Expression of hepatitis C virus proteins interferes with the antiviral action of interferon independently of PKR-mediated control of protein synthesis

Journal of Virology

Volumn 74, Issue 12, 2000, Pages 5587-5596

  Francois C ^a   Duverlie, G ^a   Rebouillat, D ^b,f   Khorsi, H ^a   Castelain, S ^a   Blum, H E ^c   Gatignol, A ^d,g   Wychowski, C ^e   Moradpour, D ^c   Meurs, E F ^b  

^a AMIENS UNIVERSITY HOSPITAL   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF FREIBURG   (Germany)

^d INSTITUT COCHIN   (France)

^e INSTITUT DE BIOLOGIE DE LILLE   (France)

^f LERNER RESEARCH INSTITUTE   (United States)

^g MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; VIRUS PROTEIN;

ANTIVIRAL ACTIVITY; ARTICLE; ENCEPHALOMYOCARDITIS VIRUS; ENZYME INHIBITION; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS REGULATION; VIRUS RESISTANCE;

2',5'-OLIGOADENYLATE SYNTHETASE; ANTIVIRAL AGENTS; CYTOPLASM; EIF-2 KINASE; ENCEPHALOMYOCARDITIS VIRUS; ENDOPLASMIC RETICULUM; EUKARYOTIC INITIATION FACTOR-2; GENE EXPRESSION; GENE EXPRESSION REGULATION, VIRAL; HEPACIVIRUS; HUMANS; INTERFERONS; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; POLY I-C; POLYPROTEINS; PROTEIN BIOSYNTHESIS; TETRACYCLINE; TUMOR CELLS, CULTURED; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS;

EID: 0242422098     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.12.5587-5596.2000     Document Type: Article

References (46)

1. Anderson, S. L., J. M. Carton, J. Lou, L. Xing, and B. Y. Rubin. 1999. Interferon-induced guanylate binding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 256:8-14.
2. Barber, G. N., R. Jagus, E. F. Meurs, A. G. Hovanessian, and M. G. Katze. 1995. Molecular mechanisms responsible for malignant transformation by regulatory and catalytic domain variants of the interferon-induced enzyme RNA-dependent protein kinase. J. Biol. Chem. 270:17423-17428.
3. Benkirane, M., C. Neuveut, R. F. Chun, S. M. Smith, C. E. Samuel, A. Gatignol, and K.-T. Jeang. 1997. Oncogenic potential of TAR RNA-binding protein TRBP and its regulatory interaction with protein kinase PKR. EMBO J. 16:611-624.
4. Besse, S., D. Rebouillat, I. Marie, F. Puvion-Dutilleul, and A. G. Hovanessian. 1998. Ultrastructural localization of interferon-inducible double-stranded RNA-activaled enzymes in human cells. Exp. Cell Res. 239:379-392.
5. Chebath, J., P. Benech, M. Revel, and M. Vigneron. 1987. Constitutive expression of (2′-5′) oligo A synthetase confers resistance to picornavirus infection. Nature 330:587-588.
6. Chong, K., L. Feng, T. F. Donahue, J. D. Friesen, E. Meurs, A. G. Hovanessian, and B. R. G. Williams. 1992. Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. EMBO J. 11:1553-1562.
7. Clemens, M. J., and E. Androulla. 1997. The double-stranded RNA-dependent protein kinase PKR: structure and function. J. Interferon Res. 17:503-524.
8. Coccia, E. M., G. Romeo, A. Nissim, G. Marziali, R. Albertini, E. Affabris, A. Battistini, G. Fiorucci, R. Orsatti, G. B. Rossi, and J. Chebath. 1990. A full-length murine 2-5A synthetase cDNA transfected in NIH-3T3 cells impairs EMCV but not VSV replication. Virology 179:228-233.
9. Duh, E. J., W. J. Maury, T. M. Folks, A. S. Fauci, and A. B. Rabson. 1989. Tumor necrosis factor α activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-κB sites in the long terminal repeat. Proc. Natl. Acad. Sci. USA 86:5974-5978.
10. Duverlie, G., H. Khorsi, S. Castelain, O. Jaillon, J. Izopet, F. Lunel, F. Eb, F. Penin, and C. Wychowski. 1998. Sequence analysis of the NS5A protein of European hepatitis C virus 1b isolates and relation to interferon sensitivity. J. Gen. Virol. 79:1373-1381.
11. Enomoto, N., I. Sakuma, Y. Asahina, M. Kurosaki, T. Murakami, C. Yamamoto, Y. Ogura. N. Izumi, F. Marumo, and C. Sato. 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.
12. Frese, M., G. Kochs, U. Meier-Dieter, J. Siebler, and O. Haller. 1995. Human MxA protein inhibits tick-borne Thogoto virus but not Dhori virus. J. Virol. 69:3904-3909.
13. Gale, M., Jr., C. M. Blakely, B. Kwieciszewski, S.-L. Tan, M. Dossett, N. M. Tang, M. J. Korth, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1998. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18:5208-5218.
14. Gale, M. J., Jr., M. J. Korth, N. M. Tang, S. L. Tan, D. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-227.
15. Gatignol, A., A. Buckler-White, B. Berkhout, and K.-T. Jeang. 1991. Characterization of human TAR RNA-binding protein that activates the HIV-1 LTR. Science 251:1597-1600.
16. Gatignol, A., M. Duarte, L. Daviet, Y. N. Chang, and K. T. Jeang. 1996. Sequential steps in Tat trans-activation of HIV-1 mediated through cellular DNA, RNA, and protein binding factors. Gene Expr. 5:217-228.
17. Heim, M. H., D. Moradpour, and H. E. Blum. 1999. Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-STAT pathway. J. Virol. 73:8469-8475.
18. Hershey, J. W. 1991. Translational control in mammalian cells. Annu. Rev. Biochem. 60:717-755.
19. Hofgärtner, W. T., S. J. Polyak, D. G. Sullivan, R. L. Carithers, and D. R. Gretch. 1997. Mutations in the NS5A gene of hepatitis C virus in North American patients infected with HCV genotype 1a or 1b. J. Med. Virol. 53: 118-126.
20. Hovanessian, A. G. 1993. Interferon-induced dsRNA-activated protein kinase (PKR): antiproliferative, antiviral and antitumoral functions. Semin. Virol. 4:237-245.
21. Hovanessian, A. G., and J. Galabru. 1987. The double-stranded RNA-dependent protein kinase is also activated by heparin. Eur. J. Biochem. 167: 467-473.
22. Hovanessian, A. G., J. Galabru, E. Meurs, C. Buffet-Janvresse, J. Svab, and N. Robert. 1987. Rapid decrease in the levels of the double-stranded RNA-dependent protein kinase during virus infections. Virology 159:126-136.
23. Hovanessian, A. G., J. Svab, I. Marie, N. Robert, S. Chamaret, and A. G. Laurent. 1988. Characterization of 69-and 100-kDa forms of 2-5A-synthetase from interferon-treated human cells. J. Biol. Chem. 263:4945-4959.
24. Jeffrey, I. W., S. Kadereit, E. F. Meurs, T. Metzger, M. Bachmann, M. Schwemmle, A. G. Hovanessian, and M. J. Clemens. 1995. Nuclear localization of the interferon-inducible protein kinase PKR in human cells and transfected mouse cells. Exp. Cell Res. 218:17-27.
25. Khorsi, H., S. Castelain, A. Wyseur, J. Izopet, V. Canva, A. Rombout, D. Capron, J. P. Capron, F. Lunel, L. Stuyver, and G. Duverlie. 1997. Mutations of hepatitis C virus 1b NS5A 2209-2248 amino acid sequence do not predict the response to recombinant interferon-alfa therapy in French patients. J. Hepatol. 27:72-77.
26. Koromilas, A. E., S. Roy, G. N. Barber, M. G. Katze, and N. Sonenberg. 1992. Malignant transformation by a mutant of the IFN-inducible dsRNA-dependent protein kinase. Science 257:1685-1689.
27. Landis, H., A. Simon-Jödicke, A. Klöti, C. Di Paolo, J.-J. Schnorr, S. Schneider-Schaulies, H. P. Hefti, and J. Pavlovic. 1998. Human MxA protein confers resistance to Semliki Forest virus and inhibits the amplification of a Semliki Forest virus-based replicon in the absence of viral structural proteins. J. Virol. 72:1516-1522.
28. r protein and their use for the detection of double-stranded RNA dependent protein kinase in human cells. Proc. Natl. Acad. Sci. USA 82:4341-4345.
29. Major, M. E., and S. M. Feinstone. 1997. The molecular virology of hepatitis C. Hepatology 25:1527-1538.
30. Marie, I., J. Blanco, D. Rebouillat, and A. G. Hovanessian. 1997. 69-kDa and 100-kDa isoforms of interferon-induced (2′-5′) oligoadenylate synthetase exhibit differential catalytic parameters. Eur. J. Biochem. 248:558-566.
31. Meurs, E. F., J. Galabru, G. N. Barber, M. G. Katze, and A. G. Hovanessian. 1993. Tumor suppressor function of the interferon-induced double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 90:232-236.
32. Meurs, E. F., N. McMillan, B. R. Williams, A. G. Hovanessian, and P. J. Southern. 1995. Human PKR transfected into murine cells stimulates expression of genes under control of the HIV1 or HTLV-I LTR. Virology 214: 653-659. (Erratum, 247:125, 1998.)
33. Meurs, E. F., Y. Watanabe, S. Kadereit, G. N. Barber, M. G. Katze, K. Chong, B. R. G. Williams, and A. G. Hovanessian. 1992 Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus growth. J. Virol. 66:5805-5814.
34. Moradpour, D., P. Kary, C. M. Rice, and H. E. Blum. 1998. Continuous human cell lines inducibly expressing hepatitis C virus structural and nonstructural proteins. Hepatology 28:192-201.
35. Patel, R. C., P. Stanton, and G. C. Sen. 1994. Role of the amino-terminal residues of the interferon-induced protein kinase in its activation by double-stranded RNA and heparin. J. Biol. Chem. 269:18593-18598.
36. Pavlovic, J., T. Zürcher, O. Haller, and P. Staeheli. 1990. Resistance to influenza virus and vesicular stomatitis virus conferred by expression of human MxA protein. J. Virol. 64:3370-3375.
37. Polyak, S. J., D. M. Paschal, S. McArdle, M. J. Gale, Jr., D. Moradpour, and D. R. Gretch. 1999. Characterization of the effects of hepatitis C virus nonstructural 5A protein expression in human cell lines and on interferon-sensitive virus replication. Hepatology 29:1262-1271.
38. r protein kinase. J. Virol. 65:632-640.
39. Schnorr, J.-J., S. Schneider-Schaulies, A. Simon-Jödicke, J. Pavlovic, M. A. Horisberger, and V. ter Meulen. 1993. MxA-dependent inhibition of measles virus glycoprotein synthesis in a stably transfected human monocytic cell line. J. Virol. 67:4760-4768.
40. Song, J., M. Fujii, F. Wang, M. Itoh, and H. Hotta. 1999. The NS5A protein of hepatitis C virus partially inhibits the antiviral activity of interferon. J. Gen. Virol. 80:879-886.
41. Squadrito, G., F. Leone, M. Sartori, B. Nalpas, P. Berthelot, G. Raimondo, S. Pol, and C. Brechot. 1997. Mutations in the nonstructural 5A region of hepatitis C virus and response of chronic hepatitis C to interferon alfa. Gastroenterology 113:567-572.
42. Tan, S. L., H. Nakao, Y. He, S. Vijaysri, P. Neddermann, B. L. Jacobs, B. J. Mayer, and M. G. Katze. 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. USA 96:5533-5538.
43. Taylor, D. R., S. T. Shi, P. R. Romano, G. N. Barber, and M. C. Lai. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285:107-110.
44. Tong, C. Y., I. T. Gilmore, and C. A. Hart. 1995. HCV-associated liver cancer. Lancet 345:1058-1059.
45. Zeuzem, S., J. H. Lee, and W. K. Roth. 1997. Mutations in the nonstructural 5A gene of European hepatitis C virus isolates and response to interferon alfa. Hepatology 25:740-744.
46. Zhou, A., J. Paranjape, S. Der, B. Williams, and R. Silverman. 1999. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 258:435-440.