanian A., Ganju R.K., Groopman J.E. Hepatitis C virus and HIV envelope proteins collaboratively mediate interleukin-8 secretion through activation of p38 MAP kinase and SHP2 in hepatocytes. J Biol Chem 2003, 278:35755-35766.
16. Zhao L.J., Zhang X.L., Zhao P., Cao J., Cao M.M., Zhu S.Y., et al. Up-regulation of ERK and p38 MAPK signaling pathways by hepatitis C virus E2 envelope protein in human T lymphoma cell line. J Leukoc Biol 2006, 80:424-432.
17. Chen Q.L., Zhu S.Y., Bian Z.Q., Zhao L.J., Cao J., Pan W., et al. Activation of p38 MAPK pathway by hepatitis C virus E2 in cells transiently expressing DC-SIGN. Cell Biochem Biophys 2010, 56:49-58.
18. Serti E., Doumba P.P., Thyphronitis G., Tsitoura P., Katsarou K., Foka P., et al. Modulation of IL-2 expression after uptake of hepatitis C virus non-enveloped capsid-like particles: the role of p38 kinase. Cell Mol Life Sci 2011, 68:505-522.
19. Felger J.C., Alagbe O., Pace T.W., Woolwine B.J., Hu F., Raison C.L., et al. Early activation of p38 mitogen activated protein kinase is associated with interferon-alpha-induced depression and fatigue. Brain Behav Immun 2011, 25:1094-1098.
20. Coenen M., Nischalke H.D., Krämer B., Langhans B., Glässner A., Schulte D., et al. Hepatitis C virus core protein induces fibrogenic actions of hepatic stellate cells via toll-like receptor 2. Lab Invest 2011, 91:1375-1382.
21. Alisi A., Ghidinelli M., Zerbini A., Missale G., Balsano C. Hepatitis C virus and alcohol: same mitotic targets but different signaling pathways. J Hepatol 2011, 54:956-963.
22. George A., Panda S., Kudmulwar D., Chhatbar S.P., Nayak S.C., Krishnan H.H. Hepatitis C virus NS5A binds to the mRNA cap-binding eukaryotic translation initiation 4F (eIF4F) complex and up-regulates host translation initiation machinery through eIF4E-binding protein 1 inactivation. J Biol Chem 2012, 287:5042-5058.
23. Zhao L.J., Hua X., He S.F., Ren H., Qi Z.T. Interferon alpha regulates MAPK and STAT1 pathways in human hepatoma cells. Virol J 2011, 8:157.
24. Zhong J., Gastaminza P., Cheng G., Kapadia S., Kato T., Burton D.R., et al. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 2005, 102:9294-9299.
25. Tong Y., Zhu Y., Xia X., Liu Y., Feng Y., Hua X., et al. Tupaia CD81, SR-BI, Claudin-1, and Occludin support hepatitis C virus infection. J Virol 2011, 85:2793-2802.
26. Zhao L.J., Wang W., Liu Y., Ren H., Qi Z.T. Interference with ERK and STAT signaling pathways and inhibition of hepatitis C virus replication by ribavirin. Antiviral Res 2012, 96:260-268.
27. Bode J.G., Ludwig S., Ehrhardt C., Albrecht U., Erhardt A., Schaper F., et al. IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. FASEB J 2003, 17:488-490.
28. Zhou Z., Hamming O.J., Ank N., Paludan S.R., Nielsen A.L., Hartmann R. Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the Jak-STAT pathway and the mitogen-activated protein kinases. J Virol 2007, 81:7749-7758.
29. Kim S.H., Chun S.Y., Kim T.S. Interferon-alpha enhances artemisinin-induced differentiation of HL-60 leukemia cells via a PKC alpha/ERK pathway. Eur J Pharmacol 2008, 587:65-72.
30. Ogbomo H, Michaelis M, Altenbrandt B, Doerr HW, Cinatl JJr. A novel immunomodulatory mechanism of ribavirin in suppressing natural killer cell function. Biochem Pharmacol 2010;79:188-97.
31. Vallée S., Fouchier F., Braguer D., Marvaldi J., Champion S. Ribavirin-induced resistance to heat shock, inhibition of the Ras-Raf-1 pathway and arrest in G(1). Eur J Pharmacol 2000, 404:49-62.
32. Thomas E., Feld J.J., Li Q., Hu Z., Fried M.W., Liang T.J. Ribavirin potentiates interferon action by augmenting interferon-stimulated gene induction in hepatitis C virus cell culture models. Hepatology 2011, 53:32-41.
33. Uddin S., Majchrzak B., Woodson J., Arunkumar P., Alsayed Y., Pine R., et al. Activation of the p38 mitogen-activated protein kinase by type I interferons. J Biol Chem 1999, 274:30127-30131.
34. Chan E.D., Winston B.W., Uh S.T., Wynes M.W., Rose D.M., Riches D.W. Evaluation of the role of mitogen-activated protein kinases in the expression of inducible nitric oxide synthase by IFN-gamma and TNF-alpha in mouse macrophages. J Immunol 1999, 162:415-422.
35. Blank V.C., Peña C., Roguin L.P. STAT1, STAT3 and p38MAPK are involved in the apoptotic effect induced by a chimeric cyclic interferon-alpha2b peptide. Exp Cell Res 2010, 316:603-614.
36. Krebs D.L., Hilton D.J. SOCS proteins: negative regulators of cytokine signaling. Stem Cells 2001, 19:378-387.
37. Marcello T., Grakoui A., Barba-Spaeth G., Machlin E.S., Kotenko S.V., MacDonald M.R., et al. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 2006, 131:1887-1898.
38. Ishida H., Ohkawa K., Hosui A., Hiramatsu N., Kanto T., Ueda K., et al. Involvement of p38 signaling pathway in interferon-alpha-mediated antiviral activity toward hepatitis C virus. Biochem Biophys Res Commun 2004, 321:722-727.
39. Zhang Y., Jamaluddin M., Wang S., Tian B., Garofalo R.P., Casola A., et al. Ribavirin treatment up-regulates antiviral gene expression via the interferon-stimulated response element in respiratory syncytial virus-infected epithelial cells. J Virol 2003, 77:5933-5947.
40. Su W.C., Liu W.L., Cheng C.W., Chou Y.B., Hung K.H., Huang W.H., et al. Ribavirin enhances interferon signaling via stimulation of mTOR and p53 activities. FEBS Lett 2009, 583:2793-2798.
41. Simone O., Tortorella C., Zaccaro B., Napoli N., Antonaci S. Impairment of TLR7-dependent signaling in dendritic cells from chronic hepatitis C virus (HCV)-infected non-responders to interferon/ribavirin therapy. J Clin Immunol 2010, 30:556-565.