Activated Ras/MEK inhibits the antiviral response of alpha interferon by reducing STAT2 levels

Journal of Virology

Volumn 83, Issue 13, 2009, Pages 6717-6726

  Christian, Sherri L ^a   Collier, Thaddeus W ^a   Zu, Dong ^a   Licursi, Maria ^a   Hough, Chris M ^a   Hirasawa, Kensuke ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ALPHA [AMINO(4 AMINOPHENYLTHIO)METHYLENE] 2 (TRIFLUOROMETHYL)PHENYLACETONITRILE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; COMPLEMENTARY DNA; CYCLOHEXIMIDE; DACTINOMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; RAS PROTEIN; RECOMBINANT ALPHA INTERFERON; RECOMBINANT GAMMA INTERFERON; RNA; STAT2 PROTEIN; UO 126; ALPHA INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE KINASE; STAT1 PROTEIN; STAT1 PROTEIN, MOUSE; STAT2 PROTEIN, MOUSE;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIRUS INFECTION; VIRUS INHIBITION; VIRUS REPLICATION; WESTERN BLOTTING; ANIMAL; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MOUSE; PHOSPHORYLATION; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS;

ANIMALS; DOWN-REGULATION; GENE EXPRESSION REGULATION; INTERFERON-ALPHA; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NIH 3T3 CELLS; PHOSPHORYLATION; RAS PROTEINS; STAT1 TRANSCRIPTION FACTOR; STAT2 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; VESICULAR STOMATITIS; VESICULAR STOMATITIS INDIANA VIRUS;

EID: 67449083795     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02213-08     Document Type: Article

References (52)

1. Balachandran, S., M. Porosnicu, and G. N. Barber. 2001. Oncolytic activity of vesicular stomatitis virus is effective against tumors exhibiting aberrant p53, Ras, or myc function and involves the induction of apoptosis. J. Virol. 75:3474-3479. (Pubitemid 32225911)
2. Barber, S. A., L. Bruett, B. R. Douglass, D. S. Herbst, M. C. Zink, and J. E. Clements. 2002. Visna virus-induced activation of MAPK is required for virus replication and correlates with virus-induced neuropathology. J. Virol. 76:817-828. (Pubitemid 34033379)
3. Battcock, S. M., T. W. Collier, D. Zu, and K. Hirasawa. 2006. Negative regulation of the alpha interferon-induced antiviral response by the Ras/Raf/MEK pathway. J. Virol. 80:4422-4430.
4. Bergmann, M., I. Romirer, M. Sachet, R. Fleischhacker, A. Garcia-Sastre, P. Palese, K. Wolff, H. Pehamberger, R. Jakesz, and T. Muster. 2001. A genetically engineered influenza A virus with ras-dependent oncolytic properties. Cancer Res. 61:8188-8193. (Pubitemid 33091611)
5. Briken, V., H. Ruffner, U. Schultz, A. Schwarz, L. F. Reis, I. Strehlow, T. Decker, and P. Staeheli. 1995. Interferon regulatory factor 1 is required for mouse Gbp gene activation by gamma interferon. Mol. Cell. Biol. 15:975-982.
6. Campbell, S. L., R. Khosravi-Far, K. L. Rossman, G. J. Clark, and C. J. Der. 1998. Increasing complexity of Ras signaling. Oncogene 17:1395-1413. (Pubitemid 28458409)
7. Cascalló, M., G. Capella, A. Mazo, and R. Alemany. 2003. Ras-dependent oncolysis with an adenovirus VAI mutant. Cancer Res. 63:5544-5550. (Pubitemid 37139876)
8. Croker, B. A., H. Kiu, and S. E. Nicholson. 2008. SOCS regulation of the JAK/STAT signalling pathway. Semin. Cell Dev. Biol. 19:414-422.
9. Davie, J. R., and V. A. Spencer. 2001. Signal transduction pathways and the modification of chromatin structure. Prog. Nucleic Acid Res. Mol. Biol. 65:299-340.
10. Der, S. D., A. Zhou, B. R. Williams, and R. H. Silverman. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 95:15623-15628.
11. Dhillon, A. S., S. Hagan, O. Rath, and W. Kolch. 2007. MAP kinase signalling pathways in cancer. Oncogene 26:3279-3290. (Pubitemid 46763021)
12. Farassati, F., A. D. Yang, and P. W. Lee. 2001. Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat. Cell Biol. 3:745-750.
13. Farrar, J. D., J. D. Smith, T. L. Murphy, S. Leung, G. R. Stark, and K. M. Murphy. 2000. Selective loss of type I interferon-induced STAT4 activation caused by a minisatellite insertion in mouse Stat2. Nat. Immunol. 1:65-69.
14. Fu, X. Y., D. S. Kessler, S. A. Veals, D. E. Levy, and J. E. Darnell, Jr. 1990. ISGF3, the transcriptional activator induced by interferon alpha, consists of multiple interacting polypeptide chains. Proc. Natl. Acad. Sci. USA 87:8555-8559.
15. García-Sastre, A. 2002. Mechanisms of inhibition of the host interferon alpha/beta-mediated antiviral responses by viruses. Microbes. Infect. 4:647-655.
16. Grandvaux, N., B. R. Tenover, M. J. Servant, and J. Hiscott. 2002. The interferon antiviral response: from viral invasion to evasion. Curr. Opin. Infect. Dis. 15:259-267.
17. Hirasawa, K., A. Kim, H. S. Han, J. Han, H. S. Jun, and J. W. Yoon. 2003. Effect of p38 mitogen-activated protein kinase on the replication of encephalomyocarditis virus. J. Virol. 77:5649-5656. (Pubitemid 36538957)
18. Hirasawa, K., S. G. Nishikawa, K. L. Norman, T. Alain, A. Kossakowska, and P. W. K. Lee. 2002. Oncolytic reovirus against ovarian and colon cancer. Cancer Res. 62:1696-1701. (Pubitemid 34408491)
19. Horvath, C. M. 2004. Silencing STATs: lessons from paramyxovirus interferon evasion. Cytokine Growth Factor Rev. 15:117-127. (Pubitemid 38521248)
20. Horvath, C. M., G. R. Stark, I. M. Kerr, and J. E. Darnell, Jr. 1996. Interactions between STAT and non-STAT proteins in the interferon-stimulated gene factor 3 transcription complex. Mol. Cell. Biol. 16:6957-6964.
21. Improta, T., C. Schindler, C. M. Horvath, I. M. Kerr, G. R. Stark, and J. E. Darnell, Jr. 1994. Transcription factor ISGF-3 formation requires phosphorylated Stat91 protein, but Stat113 protein is phosphorylated independently of Stat91 protein. Proc. Natl. Acad. Sci. USA 91:4776-4780.
22. Klampfer, L., J. Huang, G. Corner, J. Mariadason, D. Arango, T. Sasazuki, S. Shirasawa, and L. Augenlicht. 2003. Oncogenic Ki-ras inhibits the expression of interferon-responsive genes through inhibition of STAT1 and STAT2 expression. J. Biol. Chem. 278:46278-46287.
23. Kong, X., H. San Juan, A. Behera, M. E. Peeples, J. Wu, R. F. Lockey, and S. S. Mohapatra. 2004. ERK-1/2 activity is required for efficient RSV infection. FEBS Lett. 559:33-38. (Pubitemid 38186699)
24. Krebs, D. L., and D. J. Hilton. 2000. SOCS: physiological suppressors of cytokine signaling. J. Cell Sci. 113:2813-2819.
25. Leung, S., S. A. Qureshi, I. M. Kerr, J. E. Darnell, Jr., and G. R. Stark. 1995. Role of STAT2 in the alpha interferon signaling pathway. Mol. Cell. Biol. 15:1312-1317.
26. Levy, D. E., and A. Garcia-Sastre. 2001. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev. 12:143-156. (Pubitemid 32590836)
27. Levy, D. E., D. S. Kessler, R. Pine, and J. E. Darnell, Jr. 1989. Cytoplasmic activation of ISGF3, the positive regulator of interferon-alpha- stimulated transcription, reconstituted in vitro. Genes Dev. 3:1362-1371.
28. Liu, B., J. Liao, X. Rao, S. A. Kushner, C. D. Chung, D. D. Chang, and K. Shuai. 1998. Inhibition of Stat1-mediated gene activation by PIAS1. Proc. Natl. Acad. Sci. USA 95:10626-10631.
29. Luo, H., B. Yanagawa, J. Zhang, Z. Luo, M. Zhang, M. Esfandiarei, C. Carthy, J. E. Wilson, D. Yang, and B. M. McManus. 2002. Coxsackievirus B3 replication is reduced by inhibition of the extracellular signal-regulated kinase (ERK) signaling pathway. J. Virol. 76:3365-3373. (Pubitemid 34224539)
30. Mundschau, L. J., and D. V. Faller. 1992. Oncogenic ras induces an inhibitor of double-stranded RNA-dependent eukaryotic initiation factor 2 alpha-kinase activation. J. Biol. Chem. 267:23092-23098.
31. Muñoz, A., and L. Carrasco. 1984. Action of human lymphoblastoid interferon on HeLa cells infected with RNA-containing animal viruses. J. Gen. Virol. 65:377-390.
32. Norman, K. L., K. Hirasawa, A. D. Yang, M. A. Shields, and P. W. Lee. 2004. Reovirus oncolysis: the Ras/RalGEF/p38 pathway dictates host cell permissiveness to reovirus infection. Proc. Natl. Acad. Sci. USA 101:11099-11104.
33. Noser, J. A., A. A. Mael, R. Sakuma, S. Ohmine, P. Marcato, L. P. Wk, and Y. Ikeda. 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.
34. Novick, D., B. Cohen, and M. Rubinstein. 1994. The human interferon alpha/beta receptor: characterization and molecular cloning. Cell 77:391-400. (Pubitemid 24145200)
35. Offermann, M. K., and D. V. Faller. 1990. Effect of cellular density and viral oncogenes on the major histocompatibility complex class I antigen response to gamma-interferon in BALB-c/3T3 cells. Cancer Res. 50:601-605. (Pubitemid 20054186)
36. Palvimo, J. J. 2007. PIAS proteins as regulators of small ubiquitin-related modifier (SUMO) modifications and transcription. Biochem. Soc. Trans. 35:1405-1408.
37. Planz, O., S. Pleschka, and S. Ludwig. 2001. MEK-specific inhibitor U0126 blocks spread of Borna disease virus in cultured cells. J. Virol. 75:4871-4877. (Pubitemid 32381529)
38. Pleschka, S., T. Wolff, C. Ehrhardt, G. Hobom, O. Planz, U. R. Rapp, and S. Ludwig. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signalling cascade. Nat. Cell Biol. 3:301-305.
39. Qureshi, S. A., S. Leung, I. M. Kerr, G. R. Stark, and J. E. Darnell, Jr. 1996. Function of Stat2 protein in transcriptional activation by alpha interferon. Mol. Cell. Biol. 16:288-293.
40. Ramaswamy, M., L. Shi, S. M. Varga, S. Barik, M. A. Behlke, and D. C. Look. 2006. Respiratory syncytial virus nonstructural protein 2 specifically inhibits type I interferon signal transduction. Virology 344:328-339. (Pubitemid 43049621)
41. Randall, R. E., and S. Goodbourn. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
42. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
43. Schindler, C. 1999. Cytokines and JAK-STAT signaling. Exp. Cell Res. 253:7-14.
44. Sebolt-Leopold, J. S. 2000. Development of anticancer drugs targeting the MAP kinase pathway. Oncogene 19:6594-6599. (Pubitemid 32197697)
45. Sen, G. C. 2001. Viruses and interferons. Annu. Rev. Microbiol. 55:255-281.
46. Stojdl, D. F., B. Lichty, S. Knowles, R. Marius, H. Atkins, N. Sonenberg, and J. C. Bell. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821-825.
47. Strong, J. E., M. C. Coffey, D. Tang, P. Sabinin, and P. W. Lee. 1998. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. EMBO J. 17:3351-3362. (Pubitemid 28279509)
48. Thompson, N., and J. Lyons. 2005. Recent progress in targeting the Raf/MEK/ERK pathway with inhibitors in cancer drug discovery. Curr. Opin. Pharmacol. 5:350-356.
49. Tnani, M., and B. A. Bayard. 1999. Evidence for IRF-1-dependent gene expression deficiency in interferon unresponsive HepG2 cells. Biochim. Biophys. Acta 1451:59-72.
50. Wormald, S., and D. J. Hilton. 2004. Inhibitors of cytokine signal transduction. J. Biol. Chem. 279:821-824.
51. Xu, D., and C. K. Qu. 2008. Protein tyrosine phosphatases in the JAK/STAT pathway. Front. Biosci. 13:4925-4932.
52. Yamamoto, A., A. Iwata, Y. Koh, S. Kawai, S. Murayama, K. Hamada, S. Maekawa, S. Ueda, and Y. Sokawa. 1998. Two types of chicken 2′,5′- oligoadenylate synthetase mRNA derived from alleles at a single locus. Biochim. Biophys. Acta 1395:181-191.