Activation of the Ras/Raf/MEK pathway facilitates hepatitis C virus replication via attenuation of the interferon-JAK-STAT pathway

Journal of Virology

Volumn 86, Issue 3, 2012, Pages 1544-1554

  Zhang, Qi ^a,b   Gong, Rui ^a,b   Qu, Jing ^a,b   Zhou, Yijing ^a   Liu, Weiyong ^a   Chen, Mingzhou ^a   Liu, Yingle ^a,b   Zhu, Ying ^a,b   Wu, Jianguo ^a,b  

^a ZHONGNAN HOSPITAL OF WUHAN UNIVERSITY   (China)

^b Centre for Biomedicine Research   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON RECEPTOR; ALPHA INTERFERON RECEPTOR 1; ALPHA INTERFERON RECEPTOR 2; BETA INTERFERON RECEPTOR; BETA INTERFERON RECEPTOR 1; BETA INTERFERON RECEPTOR 2; INTERFERON; INTERFERON RECEPTOR; JANUS KINASE; OMEGA INTERFERON RECEPTOR 1; OMEGA INTERFERON RECEPTOR 2; STAT PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENETIC CORRELATION; HEPATITIS C; HEPATITIS C VIRUS; MARKER GENE; MEK GENE; NONHUMAN; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAF GENE; VIRUS INHIBITION; VIRUS REPLICATION;

BASE SEQUENCE; CELL LINE; DNA PRIMERS; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; HEPACIVIRUS; HUMANS; INTERFERONS; JANUS KINASES; PHOSPHORYLATION; PROTEIN KINASES; REAL-TIME POLYMERASE CHAIN REACTION; STAT TRANSCRIPTION FACTORS; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 84863158653     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00688-11     Document Type: Article

References (74)

1. Akula SM, et al. 2004. Raf promotes human herpesvirus-8 (HHV-8/ KSHV) infection. Oncogene 23:5227-5241.
2. Aoki H, Hayashi J, Moriyama M, Arakawa Y, Hino O. 2000. Hepatitis C virus core protein interacts with 14-3-3 protein and activates the kinase Raf-1. J. Virol. 74:1736-1741.
3. Balmain A, Pragnell IB. 1983. Mouse skin carcinomas induced in vivo by chemical carcinogens have a transforming Harvey-ras oncogene. Nature 303:72-74.
4. Barber SA, et al. 2002. Visna virus-induced activation of MAPK is required for virus replication and correlates with virus-induced neuropathology. J. Virol. 76:817- 828.
5. Battcock SM, Collier TW, Zu D, Hirasawa K. 2006. Negative regulation of the alpha interferon-induced antiviral response by the Ras/Raf/MEK pathway. J. Virol. 80:4422- 4430.
6. Blight KJ, Kolykhalov AA, Rice CM. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-1974.
7. Bode JG, et al. 2003. IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. FASEB J. 17: 488-490.
8. Bonjardim CA, Ferreira PC, Kroon EG. 2009. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 122:1-11.
9. Bruder JT, Heidecker G, Rapp UR. 1992. Serum-, TPA-, and Rasinduced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase. Genes Dev. 6:545-556.
10. Campbell SL, Khosravi-Far R, Rossman KL, Clark GJ, Der CJ. 1998. Increasing complexity of Ras signaling. Oncogene 17:1395-1413.
11. Chambers TJ, et al. 2005. Quasispecies heterogeneity within the E1/E2 region as a pretreatment variable during pegylated interferon therapy of chronic hepatitis C virus infection. J. Virol. 79:3071-3083.
12. Christian SL, et al. 2009. Activated Ras/MEK inhibits the antiviral response of alpha interferon by reducing STAT2 levels. J. Virol. 83: 6717-6726.
13. Cobb MH. 1999. MAP kinase pathways. Prog. Biophys. Mol. Biol. 71: 479-500.
14. Darnell JE, Jr, Kerr IM, Stark GR. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1421.
15. Di Bisceglie, AM. 1997. Hepatitis C and hepatocellular carcinoma. Hepatology 26:34S-38S.
16. Dondi E, et al. 2001. Down-modulation of type 1 interferon responses by receptor cross-competition for a shared Jak kinase. J. Biol. Chem. 276: 47004-47012.
17. Duong FH, Filipowicz M, Tripodi M, La Monica N, Heim MH. 2004. Hepatitis C virus inhibits interferon signaling through up-regulation of protein phosphatase 2A. Gastroenterology 126:263-277.
18. Enomoto N, et al. 1996. Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N. Engl. J. Med. 334:77- 81.
19. Erhardt A, Hassan M, Heintges T, Haussinger D. 2002. 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 292:272-284.
20. Foy E, et al. 2005. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc. Natl. Acad. Sci. U. S. A. 102:2986 -2991.
21. Foy E, et al. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300:1145-1148.
22. Frese M, Pietschmann T, Moradpour D, Haller O, Bartenschlager R. 2001. Interferon-alpha inhibits hepatitis C virus subgenomic RNA replication by an MxA-independent pathway. J. Gen. Virol. 82:723-733.
23. Giambartolomei S, Covone F, Levrero M, Balsano C. 2001. Sustained activation of the Raf/MEK/Erk pathway in response to EGF in stable cell lines expressing the hepatitis C virus (HCV) core protein. Oncogene 20: 2606-2610.
24. Gretton S, Hughes M, Harris M. 2010. Hepatitis C virus RNA replication is regulated by Ras-Erk signalling. J. Gen. Virol. 91:671- 680.
25. Guo JT, Bichko VV, Seeger C. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-8523.
26. Han JQ, Barton DJ. 2002. Activation and evasion of the antiviral 2′-5′ oligoadenylate synthetase/ribonuclease L pathway by hepatitis C virus mRNA. RNA 8:512-525.
27. Hoshino R, et al. 1999. Constitutive activation of the 41-/43-kDa mitogen-activated protein kinase signaling pathway in human tumors. Oncogene 18:813- 822.
28. Houghton M, Weiner A, Han J, Kuo G, Choo QL. 1991. Molecular biology of the hepatitis C viruses: implications for diagnosis, development and control of viral disease. Hepatology 14:381-388.
29. Huang Y, et al. 2006. Mechanistic link between the anti-HCV effect of interferon gamma and control of viral replication by a Ras-MAPK signaling cascade. Hepatology 43:81-90.
30. Huber M, et al. 1999. Cleavage of RasGAP and phosphorylation of mitogen-activated protein kinase in the course of coxsackievirus B3 replication. J. Virol. 73:3587-3594.
31. Kamata H, et al. 1996. Suppression of nerve growth factor-induced neuronal differentiation of PC12 cells. N-acetylcysteine uncouples the signal transduction from ras to the mitogen-activated protein kinase cascade. J. Biol. Chem. 271:33018 -33025.
32. Klampfer L, et al. 2003. Oncogenic Ki-ras inhibits the expression of interferon-responsive genes through inhibition of STAT1 and STAT2 expression. J. Biol. Chem. 278:46278-46287.
33. Krieger N, Lohmann V, Bartenschlager R. 2001. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J. Virol. 75:4614-4624.
34. Kumar KG, Krolewski JJ, Fuchs SY. 2004. Phosphorylation and specific ubiquitin acceptor sites are required for ubiquitination and degradation of the IFNAR1 subunit of type I interferon receptor. J. Biol. Chem. 279: 46614-46620.
35. Kumar KG, et al. 2007. Raf inhibitor stabilizes receptor for the type I interferon but inhibits its anti-proliferative effects in human malignant melanoma cells. Cancer Biol. Ther. 6:1437-1441.
36. Kumar KG, et al. 2003. SCF(HOS) ubiquitin ligase mediates the ligandinduced down-regulation of the interferon-alpha receptor. EMBO J. 22: 5480-5490.
37. Kuo G, et al. 1989. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 244:362-364.
38. Lauer GM, Walker BD. 2001. Hepatitis C virus infection. N. Engl. J. Med. 345:41-52.
39. Lindenbach BD, et al. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626.
40. Liu J, et al. 2009. Mammalian casein kinase 1alpha and its leishmanial ortholog regulate stability of IFNAR1 and type I interferon signaling. Mol. Cell. Biol. 29:6401-6412.
41. Liu WL, et al. 2007. Ribavirin up-regulates the activity of doublestranded RNA-activated protein kinase and enhances the action of interferon-alpha against hepatitis C virus. J. Infect. Dis. 196:425-434.
42. Lohmann V, et al. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113.
43. Macdonald A, et al. 2003. The hepatitis C virus non-structural NS5A protein inhibits activating protein-1 function by perturbing ras-ERK pathway signaling. J. Biol. Chem. 278:17775-17784.
44. Mischiati C, et al. 1999. Extracellular HIV-1 Tat protein differentially activates the JNK and ERK/MAPK pathways in CD4 T cells. AIDS 13: 1637-1645.
45. Moradpour D, Blum HE. 1999. Current and evolving therapies for hepatitis C. Eur. J. Gastroenterol. Hepatol. 11:1199-1202.
46. Mundschau LJ, Faller DV. 1992. Oncogenic ras induces an inhibitor of double-stranded RNA-dependent eukaryotic initiation factor 2 alphakinase activation. J. Biol. Chem. 267:23092-23098.
47. Murakami T, et al. 1999. Mutations in nonstructural protein 5A gene and response to interferon in hepatitis C virus genotype 2 infection. Hepatology 30:1045-1053.
48. Noser JA, et al. 2007. The RAS/Raf1/MEK/ERK signaling pathway facilitates VSV-mediated oncolysis: implication for the defective interferon response in cancer cells. Mol. Ther. 15:1531-1536.
49. Pawlotsky JM. 2004. Pathophysiology of hepatitis C virus infection and related liver disease. Trends Microbiol. 12:96-10.
50. Penin F, Dubuisson J, Rey FA, Moradpour D, Pawlotsky JM. 2004. Structural biology of hepatitis C virus. Hepatology 39:5-19.
51. Planz O, Pleschka S, Ludwig S. 2001. MEK-specific inhibitor U0126 blocks spread of Borna disease virus in cultured cells. J. Virol. 75: 4871-4877.
52. Pleschka S, et al. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nature Cell Biol. 3:301-305.
53. Randall G, et al. 2007. Cellular cofactors affecting hepatitis C virus infection and replication. Proc. Natl. Acad. Sci. U. S. A. 104:12884-12889.
54. Robertson B, et al. 1998. Classification, nomenclature, and database development for hepatitis C virus (HCV) and related viruses: proposals for standardization. Arch. Virol. 143:2493-2503.
55. Robinson MJ, Stippec SA, Goldsmith E, White MA, Cobb MH. 1998. A constitutively active and nuclear form of the MAP kinase ERK2 is sufficient for neurite outgrowth and cell transformation. Curr. Biol. 8:1141-1150.
56. Saito I, et al. 1990. Hepatitis C virus infection is associated with the development of hepatocellular carcinoma. Proc. Natl. Acad. Sci. U. S. A. 87:6547-6549.
57. Schindler C. 1999. Cytokines and JAK-STAT signaling. Exp. Cell Res. 253:7-14.
58. Schmitz KJ, et al. 2008. Activation of the ERK and AKT signalling pathway predicts poor prognosis in hepatocellular carcinoma and ERK activation in cancer tissue is associated with hepatitis C virus infection. J. Hepatol. 48:83-90.
59. Scholl FA, Dumesic PA, Khavari PA. 2005. Effects of active MEK1 expression in vivo. Cancer Lett. 230:1-5.
60. Scholle F, et al. 2004. Virus-host cell interactions during hepatitis C virus RNA replication: impact of polyprotein expression on the cellular transcriptome and cell cycle association with viral RNA synthesis. J. Virol. 78:1513-1524.
61. Shields JM, Pruitt K, McFall A, Shaub A, Der CJ. 2000. Understanding Ras: 'it ain't over 'til it's over.' Trends Cell Biol. 10:147-154.
62. Sumpter R, Jr, et al. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
63. Taguchi T, et al. 2004. Hepatitis C virus NS5A protein interacts with 2′,5′-oligoadenylate synthetase and inhibits antiviral activity of IFN in an IFN sensitivity-determining region-independent manner. J. Gen. Virol. 85:959 -969.
64. Tan SL, et al. 1999. NS5A, a nonstructural protein of hepatitis C virus, binds growth factor receptor-bound protein 2 adaptor protein in a Src homology 3 domain/ligand-dependent manner and perturbs mitogenic signaling. Proc. Natl. Acad. Sci. U. S. A. 96:5533-5538.
65. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285:107-110.
66. Tokumoto Y, et al. 2007. Hepatitis C virus expression and interferon antiviral action is dependent on PKR expression. J. Med. Virol. 79: 1120-1127.
67. Tscherne DM, et al. 2006. Time- and temperature-dependent activation of hepatitis C virus for low-pH-triggered entry. J. Virol. 80:1734 -1741.
68. Wakita T, et al. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791-796.
69. Wang C, et al. 2003. Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J. Virol. 77: 3898-3912.
70. Wang SH, et al. 2008. Natural killer cells suppress full cycle HCV infection of human hepatocytes. J. Viral Hepat. 15:855-864.
71. Washenberger CL, et al. 2007. Hepatitis C virus RNA: dinucleotide frequencies and cleavage by RNase L. Virus Res. 130:85-95.
72. Yeh TC, Dondi E, Uze G, Pellegrini S. 2000. A dual role for the kinaselike domain of the tyrosine kinase Tyk2 in interferon-alpha signaling. Proc. Natl. Acad. Sci. U. S. A. 97:8991-8996.
73. Zhao LJ, et al. 2005. Hepatitis C virus E2 protein promotes human hepatoma cell proliferation through the MAPK/ERK signaling pathway via cellular receptors. Exp. Cell Res. 305:23-32.
74. Zhao LJ, et al. 2006. 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. 80:424-432.