Monitoring hepatitis C virus (HCV) RNA-dependent RNA polymerase oligomerization by a FRET-based in vitro system

Antiviral Research

Volumn 87, Issue 1, 2010, Pages 57-66

  Bellón Echeverría, Itxaso ^a   López Jiménez, Alberto José ^a   Clemente Casares, Pilar ^a   Mas, Antonio ^a  

^a University of Castilla La Mancha   (Spain)

Author keywords

FRET; HCV; Inhibitors; Oligomerization; RNA polymerase

Indexed keywords

NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; NONSTRUCTURAL PROTEIN 5B; PF 254027; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; CONTROLLED STUDY; DRUG PROTEIN BINDING; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEL MOBILITY SHIFT ASSAY; HEPATITIS C VIRUS; IN VITRO STUDY; IONIC STRENGTH; NONHUMAN; OLIGOMERIZATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENZYME INHIBITORS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEPACIVIRUS; HUMANS; MUTANT PROTEINS; POINT MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS; RNA VIRUSES;

EID: 77953538925     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2010.04.009     Document Type: Article

References (65)

1. Allison A.C. The role of membranes in the replication of animal viruses. Int. Rev. Exp. Pathol. 1971, 10:181-242.
2. Arkin M.R., Whitty A. The road less travelled: modulating signal transduction enzymes by inhibiting their protein-protein interactions. Curr. Opin. Chem. Biol. 2009, 13:284-290.
3. Behrens S.E., Tomei L., De Francesco R. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 1996, 15:12-22.
4. Biswal B.K., Wang M., Cherney M.M., Chan L., Yannopoulos C.G., Bilimoria D., Bedard J., James M.N. Non-nucleoside inhibitors binding to hepatitis C virus NS5B polymerase reveal a novel mechanism of inhibition. J. Mol. Biol. 2006, 361:33-45.
5. Caliguiri L.A., Tamm I. Membranous structures associated with translation and transcription of poliovirus RNA. Science 1969, 166:885-886.
6. Care S., Bignon C., Pelissier M.C., Blanc E., Canard B., Coutard B. The translation of recombinant proteins in E. coli can be improved by in silico generating and screening random libraries of a -70/+96 mRNA region with respect to the translation initiation codon. Nucleic Acids Res. 2008, 36:e6.
7. Carette J.E., van Lent J., MacFarlane S.A., Wellink J., van Kammen A. Cowpea mosaic virus 32- and 60-kilodalton replication proteins target and change the morphology of endoplasmic reticulum membranes. J. Virol. 2002, 76:6293-6301.
8. Chinnaswamy, S., Murali, A., Li, P., Fujisaki, K., Kao, C.C., 2010. Regulation of de novo initiated RNA synthesis in the hepatitis C virus RNA dependent RNA polymerase by intermolecular interactions. J Virol. 2010 Apr 7. [Epub ahead of print], doi:10.1128/JVI.02446-09.
9. Choi Y.W., Tan Y.J., Lim S.G., Hong W., Goh P.Y. Proteomic approach identifies HSP27 as an interacting partner of the hepatitis C virus NS5A protein. Biochem. Biophys. Res. Commun. 2004, 318:514-519.
10. Cramer J., Jaeger J., Restle T. Biochemical and pre-steady-state kinetic characterization of the hepatitis C virus RNA polymerase (NS5Bdelta21, HC-J4). Biochemistry 2006, 45:3610-3619.
11. De Francesco R., Migliaccio G. Challenges and successes in developing new therapies for hepatitis C. Nature 2005, 436:953-960.
12. Denison M.R. Seeking membranes: positive-strand RNA virus replication complexes. PLoS Biol. 2008, 6:e270. 10.1371/journal.pbio.0060270.
13. Di Marco S., Volpari C., Tomei L., Altamura S., Harper S., Narjes F., Koch U., Rowley M., De Francesco R., Migliaccio G., Carfí A. Interdomain communication in hepatitis C virus polymerase abolished by small molecule inhibitors bound to a novel allosteric site. J. Biol. Chem. 2005, 280:29765-29770.
14. Dimitrova M., Imbert I., Kieny M.P., Schuster C. Protein-protein interactions between hepatitis c virus nonstructural proteins. J. Virol. 2003, 77:5401-5414.
15. Dye B.T., Miller D.J., Ahlquist P. In vivo self-interaction of nodavirus RNA replicase protein a revealed by fluorescence resonance energy transfer. J. Virol. 2005, 79:8909-8919.
16. Egger D., Wölk B., Gosert R., Bianchi L., Blum H.E., Moradpour D., Bienz K. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 2002, 76:5974-5984.
17. Ellis R.J. Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 2001, 26:597-604.
18. Förster T. Delocalized Excitation and Excitation Transfer 1965, Academic Press, Inc., New York, NY, pp. 93-137.
19. Gao L., Aizaki H., He J.W., Lai M.M. Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft. J. Virol. 2004, 78:3480-3488.
20. Goregaoker S.P., Culver J.N. Oligomerization and activity of the helicase domain of the tobacco mosaic virus 126- and 183-kilodalton replicase proteins. J. Virol. 2003, 77:3549-3556.
21. Gosert R., Kanjanahaluethai A., Egger D., Bienz K., Baker S.C. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 2002, 76:3697-3708.
22. Gosert R., Egger D., Lohmann V., Bartenschlager R., Blum H.E., Bienz K., Moradpour D. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J. Virol. 2003, 77:5487-5492.
23. Gu B., Gutshall L.L., Maley D., Pruss C.M., Nguyen T.T., Silverman C.L., Lin-Goerke J., Khandekar S., Liu C., Baker A.E., Casper D.J., Sarisky R.T. Mapping cooperative activity of the hepatitis C virus RNA-dependent RNA polymerase using genotype 1a-1b chimeras. Biochem. Biophys. Res. Commun. 2004, 313:343-350.
24. Hamamoto I., Nishimura Y., Okamoto T., Aizaki H., Liu M., Mori Y., Abe T., Suzuki T., Lai M.M., Miyamura T., Moriishi K., Matsuura Y. Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B. J. Virol. 2005, 79:13473-13482.
25. Hatta T., Francki R.I.B. Cytopathic structures associated with tonoplasts of plant cells infected with cucumber mosaic and tomato aspermy viruses. J. Gen. Virol. 1981, 53:343-346.
26. Heck J.A., Lam A.M., Narayanan N., Frick D.N. Effects of mutagenic and chain-terminating nucleotide analogs on enzymes isolated from hepatitis C virus strains of various genotypes. Antimicrob. Agents Chemother. 2008, 52:1901-1911.
27. Hobson S.D., Rosenblum E.S., Richards O.C., Richmond K., Kirkegaard K., Schultz S.C. Oligomeric structures of poliovirus polymerase are important for function. EMBO J. 2001, 20:1153-1163.
28. Högbom M., Jäger K., Robel I., Unge T., Rohayem J. The active form of the norovirus RNA-dependent RNA polymerase is a homodimer with cooperative activity. J. Gen. Virol. 2009, 90:281-291.
29. Kim K.S. An ultrastructural study of inclusions and disease in plant cells infected by cowpea chlorotic mottle virus. J. Gen. Virol. 1977, 35:535-543.
30. Kolykhalov A.A., Mihalik K., Feinstone S.M., Rice C.M. Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3' nontranslated region are essential for virus replication in vivo. J. Virol. 2000, 74:2046-2051.
31. Kopek B.G., Perkins G., Miller D.J., Ellisman M.H., Ahlquist P. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 2007, 5:e220. 10.1371/journal.pbio.0050220.
32. Kujala P., Ikäheimonen A., Ehsani N., Vihinen H., Auvinen P., Kääriäinen L. Biogenesis of the Semliki Forest virus RNA replication complex. J. Virol. 2001, 75:3873-3884.
33. Lavanchy D. Chronic viral hepatitis as a public health issue in the world. Best Pract. Res. Clin. Gastroenterol. 2008, 22:991-1008.
34. Lohmann V., Körner F., Herian U., Bartenschlager R. Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J. Virol. 1997, 71:8416-8428.
35. Love R.A., Parge H.E., Yu X., Hickey M.J., Diehl W., Gao J., Wriggers H., Ekker A., Wang L., Thomson J.A., Dragovich P.S., Furhman S.A. Crystallographic identification of a noncompetitive inhibitor binding site on the hepatitis C virus NS5B RNA polymerase enzyme. J. Virol. 2003, 77:7575-7581.
36. Lyle J.M., Bullitt E., Bienz K., Kirkegaard K. Visualization and functional analysis of RNA-dependent RNA polymerase lattices. Science 2002, 96:2218-2222.
37. Magliano D., Marshall J.A., Bowden D.S., Vardaxis N., Meanger J., Lee J.Y. Rubella virus replication complexes are virus-modified lysosomes. Virology 1998, 240:57-63.
38. Miller S., Krijnse-Locker J. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 2008, 6:363-374.
39. Miyawaki A., Tsien R.Y. Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol. 2000, 327:472-500.
40. O'Farrell D., Trowbridge R., Rowlands D., Jäger J. Substrate complexes of hepatitis C virus RNA polymerase (HC-J4): structural evidence for nucleotide import and de-novo initiation. J. Mol. Biol. 2003, 326:1025-1103.
41. O'Reilly E.K., Paul J.D., Kao C.C. Analysis of the interaction of viral RNA replication proteins by using the yeast two-hybrid assay. J. Virol. 1997, 71:7526-7532.
42. Pata J.D., Schultz S.C., Kirkegaard K. Functional oligomerization of poliovirus RNA-dependent RNA polymerase. RNA 1995, 1:466-477.
43. Patterson G.H., Piston D.W., Barisas B.G. Förster distances between green fluorescent protein pairs. Anal. Biochem. 2000, 284:438-440.
44. Prod'homme D., Le Panse S., Drugeon G., Jupin I. Detection and subcellular localization of the turnip yellow mosaic virus 66K replication protein in infected cells. Virology 2001, 281:88-101.
45. Qin W., Yamashita T., Shirota Y., Lin Y., Wei W., Murakami S. Mutational analysis of the structure and functions of hepatitis C virus RNA-dependent RNA polymerase. Hepatology 2001, 33:728-737.
46. Qin W., Luo H., Nomura T., Hayashi N., Yamashita T., Murakami S. Oligomeric interaction of hepatitis C virus NS5B is critical for catalytic activity of RNA-dependent RNA polymerase. J. Biol. Chem. 2002, 277:2132-2137.
47. Quinkert D., Bartenschlager R., Lohmann V. Quantitative analysis of the hepatitis C virus replication complex. J. Virol. 2005, 79:13594-13605.
48. Ralph R.K., Bullivant S., Wojcik S.J. Cytoplasmic membranes, a possible site of tobacco mosaic virus RNA replication. Virology 1971, 43:713-716.
49. Schwartz M., Chen J., Janda M., Sullivan M., den Boon J., Ahlquist P. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell. 2002, 9:505-514.
50. Shi S.T., Herlihy K.J., Graham J.P., Nonomiya J., Rahavendran S.V., Skor H., Irvine R., Binford S., Tatlock J., Li H., Gonzalez J., Linton A., Patick A.K., Lewis C. Preclinical characterization of PF-00868554, a potent nonnucleoside inhibitor of the hepatitis C virus RNA-dependent RNA polymerase. Antimicrob. Agents Chemother. 2009, 53:2544-2552.
51. Shimakami T., Hijikata M., Luo H., Ma Y.Y., Kaneko S., Shimotohno K., Muralami S. Effect of interaction between hepatitis C virus NS5A and NS5B on hepatitis C virus RNA replication with the hepatitis C virus replicon. J. Virol. 2004, 78:2738-2748.
52. Shirota Y., Luo H., Qin W., Kaneko S., Yamashita T., Kobayashi K., Murakami S. Hepatitis C virus (HCV) NS5A binds RNA-dependent RNA polymerase (RdRP) NS5B and modulates RNA-dependent RNA polymerase activity. J. Biol. Chem. 2002, 277:11149-11155.
53. Smallwood S., Cevik B., Moyer S.A. Intragenic complementation and oligomerization of the L subunit of the sendai virus RNA polymerase. Virology 2002, 20:235-245.
54. Spagnolo J.F., Rossignol E., Bullitt E., Kirkegaard K. Enzymatic and nonenzymatic functions of viral RNA-dependent RNA polymerases within oligomeric arrays. RNA 2010, 16:382-393.
55. Sreevalsan T. Association of viral ribonucleic acid with cellular membranes in chick embryo cells infected with Sindbis virus. J. Virol. 1970, 6:438-444.
56. Taylor M.P., Kirkegaard K. Potential subversion of autophagosomal pathway by picornaviruses. Autophagy 2008, 4:286-289.
57. Tu H., Gao L., Shi S.T., Taylor D.R., Yang T., Mircheff A.K., Wen Y., Gorbalenya A.E., Hwang S.B., Lai M.M. Hepatitis C virus RNA polymerase and NS5A complex with a SNARE-like protein. Virology 1999, 263:30-41.
58. Wang Q.M., Hockman M.A., Staschke K., Johnson R.B., Case K.A., Lu J., Parsons S., Zhang F., Rathnachalam R., Kirkegaard K., Colacino J.M. Oligomerization and cooperative RNA synthesis activity of hepatitis C virus RNA-dependent RNA polymerase. J. Virol. 2002, 76:3865-3872.
59. Wang M., Ng K.K.S., Cherney M.M., Chan L., Yannopoulos C.G., Bedard J., Morin N., Nguyen-Ba N., Alaoui-Ismaili M.H., Bethell R.C., James M.N. Non-nucleoside analogue inhibitors bind to an allosteric site on HCV NS5B polymerase. Crystal structures and mechanism of inhibition. J. Biol. Chem. 2003, 278:9489-9495.
60. Webster D.P., Klenerman P., Collier J., Jeffery K.J. Development of novel treatments for hepatitis C. Lancet Infect. Dis. 2009, 9:108-117.
61. Welsch S., Miller S., Romero-Brey I., Merz A., Bleck C.K., Walther P., Fuller S.D., Antony C., Krijnse-Locker J., Bartenschlager R. Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microb. 2009, 5:365-375.
62. Westaway E., Mackenzie J., Kenney M., Jones M., Khromykh A. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 1997, 71:6650-6661.
63. Williams J.A., Woodbury D.M. Determination of extracellular and intracellular electrolytes in rat liver in vivo. J. Physiol. 1971, 212:85-99.
64. Zacharias D.A., Violin J.D., Newton A.C., Tsien R.Y. Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 2002, 296:913-916.
65. Zamoto-Niikura A., Terasaki K., Ikegami T., Peters C.J., Makino S. Rift valley fever virus L protein forms a biologically active oligomer. J. Virol. 2009, 83:12779-12789.