Identification of three interferon-inducible cellular enzymes that inhibit the replication of hepatitis C virus

Journal of Virology

Volumn 82, Issue 4, 2008, Pages 1665-1678

  Jiang, Dong ^a   Guo, Haitao ^a   Xu, Chunxiao ^c   Chang, Jinhong ^a,c   Gu, Baohua ^a   Wang, Lijuan ^a   Block, Timothy M ^a,b   Guo, Ju Tao ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b HEPATITIS B FOUNDATION   (United States)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; EXONUCLEASE; INTERFERON REGULATORY FACTOR; INTERFERON STIMULATED GENE 20 PROTEIN; INTERFERON STIMULATED GENE PROTEIN; PROTEIN KINASE R; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG; VIPERIN;

ANTIVIRAL ACTIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHRONIC HEPATITIS; CONTROLLED STUDY; ENZYME ANALYSIS; GENE; GENE EXPRESSION REGULATION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INTERFERON PRODUCTION; INTERFERON STIMULATED GENE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; VIRUS INHIBITION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; CELL LINE; EIF-2 KINASE; EXONUCLEASES; GENE EXPRESSION; GENOME, VIRAL; HEPACIVIRUS; HUMANS; INTERFERON-ALPHA; MOLECULAR SEQUENCE DATA; PROTEINS; REPLICON; RNA, VIRAL; S-ADENOSYLMETHIONINE; TRANSFECTION; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 38849194747     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02113-07     Document Type: Article

References (74)

1. Ali, S., C. Pellerin, D. Lamarre, and G. Kukolj. 2004. Hepatitis C virus subgenomic replicons in the human embryonic kidney 293 cell line. J. Virol. 78:491-501.
2. Alter, H. J., and L. B. Seeff. 2000. Recovery, persistence, and sequelae in hepatitis C virus infection: a perspective on long-term outcome. Semin. Liver Dis. 20:17-35.
3. Barber, G. N. 2005. The dsRNA-dependent protein kinase, PKR and cell death. Cell Death Differ. 12:563-570.
4. Berkovitch, F., Y. Nicolet, J. T. Wan, J. T. Jarrett, and C. L. Drennan. 2004. Crystal structure of biotin synthase, an S- adenosylmethionine-dependent radical enzyme. Science 303:76-79.
5. Bigger, C. B., K. M. Brasky, and R. E. Lanford. 2001. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J. Virol. 75:7059-7066.
6. Bigger, C. B., B. Guerra, K. M. Brasky, G. Hubbard, M. R. Beard, B. A. Luxon, S. M. Lemon, and R. E. Lanford. 2004. Intrahepatic gene expression during chronic hepatitis C virus infection in chimpanzees. J. Virol. 78:13779-3792.
7. Binder, M., G. Kochs, R. Bartenschlager, and V. Lohmann. 2007. Hepatitis C virus escape from the interferon regulatory factor 3 pathway by a passive and active evasion strategy. Hepatology 46:1365-1374.
8. Boudinot, P., P. Massin, M. Blanco, S. Riffault, and A. Benmansour. 1999. vig-1, a new fish gene induced by the rhabdovirus glycoprotein, has a virus-induced homologue in humans and shares conserved motifs with the MoaA family. J. Virol. 73:1846-1852.
9. Boudinot, P., S. Riffault, S. Salhi, C. Carrat, C. Sedlik, N. Mahmoudi, B. Charley, and A. Benmansour. 2000. Vesicular stomatitis virus and pseudorabies virus induce a vig1/cig5 homologue in mouse dendritic cells via different pathways. J. Gen. Virol. 81:2675-2682.
10. Chang, J., S. O. Gudima, C. Tarn, X. Nie, and J. M. Taylor. 2005. Development of a novel system to study hepatitis delta virus genome replication. J. Virol. 79:8182-8188.
11. Chang, K. S., Z. Cai, C. Zhang, G. C. Sen, B. R. Williams, and G. Luo. 2006. Replication of hepatitis C virus (HCV) RNA in mouse embryonic fibroblasts: protein kinase R (PKR)-dependent and PKR-independent mechanisms for controlling HCV RNA replication and mediating interferon activities. J. Virol. 80:7364-7374.
12. Chin, K. C., and P. Cresswell. 2001. Viperin (cig5), an IFN-inducible anti-viral protein directly induced by human cytomegalovirus. Proc. Natl. Acad. Sci. USA 98:15125-15130.
13. D'Addario, M., A. Roulston, M. A. Weinberg, and J. Hiscott. 1990. Coordinate enhancement of cytokine gene expression in human immunodeficiency virus type 1-infected promonocytic cells. J. Virol. 64:6080-6089.
14. Der, S. D., and A. S. Lau. 1995. Involvement of the double-stranded-RNA-dependent kinase PKR in interferon expression and interferon-mediated antiviral activity. Proc. Natl. Acad. Sci. USA 92:8841-8845.
15. 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.
16. Dey, M., C. Cao, A. C. Dar, T. Tamura, K. Ozato, F. Sicheri, and T. E. Dever. 2005. Mechanistic link between PKR dimerization, autophosphorylation, and eIF2α substrate recognition. Cell 122:901-913.
17. Di Bisceglie, A. M., and J. H. Hoofnagle. 2002. Optimal therapy of hepatitis C. Hepatology 36:S121-S127.
18. Duin, E. C., M. E. Lafferty, B. R. Crouse, R. M. Allen, I. Sanyal, D. H. Flint, and M. K. Johnson. 1997. [2Fe-2S] to [4Fe-4S] cluster conversion in Escherichia coli biotin synthase. Biochemistry 36:11811-11820.
19. Espert, L., G. Degols, C. Gongora, D. Blondel, B. R. Williams, R. H. Silverman, and N. Mechti. 2003. ISG20, a new interferon-induced RNase specific for single-stranded RNA, defines an alternative antiviral pathway against RNA genomic viruses. J. Biol. Chem. 278:16151-16158.
20. Espert, L., G. Degols, Y. L. Lin, T. Vincent, M. Benkirane, and N. Mechti. 2005. Interferon-induced exonuclease ISG20 exhibits an antiviral activity against human immunodeficiency virus type 1. J. Gen. Virol. 86:2221-2229.
21. Espert, L., P. Eldin, C. Gongora, B. Bayard, F. Harper, M. K. Chelbi-Alix, E. Bertrand, G. Degols, and N. Mechti. 2006. The exonuclease ISG20 mainly localizes in the nucleolus and the Cajal (coiled) bodies and is associated with nuclear SMN protein-containing complexes. J. Cell Biochem. 98:1320-1333.
22. Foy, E., K. Li, C. Wang, R. Sumpter, Jr., M. Ikeda, S. M. Lemon, and M. Gale, Jr. 2003. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300:1145-1148.
23. Frese, M., T. Pietschmann, D. Moradpour, O. Haller, and R. Bartenschlager. 2001. Interferon-alpha inhibits hepatitis C virus subgenomic RNA replication by an MxA-independent pathway. J. Gen. Virol. 82:723-733.
24. Frey, P. A., and S. J. Booker. 2001. Radical mechanisms of S-adenosylmethionine-dependent enzymes. Adv. Protein Chem. 58:1-45.
25. Gale, M., Jr., and E. M. Foy. 2005. Evasion of intracellular host defence by hepatitis C virus. Nature 436:939-945.
26. Garcia, M. A., J. Gil, I. Ventoso, S. Guerra, E. Domingo, C. Rivas, and M. Esteban. 2006. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70:1032-1060.
27. Gongora, C., G. David, L. Pintard, C. Tissot, T. D. Hua, A. Dejean, and N. Mechti. 1997. Molecular cloning of a new interferon-induced PML nuclear body-associated protein. J. Biol. Chem. 272:19457-19463.
28. Guo, J. T., V. V. Bichko, and C. Seeger. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-8523.
29. Guo, J. T., J. A. Sohn, Q. Zhu, and C. Seeger. 2004. Mechanism of the interferon alpha response against hepatitis C virus replicons. Virology 325: 71-81.
30. Guo, J. T., Q. Zhu, and C. Seeger. 2003. Cytopathic and noncytopathic interferon responses in cells expressing hepatitis C virus subgenomic replicons. J. Virol. 77:10769-10779.
31. Guo, X., J. Ma, J. Sun, and G. Gao. 2007. The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc. Natl. Acad. Sci. USA 104:151-156.
32. Hayashi, J., R. Stoyanova, and C. Seeger. 2005. The transcriptome of HCV replicon expressing cell lines in the presence of alpha interferon. Virology 335:264-275.
33. Helbig, K. J., D. T. Lau, L. Semendric, H. A. Harley, and M. R. Beard. 2005. Analysis of ISG expression in chronic hepatitis C identifies viperin as a potential antiviral effector. Hepatology 42:702-710.
34. Horio, T., M. Murai, T. Inoue, T. Hamasaki, T. Tanaka, and T. Ohgi. 2004. Crystal structure of human ISG20, an interferon-induced antiviral ribonuclease. FEBS Lett. 577:111-116.
35. Ji, X., R. Cheung, S. Cooper, Q. Li, H. B. Greenberg, and X. S. He. 2003. Interferon alfa regulated gene expression in patients initiating interferon treatment for chronic hepatitis C. Hepatology 37:610-621.
36. Kato, T., T. Date, M. Miyamoto, Z. Zhao, M. Mizokami, and T. Wakita. 2005. Nonhepatic cell lines HeLa and 293 support efficient replication of the hepatitis C virus genotype 2a subgenomic replicon. J. Virol. 79:592-596.
37. Khaiboullina, S. F., A. A. Rizvanov, M. R. Holbrook, and S. St. Jeor. 2005. Yellow fever virus strains Asibi and 17D-204 infect human umbilical cord endothelial cells and induce novel changes in gene expression. Virology 342:167-176.
38. Kozbial, P. Z., and A. R. Mushegian. 2005. Natural history of S-adenosylmethionine-binding proteins. BMC Struct. Biol. 5:19.
39. Lanford, R. E., B. Guerra, H. Lee, D. Chavez, K. M. Brasky, and C. B. Bigger. 2006. Genomic response to interferon-alpha in chimpanzees: implications of rapid downregulation for hepatitis C kinetics. Hepatology 43:961-972.
40. Layer, G., D. W. Heinz, D. Jahn, and W. D. Schubert. 2004. Structure and function of radical SAM enzymes. Curr. Opin. Chem. Biol. 8:468-476.
41. Layer, G., J. Moser, D. W. Heinz, D. Jahn, and W. D. Schubert. 2003. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of radical SAM enzymes. EMBO J. 22:6214-6224.
42. Li, K., E. Foy, J. C. Ferreon, M. Nakamura, A. C. Ferreon, M. Ikeda, S. C. Ray, M. Gale, Jr., and S. M. Lemon. 2005. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. USA 102:2992-2997.
43. Lindenbach, B. D., and C. M. Rice. 2005. Unravelling hepatitis C virus replication from genome to function. Nature 436:933-938.
44. Loo, Y. M., D. M. Owen, K. Li, A. K. Erickson, C. L. Johnson, P. M. Fish, D. S. Carney, T. Wang, H. Ishida, M. Yoneyama, T. Fujita, T. Saito, W. M. Lee, C. H. Hagedorn, D. T. Lau, S. A. Weinman, S. M. Lemon, and M. Gale, Jr. 2006. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc. Natl. Acad. Sci. USA 103:6001-6006.
45. Marcello, T., A. Grakoui, G. Barba-Spaeth, E. S. Machlin, S. V. Kotenko, M. R. MacDonald, and C. M. Rice. 2006. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 131:1887-1898.
46. McHutchison, J. G., S. C. Gordon, E. R. Schiff, M. L. Shiffman, W. M. Lee, V. K. Rustgi, Z. D. Goodman, M. H. Ling, S. Cort, J. K. Albrecht, et al. 1998. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N. Engl. J. Med. 339:1485- 1492.
47. Melen, K., P. Keskinen, A. Lehtonen, and I. Julkunen. 2000. Interferon-induced gene expression and signaling in human hepatoma cell lines. J. Hepatol. 33:764-772.
48. Meylan, E., J. Curran, K. Hofmann, D. Moradpour, M. Binder, R. Barten-schlager, and J. Tschopp. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437:1167-1172.
49. Naka, K., K. Takemoto, K. Abe, H. Dansako, M. Ikeda, K. Shimotohno, and N. Kato. 2005. Interferon resistance of hepatitis C virus replicon-harbouring cells is caused by functional disruption of type I interferon receptors. J. Gen. Virol. 86:2787-2792.
50. Neumann, A. U., N. P. Lam, H. Dahari, D. R. Gretch, T. E. Wiley, T. J. Layden, and A. S. Perelson. 1998. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282:103-107.
51. Nguyen, L. H., L. Espert, N. Mechti, and D. M. Wilson III. 2001. The human interferon- and estrogen-regulated ISG20/HEM45 gene product degrades single-stranded RNA and DNA in vitro. Biochemistry 40:7174-7179.
52. Nie, Y., G. L. Hammond, and J. H. Yang. 2007. Double-stranded RNA deaminase ADAR1 increases host susceptibility to virus infection. J. Virol. 81:917-923.
53. Radaeva, S., B. Jaruga, F. Hong, W. H. Kim, S. Fan, H. Cai, S. Strom, Y. Liu, O. El-Assal, and B. Gao. 2002. Interferon-alpha activates multiple STAT signals and down-regulates c-Met in primary human hepatocytes. Gastroenterology 122:1020-1034.
54. Rivieccio, M. A., H. S. Sun, Y. Zhao, M. L. Zhao, K. C. Chin, S. C. Lee, and C. F. Brosnan. 2006. TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5. J. Immunol. 177:4735-4741.
55. Seeger, C. 2005. Salient molecular features of hepatitis C virus revealed. Trends Microbiol. 13:528-534.
56. Sen, G. C. 2001. Viruses and interferons. Armu. Rev. Microbiol. 55:255-281.
57. Severa, M., E. M. Coccia, and K. A. Fitzgerald. 2006. Toll-like receptor-dependent and -independent viperin gene expression and counter-regulation by PRDI-binding factor-1/BLIMP1. J. Biol. Chem. 281:26188-26195.
58. Smith, M. W., Z. N. Yue, M. J. Korth, H. A. Do, L. Boix, N. Fausto, J. Bruix, R. L. Carithers, Jr., and M. G. Katze. 2003. Hepatitis C virus and liver disease: global transcriptional profiling and identification of potential markers. Hepatology 38:1458-1467.
59. Sofia, H. J., G. Chen, B. G. Hetzler, J. F. Reyes-Spindola, and N. E. Miller. 2001. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29:1097-1106.
60. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Armu. Rev. Biochem. 67:227-264.
61. Su, A. I., J. P. Pezacki, L. Wodicka, A. D. Brideau, L. Supekova, R. Thimme, S. Wieland, J. Bukh, R. H. Purcell, P. G. Schultz, and F. V. Chisari. 2002. Genomic analysis of the host response to hepatitis C virus infection. Proc. Natl. Acad. Sci. USA 99:15669-15674.
62. Taylor, D. R., M. Puig, M. E. Darnell, K. Mihalik, and S. M. Feinstone. 2005. New antiviral pathway that mediates hepatitis C virus replicon interferon sensitivity through ADARl. J. Virol. 79:6291-6298.
63. Verma, S., K. Ziegler, P. Ananthula, J. K. Co, R. J. Frisque, R. Yanagihara, and V. R. Nerurkar. 2006. JC virus induces altered patterns of cellular gene expression: interferon-inducible genes as major transcriptional targets. Virology 345:457-467.
64. Wang, C., J. Pflugheber, R. Sumpter, Jr., D. L. Sodora, D. Hui, G. C. Sen, and M. Gale, Jr. 2003. Alpha interferon induces distinct translational control programs to suppress hepatitis C virus RNA replication. J. Virol. 77:3898-3912.
65. Wang, S. C., and P. A. Frey. 2007. S-Adenosylmethionine as an oxidant: the radical SAM superfamily. Trends Biochem. Sci. 32:101-110.
66. Williams, B. R. 2001. Signal integration via PKR. Sci. STKE 2001:RE2.
67. Zhang, Y., C. W. Burke, K. D. Ryman, and W. B. Klimstra. 2007. Identification and characterization of interferon-induced proteins that inhibit alphavirus replication. J. Virol.81:1246-11255.
68. Zhou, A., B. A. Hassel, and R. H. Silverman. 1993. Expression cloning of 2-5A-dependent RNase: a uniquely regulated mediator of interferon action. Cell 72:753-765.
69. Zhou, A., R. J. Molinaro, K. Malathi, and R. H. Silverman. 2005. Mapping of the human RNase L promoter and expression in cancer and normal cells. J. Interferon Cytokine Res. 25:595-603.
70. Zhou, A., J. M. Paranjape, S. D. Der, B. R. Williams, and R. H. Silverman. 1999. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 258:435-440.
71. Zhu, H., J. P. Cong, G. Mamtora, T. Gingeras, and T. Shenk. 1998. Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 95:14470-14475.
72. Zhu, H., J. P. Cong, and T. Shenk. 1997. Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc. Natl. Acad. Sci. USA 94:13985-13990.
73. Zhu, Q., J. T. Guo, and C. Seeger. 2003. Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J. Virol. 77:9204-9210.
74. Zuo, Y., and M. P. Deutscher. 2001. Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res. 29:1017-1026.