Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3' nontranslated region are essential for virus replication in vivo

Journal of Virology

Volumn 74, Issue 4, 2000, Pages 2046-2051

  Kolykhalov, Alexander A ^a   Mihalik, Kathy ^b   Feinstone, Stephen M ^b   Rice, Charles M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; PROTEINASE; RNA DIRECTED RNA POLYMERASE; SERINE PROTEINASE;

ANIMAL MODEL; ARTICLE; ENZYME ACTIVITY; HEPATITIS C VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; VIREMIA; VIRUS INFECTIVITY; VIRUS REPLICATION;

3' UNTRANSLATED REGIONS; CYSTEINE ENDOPEPTIDASES; DNA, COMPLEMENTARY; DNA, VIRAL; ENZYME PRECURSORS; HEPACIVIRUS; HUMANS; MUTAGENESIS; RNA REPLICASE; RNA, VIRAL; SERINE ENDOPEPTIDASES; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 0033920304     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.4.2046-2051.2000     Document Type: Article

References (58)

1. Bassett, S. E., K. M. Brasky, and R. E. Lanford. 1998. Analysis of hepatitis C virus-inoculated chimpanzees reveals unexpected clinical profiles. J. Virol. 72:2589-2599.
2. Bassett, S. E., D. L. Thomas, K. M. Brasky, and R. E. Lanford. 1999. Viral persistence, antibody to E1 and E2, and hypervariable region 1 sequence stability in hepatitis C virus-inoculated chimpanzees. J. Virol. 73:1118-1126.
3. Beard, M. R., G. Abell, M. Honda, A. Carroll, M. Gartland, B. Clarke, K. Suzuki, R. Lanford, D. V. Sangar, and S. M. Lemon. 1999. An infectious molecular clone of a Japanese genotype 1b hepatitis C virus. Hepatology 30:315-324.
4. Behrens, S.-E., C. W. Grassmann. H.-J. Thiel, G. Meyers, and N. Tautz. 1998. Characterization of an autonomous subgenomic pestivirus RNA replicon. J. Virol. 72:2364-2372.
5. Behrens, S. E., L. Tomei, and R. DeFrancesco. 1996. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 15:12-22.
6. Blight, K. J., and C. M. Rice. 1997. Secondary structure determination of the conserved 98-hase sequence at the 3′ terminus of hepatitis C virus genome RNA. J. Virol. 71:7345-7352.
7. Boyer, J. C., K. Bebenek, and T. A. Kunkel. 1992. Unequal human immunodeficiency virus type 1 reverse transcriptase error rates with RNA and DNA templates. Proc. Natl. Acad. Sci. USA 89:6919-6923.
8. Chambers, T. J., A. Grakoui, and C. M. Rice. 1991. Processing of the yellow fever virus nonstructural polyprotein: a catalytically active NS3 proteinase domain and NS2B are required for cleavages at dibasic sites. J. Virol. 65: 6042-6050.
9. Chambers, T. J., A. Nestorowicz, and C. M. Rice. 1995. Mutagenesis of the yellow fever virus NS2B/3 cleavage site: determinants of cleavage site specificity and effects on polyprotein processing and viral replication. J. Virol. 69:1600-1605.
10. Chambers, T. J., R. C. Weir, A. Grakoui, D. W. McCourt, J. F. Bazan, R. J. Fletterick, and C. M. Rice. 1990. Evidence that the N-terminal domain of nonstructural protein NS3 from yellow fever virus is a serine protease responsible for site-specific cleavages in the viral polyprotein. Proc. Natl. Acad. Sci. USA 87:8898-8902.
11. Chung, R. T., and L. M. Kaplan. 1999. Heterogeneous nuclear ribonucleoprotein I (hnRNP-I/PTB) selectively binds the conserved 3′ terminus of hepatitis C viral RNA. Biochem. Biophys. Res. Commun. 254:351-362.
12. Cooper, S., A. L. Erickson, E. J. Adams, J. Kansopon, A. J. Weiner, D. Y. Chien, M. Houghton, P. Parham, and C. M. Walker. 1999. Analysis of a successful immune response against hepatitis C virus. Immunity 10:439-449.
13. Dash, S., A.-B. Halim, H. Tsuji, N. Hiramatsu, and M. A. Gerber. 1997. Transfection of HepG2 cells with infectious hepatitis C virus genome. Am. J. Pathol. 151:363-373.
14. D'Souza, E. D., E. O'Sullivan, E. M. Amphlett, D. J. Rowlands, D. V. Sangar, and B. E. Clarke. 1994. Analysis of NS3-mediated processing of the hepatitis C virus non-structural region in vitro. J. Gen. Virol. 75:3469-3476.
15. Failla, C., L. Tomei, and R. DeFrancesco. 1994. Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins. J. Virol. 68:3753-3760.
16. Gorbalenya, A. E., E. V. Koonin, A. P. Donchenko, and V. M. Blinov. 1989. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 17:4713-4729.
17. Grakoui, A., D. W. McCourt, C. Wychowski, S. M. Feinstone, and C. M. Rice. 1993. Characterization of the hepatitis C virus-encoded serine proteinase: determination of proteinase-dependent polyprotein cleavage sites. J. Virol. 67:2832-2843.
18. Grakoui, A., D. W. McCourt, C. Wychowski, S. M. Feinstone, and C. M. Rice. 1993. A second hepatitis C virus-encoded proteinase. Proc. Natl. Acad. Sci. USA 90:10583-10587.
19. Gross, C. H., and S. Shuman. 1995. Mutational analysis of vaccinia virus nucleoside triphosphate phosphohydrolase II, a DExH box RNA helicase. J. Virol. 69:4727-4736.
20. Han, J. H., V. Shyamala, K. H. Richman, M. J. Brauer, B. Irvine, M. S. Urdea, P. Tekamp-Olson, G. Kuo, Q.-L. Choo, and M. Houghton. 1991. Characterization of the terminal regions of hepatitis C viral RNA: identification of conserved sequences in the 5′ untranslated region and poly(A) tails at the 3′ end. Proc. Natl. Acad. Sci. USA 88:1711-1715.
21. Hayashi, N., H. Higashi, K. Kaminaka, H. Sugimoto, M. Esumi, K. Komatsu, K. Hayashi, M. Sugitani, K. Suzuki, O. Tadao, C. Nozaki, K. Mizuno, and T. Shikata. 1993. Molecular cloning and heterogeneity of the human hepatitis C virus (HCV) genome. J. Hepatol. 17(Suppl. 3):S94-S107.
22. Hijikata, M., H. Mizushima, T. Akagi, S. Mori, N. Kakiuchi, N. Kato, T. Tanaka, K. Kimura, and K. Shimotohno. 1993. Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J. Virol. 67:4665-4675.
23. Hong, Z., M. Beaudet-Miller, R. E. Lanford, B. Guerra, J. Wright-Minogue, A. Skelton, B. M. Baroudy, G. R. Reyes, and J. Y. N. Lau. 1999. Generation of transmissible hepatitis C virions from a molecular clone in chimpanzees. Virology 256:36-44.
24. Hoofnagle, J. H. 1997. Hepatitis C: the clinical spectrum of disease. Hepatology 26:15S-20S.
25. Houghton, M. 1996. Hepatitis C viruses, p. 1035-1058. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology. Raven Press, Philadelphia, Pa.
26. Ishii, K., Y. Tanaka, C. C. Yap, H. Aizaki, Y. Matsuura, and T. Miyamura. 1999. Expression of hepatitis C virus NS5B protein: characterization of its RNA polymerase activity and RNA binding. Hepatology 29:1227-1235.
27. Ito, T., and M. M. C. Lai. 1997. Determination of the secondary structure of and cellular protein binding to the 3′-untranslated region of the hepatitis C virus RNA genome. J. Virol. 71:8698-8706.
28. Ito, T., S. M. Tahara, and M. M. C. Lai. 1998. The 3′-untranslated region of hepatitis C virus RNA enhances translation from an internal ribosomal entry site. J. Virol. 72:8789-3796.
29. Kadaré, G., and A.-L. Haenni. 1997. Virus-encoded RNA helicases. J. Virol. 71:2583-2590.
30. Kato, N., M. Hijikata, Y. Ootsuyama, M. Nakagawa, S. Ohkoshi, T. Sugimura, and K. Shimotohno. 1990. Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc. Natl. Acad. Sci. USA 87:9524-9528.
31. Kolykhalov, A. A., E. V. Agapov, K. J. Blight, K. Mihalik, S. M. Feinstone, and C. M. Rice. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570-574.
32. Kolykhalov, A. A., E. V. Agapov, and C. M. Rice. 1994. Specificity of the hepatitis C virus serine proteinase: effects of substitutions at the 3/4A, 4A/ 4B, 4B/5A, and 5A/5B cleavage sites on polyprotein processing. J. Virol. 68:7525-7533.
33. Kolykhalov, A. A., S. M. Feinstone, and C. M. Rice. 1996. Identification of a highly conserved sequence element at the 3′ terminus of hepatitis C virus genome RNA. J. Virol. 70:3363-3371.
34. Lemon, S. H., and M. Honda. 1997. Internal ribosome entry sites within the RNA genomes of hepatitis C virus and other flaviviruses. Semin. Virol. 8:274-288.
35. Lin, C., B. D. Lindenbach, B. Prágai, D. W. McCourt, and C. M. Rice. 1994. Processing of the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini. J. Virol. 68:5063-5073.
36. Lin, C., B. Prágai, A. Grakoui, J. Xu, and C. M. Rice. 1994. Hepatitis C virus NS3 serine proteinase: trans-cleavage requirements and processing kinetics. J. Virol. 68:8147-8157.
37. Lindsay, K. L. 1997. Therapy of hepatitis C: overview. Hepatology 26:71S-77S.
38. Lohmann, V., F. Körner, U. Herian, and R. Bartenschlager. 1997. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J. Virol. 71:8416-8428.
39. Luo, G. 1999. Cellular proteins bind to the poly(U) tract of the 3′ untranslated region of hepatitis C virus RNA genome. Virology 256:105-118.
40. Meyers, G., and H.-J. Thiel. 1996. Molecular characterization of pestiviruses. Adv. Virus Res. 47:53-118.
41. Mizushima, H., H. Hijikata, S.-I. Asabe, M. Hirota, K. Kimura, and K. Shimotohno. 1994. Two hepatitis C virus glycoprotein E2 products with different C termini. J. Virol. 68:6215-6222.
42. Okamoto, H., S. Okada, Y. Sugiyama, K. Kurai, H. Iizuka, A. Machida, Y. Miyakawa, and M. Mayumi. 1991. Nucleotide sequence of the genomic RNA of hepatitis C virus isolated from a human carrier: comparison with reported isolates for conserved and divergent regions. J. Gen. Virol. 72: 2697-2704.
43. O'Reilly, E. K., and C. C. Kao. 1998. Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure. Virology 252:287-303.
44. Pai, E. F., U. Krengel, G. A. Petsko, R. S. Gody, W. Katsh, and A. Wittinghofer. 1990. Refined crystal structure of the triphosphate conformation of H-Ras p21 at 1.35A resolution: implications for the mechanism of GTP hydrolysis. EMBO J. 9:2351-2359.
45. Reed, K. E., and C. M. Rice. 1999. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr. Top. Microbiol. Immunol. 242:55-84.
46. Reichard, O., R. Schvarez, and O. Weiland. 1997. Therapy of hepatitis C: alpha interferon and ribavirin. Hepatology 26:108S-111S.
47. Rice, C. M. 1996. Flaviviridae: the viruses and their replication, p. 931-960. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology. Lippincott-Raven Publishers, Philadelphia, Pa.
48. Selby, M. J., E. Glazer, F. Masiarz, and M. Houghton. 1994. Complex processing and protein:protein interactions in the E2:NS2 region of HCV. Virology 204:114-122.
49. Tanaka, T., N. Kato, M.-J. Cho, and K. Shimotohno. 1995. A novel sequence found at the 3′ terminus of hepatitis C virus genome. Biochem. Biophys. Res. Commun. 215:744-749.
50. Tanaka, T., N. Kato, M.-J. Cho, K. Sugiyama, and K. Shimotohno. 1996. Structure of the 3′ terminus of the hepatitis C virus genome. J. Virol. 70:3307-3312.
51. Tokita, H., H. Okamoto, H. Iizuka, J. Kishimoto, F. Tsuda, Y. Miyakawa, and M. Mayumi. 1998. The entire nucleotide sequences of three hepatitis C virus isolates in genetic groups 7-9 and comparison with those in the other eight genetic groups. J. Gen. Virol. 79:1847-1857.
52. Tsuchihara, K., T. Tanaka, M. Hijikata, S. Kuge, H. Toyoda, A. Nomoto, N. Yamamoto, and K. Shimotohno. 1997. Specific interaction of polypyrimidine tract-binding protein with the extreme 3′-terminal structure of the hepatitis C virus genome, the 3′X. J. Virol. 71:6720-6726.
53. Xu, J., E. Mendez, P. R. Caron, C. Lin, M. A. Murcko, M. S. Collett, and C. M. Rice. 1997. Bovine viral diarrhea virus NS3 serine proteinase: polyprotein cleavage sites, cofactor requirements, and molecular model of an enzyme essential for pestivirus replication. J. Virol. 71:5312-5322.
54. Yamada, N., K. Tanihara, A. Takada, T. Yorihuzi, M. Tsutsumi, H. Shimomura, T. Tsuji, and T. Date. 1996. Genetic organization and diversity of the 3′ noncoding region of the hepatitis C virus genome. Virology 223:255-261.
55. Yanagi, M., R. H. Purcell, S. U. Emerson, and J. Bukh. 1997. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. Proc. Natl. Acad. Sci. USA 94:8738-8743.
56. Yanagi, M., M. St. Claire, S. U. Emerson, R. H. Purcell, and J. Bukh. 1999. In vivo analysis of the 3′ untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc. Natl. Acad. Sci. USA 96:2291-2295.
57. Yanagi, M., M. St. Claire, M. Shapiro, S. U. Emerson, R. H. Purcell, and J. Bukh. 1998. Transcripts of a chimeric cDNA clone of hepatitis C virus genotype 1b are infectious in vivo. Virology 244:161-172.
58. Yoo, B. J., M. Selby, J. Choe, B. S. Suh, S. H. Choi, J. S. Joh, G. J. Nuovo, H.-S. Lee, M. Houghton, and J. H. Han. 1995. Transfection of a differentiated human hepatoma cell line (Huh7) with in vitro-transcribed hepatitis C virus (HCV) RNA and establishment of a long-term culture persistently infected with HCV. J. Virol. 69:32-38.