Recombinant viral RdRps can initiate RNA synthesis from circular templates

RNA

Volumn 12, Issue 2, 2006, Pages 303-312

  Ranjith Kumar, C T ^a   Kao, C C ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

Circular template; Elongation; Heparin; Hepatitis C virus; RNA dependent RNA polymerase; Ternary complex

Indexed keywords

GUANOSINE TRIPHOSPHATE; HEPARIN; RECOMBINANT ENZYME; RNA DIRECTED RNA POLYMERASE;

3' UNTRANSLATED REGION; ARTICLE; BACTERIOPHAGE; COMPLEX FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; FLAVIVIRUS; HEPATITIS C VIRUS; NONHUMAN; PRIORITY JOURNAL; RNA SYNTHESIS; TERMINAL SEQUENCE; VIRUS GENOME;

CATALYTIC DOMAIN; GUANOSINE TRIPHOSPHATE; HEPACIVIRUS; HEPARIN; MUTATION; RECOMBINANT PROTEINS; RNA; RNA REPLICASE; TEMPLATES, GENETIC; VIRAL NONSTRUCTURAL PROTEINS;

FLAVIVIRUS; HEPATITIS C VIRUS; PSEUDOMONAS;

EID: 31044446937     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2163106     Document Type: Article

References (64)

1. Adkins, S., Stawicki, S.S., Faurote, G., Siegel, R.W., and Kao, C.C. 1998. Mechanistic analysis of RNA synthesis by RNA-dependent RNA polymerase from two promoters reveals similarities to DNAdependent RNA polymerase. RNA 4: 455-470.
2. Ago, H., Adachi, T., Yoshida, A., Yamamoto, M., Habuka, N., Yatsunami, K., and Miyano, M. 1999. Crystal structure of the RNAdependent RNA polymerase of hepatitis C virus. Struct. Fold. Des. 7: 1417-1426.
3. 2+. Biochemistry 43: 5126-5137.
4. Arnold, J.J., Vignuzzi, M., Stone, J.K., Andino, R., and Cameron, C.E. 2005. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J. Biol. Chem. 280: 25706-25716.
5. 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.
6. Biswal, B.K., Cherney, M.M., Wang, M., Chan, L., Yannopoulos, C.G., Bilimoria, D., Nicolas, O., Bedard, J., and James, M.N. 2005. Crystal structures of the RNA dependent RNA polymerase genotype 2a of hepatitis C virus reveal two conformations and suggest mechanisms of inhibition by non-nucleoside inhibitors. J. Biol. Chem. 280: 18202-18210.
7. Bressanelli, S., Tomei, L., Roussel, A., Incitti, I., Vitale, R.L., Mathieu, M., and DeFrancesco, R. 1999. Crystal structure of the RNAdependent RNA polymerase of hepatitis C virus. Proc. Natl. Acad. Sci. 96: 13034-13039.
8. Bressanelli, S., Tomei, L., Rey, F.A., and DeFrancesco, R. 2002. Structural analysis of the hepatitis C virus RNA polymerase in complex with ribonucleotides. J. Virol. 76: 3482-3492.
9. Butcher, S.J., Grimes, J.M., Makeyev, E.V., Bramford, D.H., and Stuart, D.I. 2001. A mechanism for initiating RNA-dependent RNA polymerization. Nature 410: 235-240.
10. Chapman, M.R. and Kao, C. 1999. A minimal RNA promoter for minus-strand RNA synthesis by the brome mosaic virus polymerase complex. J. Mol. Biol. 286: 709-720.
11. Choi, K.H., Groarke, J.M., Young, D.C., Kuhn, R.J., Smith, J.L., Pevear, D.C., and Rossmann, M.G. 2004a. The structure of the RNA-dependent RNA polymerase from bovine viral diarrhea virus establishes the role of GTP in de novo initiation. Proc. Natl. Acad. Sci. 30: 4425-4430.
12. Choi, S.K., Hema, M., Gopinath, K., Santos, J., and Kao, C. 2004b. Replicase-binding sites on plus- and minus-strand brome mosaic virus RNAs and their roles in RNA replication in plant cells. J. Virol. 78: 13420-13429.
13. Dahlberg, M.E. and Benkovic, S.J. 1991. Kinetic mechanism of DNA polymerase I (Klenow fragment): Identification of a second conformational change and evaluation of the internal equilibrium constant. Biochemistry 30: 4835-4843.
14. Dreher, T.W. 1999. Functions of the 3′-untranslated regions of positive strand RNA viral genomes. Annu. Rev. Phytopathol. 37: 151-174.
15. Ferrari, E., Wright-Minogue, J., Fang, J.W.S., Baroudy, B.M., Lau, J.Y.N., and Hong, Z. 1999. Characterization of soluble hepatitis C virus RNA-dependent RNA polymerase expressed in Escherichia coli. J. Virol. 73: 1649-1654.
16. Ferrer-Orta, C., Arias, A., Perez-Luque, R., Escarmis, C., Domingo, E., and Verdaguer, N. 2004. Structure of foot-and-mouth disease virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J. Biol. Chem. 279: 47212-47221.
17. Hansen, J.L., Long, A.M., and Schultz, S.C. 1997. Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5: 1109-1122.
18. 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.
19. Ishii, K., Tanaka, Y., Yap, C.C., Aizaki, H., Matsuura, Y., and Miyamura, T. 1999. Expression of hepatitis C virus NS5B protein: Characterization of its RNA polymerase activity and RNA binding. Hepatology 29: 1227-1235.
20. Joyce, C.M. and Steitz, T.A. 1995. Polymerase structures and function: Variations on a theme? J. Bacteriol. 177: 6321-6329.
21. Kao, C.C., Del Vecchio, A.M., and Zhong, W. 1999. De novo initiation of RNA synthesis by a recombinant flaviviridae RNA-dependent RNA polymerase. Virology 253: 1-7.
22. 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.
23. Kim, M.-J. and Kao, C.C. 2001. Factors regulating template switch in vitro by viral RNA-dependent RNA polymerases: Implications for RNA-RNA recombination. Proc. Natl. Acad. Sci. 98: 4972-4977.
24. Krieger, N., Lohmann, V., and Bartenschlager, R. 2001. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J. Virol. 75: 4614-4624.
25. Laurila, M.R., Makeyev, E.V., and Bamford, D.H. 2002. Bacteriophage φ 6 RNA-dependent RNA polymerase: Molecular details of initiating nucleic acid synthesis without primer. J. Biol. Chem. 277: 17117-17124.
26. Lesberg, 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.
27. Li, M.L. and Stollar, V. 2004. Identification of the amino acid sequence in Sindbis virus nsP4 that binds to the promoter for the synthesis of the subgenomic RNA. Proc. Natl. Acad. Sci. 101: 9429-9434.
28. Li, Y., Korolev, S., and Waksman, G. 1998. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: Structural basis for nucleotide incorporation. EMBO J. 17: 7514-7525.
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., Roos, A., Korner, F., Koch, J.O., and Bartenschlager, R. 1998. Biochemical and kinetic analyses of NS5B RNA-dependent RNA polymerase of the hepatitis C virus. Virology 249: 108-118.
31. Love, R.A., Maegley, K.A., Yu, X., Ferre, R.A., Lingardo, L.K., Diehl, W., Parge, H.E., Dragovich, P.S., and Fuhrman, S.A. 2004. The crystal structure of the RNA-dependent RNA polymerase from human rhinovirus: A dual function target for common cold antiviral therapy. Structure 12: 1533-1544.
32. Makeyev, E.V. and Bamford, D.H. 2000. Replicase activity of purified recombinant protein P2 of double-stranded RNA bacteriophage φ6. EMBO J. 19: 124-133.
33. McClure, W.R. 1985. Mechanism and control of transcription initiation in prokaryotes. Annu. Rev. Biochem. 54: 171-204.
34. Nagy, P.D., Carpenter, C.D., and Simon, A.E. 1997. A novel 3′-end repair mechanism in an RNA virus. Proc. Natl. Acad. Sci. 94: 1113-1118.
35. Ng, K.K., Cherney, M.M., Vazquez, A.L., Machin, A., Alonso, J.M., Parra, F., and James, M.N. 2002. Crystal structures of active and inactive conformations of a caliciviral RNA-dependent RNA polymerase. J. Biol. Chem. 277: 1381-1387.
36. Oh, J.W., Ito, T., and Lai, M.M. 1999. A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the fulllength viral RNA. J. Virol. 73: 7694-7702.
37. Ollis, D.L., Brick, P., Hamlin, R., Xuong, N.G., and Steitz, T.A. 1985a. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 313: 762-766.
38. Ollis, D.L., Kline, C., and Steitz, T.A. 1985b. Domain of E. coli DNA polymerase I showing sequence homology to T7 DNA polymerase. Nature 313: 818-819.
39. Panavas, T., Pogany, J., and Nagy, P.D. 2002. Internal initiation by the cucumber necrosis virus RNA-dependent RNA polymerase is facilitated by promoter-like sequences. Virology 296: 275-287.
40. Pogany, J., Fabian, M.R., White, K.A., and Nagy, P.D. 2003. A replication enhancer element in a plus-strand RNA virus. EMBO J. 22: 5602-5611.
41. Ranjith-Kumar, C.T., Gajewski, J., Gutshall, L., Maley, D., Sarisky, R., and Kao, C. 2001. Viral RNA-dependent RNA polymerase has terminal transferase activity: Implications for viral RNA synthesis J. Virol. 75: 8615-8623.
42. Ranjith-Kumar, C.T., Gutshall, L., Kim, M.-J., Sarisky, R.T., and Kao, C.C. 2002a. Requirements for de novo initiation of RNA synthesis by recombinant flaviviral RNA-dependent RNA polymerases. J. Virol. 76: 12526-12536.
43. Ranjith-Kumar, C.T., Kim, Y.C., Gutshall, L., Silverman, C., Khandekar, S., Sarisky, R.T., and Kao, C.C. 2002b. Mechanism of de novo initiation by the hepatitis C virus RNA-dependent RNA polymerase: Role of divalent metals. J. Virol. 76: 12513-12525.
44. Ranjith-Kumar, C.T., Gutshall, L., Sarisky, R.T., and Kao, C.C. 2003a. Multiple interactions within the hepatitis C virus RNA polymerase repress primer-dependent RNA synthesis. J. Mol. Biol. 330: 675-685.
45. Ranjith-Kumar, C.T., Santos, J.L., Gutshall, L.L., Johnston, V.K., Lin-Goerke, J., Kim, M.-J., Porter, D.J., Maley, D., Greenwood, C., Earnshaw, D.L., et al. 2003b. Enzymatic activities of the GB virus-B RNA-dependent RNA polymerase. Virology 312: 270-280.
46. Ranjith-Kumar, C.T., Sarisky, R.T., Gutshall, L., Thomson, M., and Kao, C.C. 2004. De novo initiation pocket mutations have multiple effects on hepatitis C virus RNA-dependent RNA polymerase activities. J. Virol. 78: 12207-12217.
47. Rao, A.L.N. and Hall, T.C. 1993. Recombination and polymerase error facilitate restoration of infectivity in brome mosaic virus. J. Virol. 67: 969-979.
48. Rao, A.L.N., Dreher, T.W., Marsh, L.E., and Hall, T.C. 1989. Telomeric function of the transfer RNA-like structure of brome mosaic virus RNA. Proc. Natl. Acad. Sci. 86: 5335-5339.
49. Sarafianos, S.G., Clark Jr., A.D., Das, K., Tuske, S., Birktoft, J.J., Ilankumaran, P., Ramesha, A.R., Sayer, J.M., Jerina, D.M., Boyer, P.L., et al. 2002. Structures of HIV-1 reverse transcriptase with preand post-translocation AZTMP-terminated DNA. EMBO J. 21: 6614-6624.
50. Schuppli, D., Georgijevic, J., and Weber, H. 2000. Synergism of mutations in bacteriophage Qβ affecting host factor dependence of Qβ replicase. J. Mol. Biol. 295: 149-154.
51. Siegel, R.W., Adkins, S., and Kao, C.C. 1997. Sequence-specific recognition of a subgenomic promoter by a viral RNA polymerase. Proc. Natl. Acad. Sci. 94: 11238-11243.
52. Siegel, R.W., Bellon, L., Beigelman, L., and Kao, C.C. 1998. Moieties in an RNA promoter specifically recognized by a viral RNA-dependent RNA polymerase. Proc. Natl. Acad. Sci. 95: 11613-11618.
53. Steitz, T.A. 1999. DNA polymerases: Structural diversity and common mechanisms. J. Biol. Chem. 274: 17395-17398.
54. _. 2004. The structural basis of the transition from initiation to elongation phases of transcription, as well as translocation and strand separation, by T7 RNA polymerase. Curr. Opin. Struct. Biol. 14: 4-9.
55. Sun, J.H. and Kao, C.C. 1997a. RNA synthesis by the brome mosaic virus RNA-dependent RNA polymerase: Transition from initiation to elongation. Virology 233: 63-73.
56. _. 1997b. Characterization of RNA products associated with or aborted by a viral RNA-dependent RNA polymerase. Virology 236: 348-353.
57. Sun, J.H., Adkins, S., Faurote, G., and Kao, C.C. 1996. Initiation of (-)-strand RNA synthesis catalyzed by the BMV RNA-dependent RNA polymerase: Synthesis of oligonucleotides. Virology 226: 1-12.
58. van den Hoff, M.J., Moorman, A.F., and Lamers, W.H. 1992. Electroporation in 'intracellular' buffer increases cell survival. Nucleic Acids Res. 20: 2902.
59. 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.
60. Vo, N.V., Tuler, J.R., and Lai, M.M. 2004. 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 43: 10579-10591.
61. von Hippel, P.H., Bear, D.G., Morgan, W.D., and McSwiggen, J.A. 1984. Protein-nucleic acid interactions in transcription: A molecular analysis. Annu. Rev. Biochem. 53: 389-446.
62. Wong, I., Patel, S.S., and Johnson, K.A. 1991. An induced-fit kinetic mechanism for DNA replication fidelity: Direct measurement by single-turnover kinetics. Biochemistry 30: 526-537.
63. Zheng, W., Brooks, B.R., Doniach, S., and Thirumalai, D. 2005. Network of dynamically important residues in the open/closed transition in polymerases is strongly conserved. Structure 13: 565-577.
64. 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.