Regulation of mRNA translation and cellular signaling by hepatitis C virus nonstructural protein NS5A

Journal of Virology

Volumn 75, Issue 11, 2001, Pages 5090-5098

  He, Yupeng ^a   Tan, Seng Lai ^a,d   Tareen, Semih U ^b   Vijaysri, Sangeetha ^c   Langland, Jeffrey O ^c   Jacobs, Bertram L ^c   Katze, Michael G ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTERFERON; EPIDERMAL GROWTH FACTOR; INITIATION FACTOR 4E; INTERFERON; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN KINASE R; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; VACCINIA VACCINE; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL COMMUNICATION; HELA CELL; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; SIGNAL TRANSDUCTION; VIRUS GENE; VIRUS INFECTION;

AUTORADIOGRAPHY; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; EUKARYOTIC INITIATION FACTOR-4E; GENETIC VECTORS; HELA CELLS; HEPACIVIRUS; HUMANS; IMMUNOBLOTTING; INTERFERONS; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDE INITIATION FACTORS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RECOMBINANT PROTEINS; RNA REPLICASE; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; VACCINIA VIRUS; VIRAL NONSTRUCTURAL PROTEINS; VIRAL PROTEINS;

EID: 0035041305     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.75.11.5090-5098.2001     Document Type: Article

References (59)

1. Alter, M. J. H. 1997. Epidemiology of hepatitis C. Hepatology 26:62-65.
2. Barber, G. N., J. Tomita, M. S. Garfinkel, E. Meurs, A. Hovanessian, and M. G. Katze. 1992. Detection of protein kinase homologues and viral RNA-binding domains utilizing polyclonal antiserum prepared against a baculovirus-expressed dsRNA-activated 68,000-Da protein kinase. Virology 191: 670-679.
3. Beattie, E., K. L. Denzler, J. Tartaglia, M. E. Perkus, E. Paoletti, and B. L. Jacobs. 1995. Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene. J. Virol. 69:499-505.
4. Beattie, E., E. Paoletti, and J. Tartaglia. 1995. Distinct patterns of IFN sensitivity observed in cells infected with vaccinia K3L and E3L mutant viruses. Virology 210:254-263.
5. Beattie, E., J. Tartaglia, and E. Paoletti. 1991. Vaccinia virus-encoded eIF-2α homolog abrogates the antiviral effect of interferon. Virology 183: 419-422.
6. Black, T. L., G. N. Barber, and M. G. Katze. 1993. Degradation of the interferon-induced 68,000-M(r) protein kinase by poliovirus requires RNA. J. Virol. 67:791-800.
7. Black, T. L., B. Safer, A. Hovanessian, and M. G. Katze. 1989. The cellular 68,000-Mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J. Virol. 63:2244-2251.
8. Chang, H. W., J. C. Watson, and B. L. Jacobs. 1992. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 89: 4825-4829.
9. Chang, H. W., L. H. Uribe, and B. L. Jacobs. 1995. Rescue of vaccinia virus lacking the E3L gene by mutant of E3L. J. Virol. 69:6605-6608.
10. Chardin, P., D. Cussac, S. Maignan, and A. Ducruix. 1995. The Grb2 adaptor. FEBS Lett. 369:47-51.
11. Clemens, M. J. 1996. Protein kinases that phosphorylate eIF2 and eIF2B, and their role in eukaryotic cell translational control, p. 139-172. In J. W. B Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
12. Dever, T. E. 1999. Translation initiation: adept at adapting. Trends Biochem. Sci. 24:398-403.
13. Downward, J. 1994. The GRB2/Sem-5 adaptor protein. FEBS Lett. 338:113-117.
14. Enomoto, N., I. Sakuma, Y. Asahina, M. Kurosaki, T. Murakami, C. Yamamoto, Y. Ogura, N. Izumi, F. Maruno, 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.
15. Enomoto, N., I. Sakuma, Y. Asahina, M. Kurosaki, T. Murankami, C. Yamamoto, N. Izumi, F. Marumo, and C. Sato. 1995. Comparison of full-length sequences of interferon-sensitive and resistant hepatitis C virus 1b. J. Clin. Investig. 96:224-230.
16. Francois, C., G. Duverlie, D. Rebouillat, H. Khorsi, S. Castelain, H. E. Blum, A. Gatignol, C. Wychowski, D. Moradpour, and E. F. Meurs. 2000. Expression of hepatitis C virus proteins interferes with the antiviral action of interferon independently of PKR-mediated control of protein synthesis. J. Virol. 74:5587-5596.
17. Galabru, J., and A. G. Hovanessian. 1987. Autophosphorylation of the protein kinase dependent on double-stranded RNA. J. Biol. Chem. 262:15538-15544.
18. Gale, M., Jr., M. J. Korth, N. M. Tang, S. L. Tan, D. A. 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.
19. Gale, M., Jr., C. M. Blakely, B. Kwieciszewski, S. L. Tan, M. Dossett, 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.
20. Gale, M., Jr., B. Kwieciszewski, M. Dossett, H. Nakao, and M. G,. Katze. 1999. Antiapoptotic and oncogenic potentials of hepatitis C virus are linked to interferon resistance hy viral repression of the PKR protein kinase. J. Virol. 73:6506-6516.
21. Gale, M., Jr., and M. G. Katze. 1998. Molecular mechanisms of interferon resistance mediated by viral-directed inhihition of PKR, the interferon-induced protein kinase. Pharmacol. Ther. 78:29-46.
22. Gale, M., Jr., S. L. Tan, and M. G. Katze. 2000. Translational control of viral gene expression in eukaryotes. Microbiol. Mol. Biol. Rev. 64:239-280.
23. Garrington, T. P., and G. L. Johnson. 1999. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell Biol. 11:211-218.
24. Goh, K. C., M. J. deVeer, and B. R. Williams. 2000. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J. 19:4292-4297.
25. Herion, D., and J. H. Hoofnagle. 1997. The interferon sensitivity determining region: all hepatitis C virus isolates are not the same. Hepatology 25:769-771.
26. Hoofnagle, J. H. 1994. Therapy of acute and chronic viral hepatitis. Adv. Intern. Med. 39:241-275.
27. Hovanessian, A. G. 1989. The double stranded RNA-activated protein kinase induced by interferon: dsRNA-PK. J. Interferon Res. 9:641-647.
28. Ihle, J. N. 1996. STATs and MAPKs: obligate or opportunistic partners in signaling. Bioessays 18:95-98.
29. 2-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R, and alternative pathways. Mol. Cell. Biol. 20:617-627.
30. Kibler, K. V., T. Shors, K. B. Perkins, C. C. Zeman, M. P. Banaszak, J. Biesterfeldt, J. O. Langland, and B. L. Jacobs. 1997. Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells. J. Virol. 71:1992-2003.
31. Langland, J. O., S. Pettiford, B. Jiang, and B. L. Jacobs. 1994. Products of the porcine group C rotavirus NSP3 gene bind specifically to double-stranded RNA and inhibit activation of the interferon-induced protein kinase PKR. J. Virol. 68:3821-3829.
32. Leaman, D. W., S. Leung, X. Li, and G. R. Stark. 1996. Regulation of STAT-dependent pathways by growth factors and cytokines. FASEB J. 10: 1578-1588.
33. Lindsay, K. L. 1997. Therapy of hepatitis C: overview. Hepatology 26:71S-77S.
34. Moradpour, D., and H. E. Blum. 1999. Current and evolving therapies for hepatitis C. Eur. J. Gastroenterol. Hepatol. 11:1199-1202.
35. Obata, T., G. E. Brown, and M. B. Yaffe. 2000. MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit. Care Med. 28:N67-N77.
36. Okuda, K. 1998. Hepatitis C and hepatocellular carcinoma. J. Gastroenterol. Hepatol. 13:294-298.
37. Paez, E., and M. Esteban. 1984. Resistance of vaccinia virus to interferon is related to an interference phenomenon between the virus and the interferon system. Virology 134:12-28.
38. Park, H., M. V. Davies, J. O. Langland, H. W. Chang, Y. S. Nam, J. Tartaglia, E. Paoletti, B. L. Jacobs, R. J. Kaufman, and S. Venkatesan. 1994. TAR RNA-binding protein is an inhibitor of the interferon-induced protein kinase PKR. Proc. Natl. Acad. Sci. USA 91:4713-4717.
39. 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.
40. Reed, K. E., and C. M. Rice. 2000. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 242:55-84.
41. Reed, K. E., J. Xu, and C. M. Rice. 1997. Phosphorylation of the hepatitis C virus NS5A protein in vitro and in vivo: properties of the NS5A-associated kinase. J. Virol. 71:7187-7197.
42. Rice, A. P., and I. M. Kerr. 1984. Interferon-mediated, double-stranded RNA-dependent protein kinase is inhibited in extracts from vaccinia virus-infected cells. J. Virol. 50:229-236.
43. Rice, A. P., W. K. Roberts, and I. M. Kerr. 1984. 2-5A accumulates to high levels in interferon-treated, vaccinia virus-infected cells in the absence of any inhibition of virus replication. J. Virol. 50:220-228.
44. Rivas, C., J. Gil, Z. Melkova, M. Esteban, and M. Diaz-Guerra. 1998. Vaccinia virus E3L protein is an inhibitor of the interferon (IFN)-induced 2-5A synthetase enzyme. Virology 243:406-414.
45. Romano, P. R., S. R. Green, G. N. Barber, M. B. Mathews, and A. G. Hinnebusch. 1995. Structural requirements for double-stranded RNA binding, dimerization, and activation of the human eIF-2 alpha kinase DA1 in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:365-378.
46. Romano, P. R., F. Zhang, S. L. Tan, M. T. Garcia-Barrio, M. G. Katze, T. E. Dever, and A. G. Hinnebusch. 1998. Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: role of complex formation and the E3 N-terminal domain. Mol. Cell. Biol. 18:7304-7316.
47. Shors, T., and B. L. Jacobs. 1997. Complementation of deletion of the vaccinia virus E3L gene by the Escherichia coli RNase III gene. Virology 227:77-87.
48. Sonenberg, N. 1996. mRNA 5′ cap-binding protein eIF4E and control of cell growth, p. 245-270. In J. Hershey, M. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Sonenberg, N., and A. C. Gingras. 1998. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10:268-275.
50. 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.
51. Tan, S. L., H. Nakao, Y. He, V. 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.
52. Tanji, Y., T. Kaneko, S. Satoh, and K. Shimotohno. 1995. Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J. Virol. 69:3980-3986.
53. Tartaglia, J., M. E. Perkus, J. Taylor, E. K. Norton, J. C. Audonnet, W. I. Cox, S. W. Davis, J. van der Hoeven, B. Meignier, M. Riviere, et al. 1992. NYVAC: a highly attenuated strain of vaccinia virus. Virology 188:217-232.
54. Taylor, D. R., S. T. Shi, P. R. Romano, G. N. Barber, and M. M. Lai. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285:107-110.
55. Tsukiyama-Kohara, K., N. Iizuka, M. Kohara, and A. Nomoto. 1992. Internal ribosome entry site within hepatitis C virus RNA. J. Virol. 66:1475-1483.
56. Ventoso, I., S. E. MacMillan, J. W. Hershey, and L. Carrasco. 1998. Polio-virus 2A proteinase cleaves directly the eIF-4G subunit of eIF-4F complex. FEBS Lett. 435:79-83.
57. Vojtek, A. B., and C. J. Der. 1998. Increasing complexity of the Ras signaling pathway. J. Biol. Chem. 273:9925-9928.
58. Wang, C., P. Sarnow, and A. Siddiqui. 1993. Translation of human hepatitis C virus RNA in cultured cells is mediated by an internal ribosome-binding mechanism. J. Virol. 67:3338-3344.
59. Williams, B. R. G. 1999. PKR; a sentinel kinase for cellular stress. Oncogene 18:6112-6120.