RNA-dependent RNA polymerases from different hepatitis C virus genotypes reveal distinct biochemical properties and drug susceptibilities

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 10, 2011, Pages 1325-1332

  May, Marina M ^a   Lorengel, Heike ^a   Kreuter, Joerg ^b   Zimmermann, Holger ^a   Ruebsamen Schaeff, Helga ^a   Urban, Andreas ^a  

^a AiCuris GmbH   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Genotype; HCV; Non nucleoside inhibitor; NS5B; RNA polymerase

Indexed keywords

RNA DIRECTED RNA POLYMERASE;

ARTICLE; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME SPECIFICITY; GENOTYPE; HEPATITIS C VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VIRAL GENETICS;

ANTIVIRAL AGENTS; BIOCHEMICAL PROCESSES; CATIONS, MONOVALENT; DRUG RESISTANCE, VIRAL; ENZYME ACTIVATION; ENZYME INHIBITORS; GENOTYPE; HEPACIVIRUS; HYDROGEN-ION CONCENTRATION; MAGNESIUM CHLORIDE; MODELS, BIOLOGICAL; RNA REPLICASE; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

HEPATITIS C VIRUS;

EID: 80051663203     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.05.006     Document Type: Article

References (42)

1. J.H. Hoofnagle Course and outcome of hepatitis C Hepatology 36 2002 S21 S29
2. M.W. Fried, M.L. Shiffman, K.R. Reddy, C. Smith, G. Marinos, F.L. Goncales Jr., D. Haussinger, M. Diago, G. Carosi, D. Dhumeaux, A. Craxi, A. Lin, J. Hoffman, and J. Yu Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection N. Engl. J. Med. 347 2002 975 982
3. M.P. Manns, J.G. McHutchison, S.C. Gordon, V.K. Rustgi, M. Shiffman, R. Reindollar, Z.D. Goodman, K. Koury, M. Ling, and J.K. Albrecht Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial Lancet 358 2001 958 965 (Pubitemid 32913521)
4. S.M. Kamal Hepatitis C virus genotype 4 therapy: progress and challenges Liver Int. 31 Suppl 1 2011 45 52
5. N. Ivashkina, B. Wolk, V. Lohmann, R. Bartenschlager, H.E. Blum, F. Penin, and D. Moradpour The hepatitis C virus RNA-dependent RNA polymerase membrane insertion sequence is a transmembrane segment J. Virol. 76 2002 13088 13093 (Pubitemid 35386995)
6. J. Schmidt-Mende, E. Bieck, T. Hugle, F. Penin, C.M. Rice, H.E. Blum, and D. Moradpour Determinants for membrane association of the hepatitis C virus RNA-dependent RNA polymerase J. Biol. Chem. 276 2001 44052 44063
7. S. Bressanelli, L. Tomei, A. Roussel, I. Incitti, R.L. Vitale, M. Mathieu, R. De Francesco, and F.A. Rey Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus Proc. Natl. Acad. Sci. U.S.A. 96 1999 13034 13039
8. C.A. Lesburg, M.B. Cable, E. Ferrari, Z. Hong, A.F. Mannarino, and P.C. Weber Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site Nat. Struct. Biol. 6 1999 937 943 (Pubitemid 29463307)
9. S.E. Behrens, L. Tomei, and R. De Francesco Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus EMBO J. 15 1996 12 22 (Pubitemid 26020384)
10. T. Adachi, H. Ago, N. Habuka, K. Okuda, M. Komatsu, S. Ikeda, and K. Yatsunami The essential role of C-terminal residues in regulating the activity of hepatitis C virus RNA-dependent RNA polymerase Biochim. Biophys. Acta 1601 2002 38 48 (Pubitemid 38234529)
11. F. Legrand-Abravanel, F. Nicot, and J. Izopet New NS5B polymerase inhibitors for hepatitis C Expert Opin. Investig. Drugs 19 2010 963 975
12. R.R. Deore, and J.W. Chern NS5B RNA dependent RNA polymerase inhibitors: the promising approach to treat hepatitis C virus infections Curr. Med. Chem. 17 2010 3806 3826
13. W.J. Watkins, A.S. Ray, and L.S. Chong HCV NS5B polymerase inhibitors Curr. Opin. Drug Discov. Devel. 13 2010 441 465
14. J. Botyanszki, C.D. Roberts, F.U. Schmitz, J.M. Gralapp, R.C. Griffith, D.-F. Shi, M.R. Leivers, and R.E. Brewster Indole Derivatives for Treating Viral Infections 2006 Genelabs Technologies Inc. USA
15. M. Wang, K.K. Ng, M.M. Cherney, L. Chan, C.G. Yannopoulos, J. Bedard, N. Morin, N. Nguyen-Ba, M.H. Alaoui-Ismaili, R.C. Bethell, and M.N. James Non-nucleoside analogue inhibitors bind to an allosteric site on HCV NS5B polymerase. Crystal structures and mechanism of inhibition J. Biol. Chem. 278 2003 9489 9495 (Pubitemid 36800441)
16. T.D. Bosse, D.P. Larson, R. Wagner, D.K. Hutchinson, T.W. Rockway, W.M. Kati, Y. Liu, S. Masse, T. Middleton, H. Mo, D. Montgomery, W. Jiang, G. Koev, D.J. Kempf, and A. Molla Synthesis and SAR of novel 1,1-dialkyl-2(1H)- naphthalenones as potent HCV polymerase inhibitors Bioorg. Med. Chem. Lett. 18 2008 568 570
17. A.Y. Howe, H. Cheng, S. Johann, S. Mullen, S.K. Chunduru, D.C. Young, J. Bard, R. Chopra, G. Krishnamurthy, T. Mansour, and J. O'Connell Molecular mechanism of hepatitis C virus replicon variants with reduced susceptibility to a benzofuran inhibitor, HCV-796 Antimicrob. Agents Chemother. 52 2008 3327 3338
18. A.U. Neumann, N.P. Lam, H. Dahari, D.R. Gretch, T.E. Wiley, T.J. Layden, and A.S. Perelson Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy Science 282 1998 103 107 (Pubitemid 28471138)
19. P. Simmonds, J. Bukh, C. Combet, G. Deleage, N. Enomoto, S. Feinstone, P. Halfon, G. Inchauspe, C. Kuiken, G. Maertens, M. Mizokami, D.G. Murphy, H. Okamoto, J.M. Pawlotsky, F. Penin, E. Sablon, I. Shin, L.J. Stuyver, H.J. Thiel, S. Viazov, A.J. Weiner, and A. Widell Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes Hepatology 42 2005 962 973 (Pubitemid 41401136)
20. F. Gray, L. Amphlett, H. Bright, L. Chambers, A. Cheasty, R. Fenwick, D. Haigh, D. Hartley, P. Howes, R. Jarvest, F. Mirzai, F. Nerozzi, N. Parry, M. Slater, S. Smith, P. Thommes, C. Wilkinson, and E. Williams GSK625433: a novel and highly potent inhibitor of the HCV NS5B polymerase 42nd Meeting of the European Association for the Study of Liver Diseases, Barcelona, Spain 2007
21. S.W. Ludmerer, D.J. Graham, E. Boots, E.M. Murray, A. Simcoe, E.J. Markel, J.A. Grobler, O.A. Flores, D.B. Olsen, D.J. Hazuda, and R.L. Lafemina Replication fitness and NS5B drug sensitivity of diverse hepatitis C virus isolates characterized by using a transient replication assay Antimicrob. Agents Chemother. 49 2005 2059 2069 (Pubitemid 40631625)
22. F. Pauwels, W. Mostmans, L.M. Quirynen, L. van der Helm, C.W. Boutton, A.S. Rueff, E. Cleiren, P. Raboisson, D. Surleraux, O. Nyanguile, and K.A. Simmen Binding-site identification and genotypic profiling of hepatitis C virus polymerase inhibitors J. Virol. 81 2007 6909 6919 (Pubitemid 46986627)
23. S.T. Shi, K.J. Herlihy, J.P. Graham, J. Nonomiya, S.V. Rahavendran, H. Skor, R. Irvine, S. Binford, J. Tatlock, H. Li, J. Gonzalez, A. Linton, A.K. Patick, and C. Lewis Preclinical characterization of PF-00868554, a potent nonnucleoside inhibitor of the hepatitis C Virus RNA-dependent RNA polymerase Antimicrob. Agents Chemother. 53 2009 2544 2552
24. K.J. Herlihy, J.P. Graham, R. Kumpf, A.K. Patick, R. Duggal, and S.T. Shi Development of intergenotypic chimeric replicons to determine the broad-spectrum antiviral activities of hepatitis C virus polymerase inhibitors Antimicrob. Agents Chemother. 52 2008 3523 3531
25. O. Nyanguile, B. Devogelaere, L. Vijgen, and B.W. Van Test 1a/1b subtype profiling of nonnucleoside polymerase inhibitors of hepatitis C virus J. Virol. 84 2010 2923 2934
26. R.L. Tripathi, P. Krishnan, Y. He, T. Middleton, T. Pilot-Matias, C.M. Chen, D.T. Lau, S.M. Lemon, H. Mo, W. Kati, and A. Molla Replication efficiency of chimeric replicon containing NS5A-5B genes derived from HCV-infected patient sera Antiviral Res. 73 2007 40 49 (Pubitemid 46080476)
27. L. Chan, O. Pereira, T.J. Reddy, S.K. Das, C. Poisson, M. Courchesne, M. Proulx, A. Siddiqui, C.G. Yannopoulos, N. Nguyen-Ba, C. Roy, D. Nasturica, C. Moinet, R. Bethell, M. Hamel, L. L'Heureux, M. David, O. Nicolas, P. Courtemanche-Asselin, S. Brunette, D. Bilimoria, and J. Bedard Discovery of thiophene-2-carboxylic acids as potent inhibitors of HCV NS5B polymerase and HCV subgenomic RNA replication. Part 2: tertiary amides Bioorg. Med. Chem. Lett. 14 2004 797 800 (Pubitemid 38114874)
28. N.M. Kneteman, A.Y. Howe, T. Gao, J. Lewis, D. Pevear, G. Lund, D. Douglas, D.F. Mercer, D.L. Tyrrell, F. Immermann, I. Chaudhary, J. Speth, S.A. Villano, J. O'Connell, and M. Collett HCV796: a selective nonstructural protein 5B polymerase inhibitor with potent anti-hepatitis C virus activity in vitro, in mice with chimeric human livers, and in humans infected with hepatitis C virus Hepatology 49 2009 745 752
29. A. Erhardt, H. Wedemeyer, Y. Benhamou, C. Moellekens, X. Forns, S. Pol, J.L. Calleja, S. Ross, H.C. Spangenberg, J. Garcia-Samaniego, M. Fuchs, J. Enriquez, J. Wiegand, J. Stern, K. Wu, G. Nehmiz, and J. Steffgen Safety, pharmacokinetics and antiviral effect of BILB1941, a novel HCV RNA polymerase inhibitor, after 5 days oral treatment in patients with chronic hepatitis C 42nd Annual Meeting of the European Association for the Study of the Liver, Barcelona, Spain 2007
30. E. Lawitz, C. Cooper, M. Rodriguez-Torres, R. Ghalib, R. Lalonde, A. Sheikh, B. Bourgault, N. Chauret, L. Proulx, and J. McHutchison Safety, tolerability and antiviral activity of VCH-916, a novel non-nucleoside HCV polymerase inhibitor in patients with chronic HCV genotype-1 infection 44th Annual Meeting of the European Association for the Study of the Liver, Copenhagen, Denmark 2009
31. E. Lawitz, M. Rodriguez-Torres, V.K. Rustgi, T. Hassanein, M.H. Rahimy, C.A. Crowley, J.L. Freddo, A. Muir, and J. McHutchison Safety and antiviral activity of ANA598 in combination with pegylated interferon alpha2a plus ribavirin in treatment-naive genotype-1 chronic HCV patients 45th Annual Meeting of the European Association for the Study of the Liver, Vienna, Austria 2010
32. P. Pockros, M. Rodriguez-Torres, S. Villano, E. Maller, and M. Chojkier A phase 2, randomized study of HCV-796 in combination with pegylated-interferon (PEG) plus ribavirin (RBV) versus PEG Plus RBV in hepatitis C virus genotype-1 infection 44th Annual Meeting of the European Association for the Study of the Liver, Copenhagen, Denmark 2010
33. S. Le Pogam, A. Seshaadri, A. Kosaka, S. Chiu, H. Kang, S. Hu, S. Rajyaguru, J. Symons, N. Cammack, and I. Najera Existence of hepatitis C virus NS5B variants naturally resistant to non-nucleoside, but not to nucleoside, polymerase inhibitors among untreated patients J. Antimicrob. Chemother. 61 2008 1205 1216 (Pubitemid 351753583)
34. L. Tomei, R.L. Vitale, I. Incitti, S. Serafini, S. Altamura, A. Vitelli, and F.R. De Biochemical characterization of a hepatitis C virus RNA-dependent RNA polymerase mutant lacking the C-terminal hydrophobic sequence J. Gen. Virol. 81 2000 759 767 (Pubitemid 30105507)
35. V. Lohmann, A. Roos, F. Korner, J.O. Koch, and R. Bartenschlager Biochemical and structural analysis of the NS5B RNA-dependent RNA polymerase of the hepatitis C virus J. Viral Hepat. 7 2000 167 174 (Pubitemid 30337612)
36. S.S. Carroll, V. Sardana, Z. Yang, A.R. Jacobs, C. Mizenko, D. Hall, L. Hill, J. Zugay-Murphy, and L.C. Kuo 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 2000 8243 8249 (Pubitemid 30460975)
37. Y. Liu, W.W. Jiang, J. Pratt, T. Rockway, K. Harris, S. Vasavanonda, R. Tripathi, R. Pithawalla, and W.M. Kati Mechanistic study of HCV polymerase inhibitors at individual steps of the polymerization reaction Biochemistry 45 2006 11312 11323 (Pubitemid 44453979)
38. T. Yamashita, S. Kaneko, Y. Shirota, W. Qin, T. Nomura, K. Kobayashi, and S. Murakami RNA-dependent RNA polymerase activity of the soluble recombinant hepatitis C virus NS5B protein truncated at the C-terminal region J. Biol. Chem. 273 1998 15479 15486 (Pubitemid 28298156)
39. V. Lohmann, A. Roos, F. Korner, J.O. Koch, and R. Bartenschlager Biochemical and kinetic analyses of NS5B RNA-dependent RNA polymerase of the hepatitis C virus Virology 249 1998 108 118 (Pubitemid 28430912)
40. D.M. Brainard, M.S. Anderson, A. Petry, K. Van Dyck, I. De Lepeleire, K. Sneddon, C.E. Cummings, R.B. Nachbar, R.J. Barnard, P. Sun, P. Panorchan, J.B. Sanderson, E. Udezue, F. Wagner, M. Iwamoto, J. Chodakewitz, and J.A. Wagner Safety and antiviral activity of NS5B polymerase inhibitor MK-3281, in treatment-naïve genotype 1A, 1B and 3 HCV infected patients 60th Annual Meeting of the American Association for the Study of Liver Diseases, Boston, MA, USA 2009
41. B.K. Biswal, M.M. Cherney, M. Wang, L. Chan, C.G. Yannopoulos, D. Bilimoria, O. Nicolas, J. Bedard, and M.N. James 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 2005 18202 18210 (Pubitemid 41389065)
42. G. McKercher, P.L. Beaulieu, D. Lamarre, S. LaPlante, S. Lefebvre, C. Pellerin, L. Thauvette, and G. Kukolj Specific inhibitors of HCV polymerase identified using an NS5B with lower affinity for template/primer substrate Nucleic Acids Res. 32 2004 422 431 (Pubitemid 38268075)