Enzymatic characterization of the full-length and C-terminally truncated hepatitis C virus RNA polymerases: Function of the last 21 amino acids of the C terminus in template binding and RNA synthesis

Biochemistry

Volumn 43, Issue 32, 2004, Pages 10579-10591

  Vo, Nam Viet ^a   Tuler, Jerry R ^a   Lai, Michael M C ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b HMR 401 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CONCENTRATION (PROCESS); ENZYMES; HYDROPHOBICITY; POLYPEPTIDES; PROTEINS; RNA; SYNTHESIS (CHEMICAL);

MONOVALENTS; NONSTRUCTURAL PROTEINS;

BIOCHEMISTRY;

AMINO ACID; AROMATIC AMINO ACID; POTASSIUM CHLORIDE; RNA; RNA POLYMERASE; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHEMICAL ANALYSIS; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STABILITY; HEPATITIS C VIRUS; IN VITRO STUDY; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RNA SYNTHESIS; VIRUS REPLICATION;

BASE SEQUENCE; BINDING SITES; DNA NUCLEOTIDYLEXOTRANSFERASE; HEPACIVIRUS; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; POTASSIUM CHLORIDE; RECOMBINANT FUSION PROTEINS; RNA REPLICASE; RNA, VIRAL; SEQUENCE DELETION; SUBSTRATE SPECIFICITY; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

HEPATITIS C VIRUS; RNA VIRUSES;

EID: 4043080522     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049773g     Document Type: Article

References (48)

1. Adachi, T. H., Ago, N., Habuka, K., Okuda, M., Komatsu, S., Ikeda, and Yatsunami, K. (2002) The essential role of C-terminal residues in regulating the activity of hepatitis C virus RNA-dependent RNA polymerase, Biochim. Biophys. Acta 1601, 38-48.
2. Altmann, C. R., Solow-Cordero, D. E., and Chamberlin, M. J. (1994) RNA cleavage and chain elongation by Escherichia coli DNA-dependent RNA polymerase in a binary enzyme. RNA complex, Proc. Natl. Acad. Sci. U.S.A. 91, 3784-3788.
3. Arnold, J. J., Ghosh, S. K., and Cameron, C. E. (1999) Poliovirus RNA-dependent RNA polymerase (3D(pol)). Divalent cation modulation of primer, template, and nucleotide selection, J. Biol. Chem. 274, 37060-37069.
4. Behrens, S. E., Tomei, L., and De Francesco, R. (1996) Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus, EMBO J. 15, 12-22.
5. Biroccio, A., Hamm, J., Incitti, I., De Francesco, R., and Tomei, L. (2002) Selection of RNA aptamers that are specific and high-affinity ligands of the hepatitis C virus RNA-dependent RNA polymerase, J. Virol. 76, 3688-3696.
6. Bressanelli, S., Tomei, L., Roussel, A., Incitti, I., Vitale, R. L., Mathieu, M., De Francesco, R., and Rey, F. A. (1999) Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus, Proc. Natl. Acad. Sci. U.S.A. 96, 13034-13039.
7. Butcher, S. J., Grimes, J. M., Makeyev, E. V., Bamford, D. H., and Stuart, D. I. (2001) A mechanism for initiating RNA-dependent RNA polymerization, Nature 410, 235-240.
8. Carroll, S. S., Sardana, V., Yang, Z., Jacobs, A. R., Mizenko, C., Hall, D., Hill, L., Zugay-Murphy, J., and Kuo, L. C. (2000) Only a small fraction of purified hepatitis C RNA-dependent RNA polymerase is catalytically competent: Implications for viral replication and in vitro assays, Biochemistry 39, 8243-8249.
9. Casas-Finet, J. R., Khamis, M. I., Maki, A. H., and Chase, J. W. (1987) Tryptophan 54 and phenylalanine 60 are involved synergistically in the binding of E. coli SSB protein to single-stranded polynucleotides, FEBS Lett. 220, 347-352.
10. Chamberlin, M. J. A. B. P. (1964) Mechanism of RNA polymerase action: Characterization of the DNA-dependent synthesis of polyadenylic acid, J. Mol. Biol. 8, 708-726.
11. Crotty, S., Maag, D., Arnold, J. J., Zhong, W., Lau, J. Y., Hong, Z., Andino, R., and Cameron, C. E. (2000) The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen, Nat. Med. 6, 1375-1379.
12. Ferrari, E., Wright-Minogue, J., Fang, J. W., Baroudy, B. M., Lau, J. Y., and Hong, Z. (1999) Characterization of soluble hepatitis C virus RNA-dependent RNA polymerase expressed in Escherichia coli, J. Virol. 73, 1649-1654.
13. Guan, H., and Simon, A. E. (2000) Polymerization of nontemplate bases before transcription initiation at the 3′ ends of templates by an RNA-dependent RNA polymerase: An activity involved in 3′ end repair of viral RNAs, Proc. Natl. Acad. Sci. U.S.A. 97, 12451-12456.
14. Hearne, P. Q., Knorr, D. A., Hillman, B. I., and Morris, T. J. (1990) The complete genome structure and synthesis of infectious RNA from clones of tomato bushy stunt virus, Virology 177, 141-151.
15. Helmann, J. D., and Chamberlin, M. J. (1988) Structure and function of bacterial sigma factors, Annu. Rev. Biochem. 57, 839-872.
16. Hong, Z., Cameron, C. E., Walker, M. P., Castro, C., Yao, N., Lau, J. Y., and Zhong, W. (2001) A novel mechanism to ensure terminal initiation by hepatitis C virus NS5B polymerase, Virology 285, 6-11.
17. Hwang, S. B., Park, K. J., Kim, Y. S., Sung, Y. C., and Lai, M. M. (1997) Hepatitis C virus NS5B protein is a membrane-associated phosphoprotein with a predominantly perinuclear localization, Virology 227, 439-446.
18. Ivashkina, N., Wolk, B., Lohmann, V., Bartenschlager, R., Blum, H. E., Penin, F., and Moradpour, D. (2002) The hepatitis C virus RNA-dependent RNA polymerase membrane insertion sequence is a transmembrane segment, J. Virol. 76, 13088-13093.
19. Johnson, T. L., and Chamberlin, M. J. (1994) Complexes of yeast RNA polymerase II and RNA are substrates for TFIIS-induced RNA cleavage, Cell 77, 217-224.
20. Kao, C. C., Yang, X., Kline, A., Wang, Q. M., Barket, D., and Heinz, B. A. (2000) Template requirements for RNA synthesis by a recombinant hepatitis C virus RNA-dependent RNA polymerase, J. Virol. 74, 11121-11128.
21. Kolykhalov, A. A., Mihalik, K., Feinstone, S. M., and Rice, C. M. (2000) Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3′ nontranslated region are essential for virus replication in vivo, J. Virol. 74, 2046-2051.
22. Koonin, E. V. (1993) A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication, Nucleic Acids Res. 21, 2541-2547.
23. Kumar, A., Casas-Finet, J. R., Luneau, C. J., Karpel, R. L., Merrill, B. M., Williams, K. R., and Wilson, S. H. (1990) Mammalian heterogeneous nuclear ribonucleoprotein A1. Nucleic acid binding properties of the COOH-terminal domain, J. Biol. Chem. 265, 17094-17100.
24. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity, Annu. Rev. Biochem. 69, 497-529.
25. Lauger, P. (1987) Dynamics of ion transport systems in membranes, Physiol. Rev. 67, 1296-1331.
26. Lee, K. J., Ou, C. J., and Lai, M. C. (2003) The C-terminal transmembrane domain of hepatitis C virus RNA polymerase is essential for HCV replication in vivo, J. Virol. 78, 3797-3802.
27. Lesburg, C. A., Cable, M. B., Ferrari, E., Hong, Z., Mannarino, A. F., and Weber, P. C. (1999) Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site, Nat. Struct. Biol. 6, 937-943.
28. Leveque, V. J., Johnson, R. B., Parsons, S., Ren, J., Xie, C., Zhang, F., and Wang, Q. M. (2003) Identification of a C-terminal regulatory motif in hepatitis C virus RNA-dependent RNA polymerase: Structural and biochemical analysis, J. Virol. 77, 9020-9028.
29. Lohmann, V., Korner, F., Herian, U., and Bartenschlager, R. (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.
30. Lohmann, V., Korner, F., Koch, J., Herian, U., Theilmann, L., and Bartenschlager, R. (1999) Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line, Science 285, 110-113.
31. Lohmann, V., Overton, H., and Bartenschlager, R. (1999) Selective stimulation of hepatitis C virus and pestivirus NS5B RNA polymerase activity by GTP, J. Biol. Chem. 274, 10807-10815.
32. Merrill, B. M., Stone, K. L., Cobianchi, F., Wilson, S. H., and Williams, K. R. (1988) Phenylalanines that are conserved among several RNA-binding proteins form part of a nucleic acid-binding pocket in the A1 heterogeneous nuclear ribonucleoprotein, J. Biol. Chem. 263, 3307-3313.
33. Milligan, J. F., Groebe, D. R., Witherell, G. W., and Uhlenbeck, O. C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates, Nucleic Acids Res. 15, 8783-8798.
34. Oh, J. W., Ito, T., and Lai, M. M. (1999) A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the full-length viral RNA, J. Virol. 73, 7694-7702.
35. Oh, J. W., Sheu, G. T., and Lai, M. M. (2000) Template requirement and initiation site selection by hepatitis C virus polymerase on a minimal viral RNA template, J. Biol. Chem. 275, 17710-17717.
36. O'Reilly, E. K., and Kao, C. C. (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.
37. Rajendran, K. S., and Nagy, P. D. (2003) Characterization of the RNA-binding domains in the replicase proteins of tomato bushy stunt virus, J. Virol. 77, 9244-9258.
38. Ranjith-Kumar, C. T., Gajewski, J., Gutshall, L., Maley, D., Sarisky, R. T., and Kao, C. C. (2001) Terminal nucleotidyl transferase activity of recombinant Flaviviridae RNA-dependent RNA polymerases, implication for viral RNA synthesis, J. Virol. 75, 8615-8623.
39. Ranjith-Kumar, C. T., Gutshall, L., Sarisky, R. T., and Kao, C. C. (2003) Multiple interactions within the hepatitis C virus RNA polymerase repress primer-dependent RNA synthesis, J. Mol. Biol. 330, 675-685.
40. Rhodes, G., and Chamberlin, M. J. (1974) Ribonucleic acid chain elongation by Escherichia coli ribonucleic acid polymerase. I. Isolation of ternary complexes and the kinetics of elongation, J. Biol. Chem. 249, 6675-6683.
41. Schmidt-Mende, J., Bieck, E., Hugle, T., Penin, F., Rice, C. M., Blum, H. E., and Moradpour, D. (2001) Determinants for membrane association of the hepatitis C virus RNA-dependent RNA polymerase, J. Biol. Chem. 276, 44052-44063.
42. Shi, S. T., Lee, K. J., Aizaki, H., Hwang, S. B., and Lai, M. M. (2003) Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2, J. Virol. 77, 4160-4168.
43. Siegel, R. W., Adkins, S., and Kao, C. C. (1997) Sequence-specific recognition of a subgenomic RNA promoter by a viral RNA polymerase, Proc. Natl. Acad. Sci. U.S.A. 94, 11238-11243.
44. Steiner, T., Kaiser, J. T., Marinkovic, S., Huber, R., and Wahl, M. C. (2002) Crystal structures of transcription factor NusG in light of its nucleic acid- and protein-binding activities, EMBO J. 21, 4641-4653.
45. Vo, N. V., Oh, J. W., and Lai, M. M. (2003) Identification of RNA ligands that bind hepatitis C virus polymerase selectively and inhibit its RNA synthesis from the natural viral RNA templates, Virology 307, 301-316.
46. Vo, N. V., Young, K. C., and Lai, M. M. (2003) Mutagenic and inhibitory effects of ribavirin on hepatitis C virus RNA polymerase, Biochemistry 42, 10462-10471.
47. Wang, Q. M., Hockman, M. A., Staschke, K., Johnson, R. B., Case, K. A., Lu, J., Parsons, S., Zhang, F., Rathnachalam, R., Kirkegaard, K., and Colacino, J. M. (2002) Oligomerization and cooperative RNA synthesis activity of hepatitis C virus RNA-dependent RNA polymerase, J. Virol. 76, 3865-3872.
48. Zhong, W., Ferrari, E., Lesburg, C. A., Maag, D., Ghosh, S. K., Cameron, C. E., Lau, J. Y., and Hong, Z. (2000) Template/primer requirements and single nucleotide incorporation by hepatitis C virus nonstructural protein 5B polymerase, J. Virol. 74, 9134-9143.