Identification and analysis of fitness of resistance mutations against the HCV protease inhibitor SCH 503034

Antiviral Research

Volumn 70, Issue 2, 2006, Pages 28-38

  Tong, Xiao ^a   Chase, Robert ^a   Skelton, Angela ^a   Chen, Tong ^a   Wright Minogue, Jackie ^a   Malcolm, Bruce A ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

Antiviral; Hepatitis C virus; Inhibitor; Protease; Resistance

Indexed keywords

CILUPREVIR; NONSTRUCTURAL PROTEIN 3 INHIBITOR; PROTEINASE INHIBITOR; RECOMBINANT ALPHA INTERFERON; SCH 503034; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; VIRUS RNA; VX 950;

ANTIBIOTIC RESISTANCE; ARTICLE; CONTROLLED STUDY; DRUG POTENCY; DRUG SCREENING; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IN VITRO STUDY; MUTAGENESIS; MUTATION; PRIORITY JOURNAL; PROTEIN STRUCTURE; REPLICON; STRUCTURE ANALYSIS; VIROGENESIS; VIRUS CULTURE; VIRUS GENOME; VIRUS MUTANT; VIRUS RESISTANCE; WILD TYPE;

BLOTTING, WESTERN; CELL LINE, TUMOR; DRUG RESISTANCE, VIRAL; ENZYME ACTIVATION; HEPACIVIRUS; HUMANS; KINETICS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENOTYPE; PROLINE; PROTEASE INHIBITORS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; REPLICON; SEQUENCE ANALYSIS; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS; HUMAN HERPESVIRUS 5;

EID: 33646036163     PISSN: 01663542     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.antiviral.2005.12.003     Document Type: Article

References (43)

1. Battaglia A.M., and Hagmeyer K.O. Combination therapy with interferon and ribavirin in the treatment of chronic hepatitis C infection. Ann. Pharmacother. 34 4 (2000) 487-494
2. Blight K.J., Kolykhalov A.A., and Rice C.M. Efficient initiation of HCV RNA replication in cell culture. Science 290 5498 (2000) 1972-1974
3. Blower S.M., Aschenbach A.N., Gershengorn H.B., and Kahn J.O. Predicting the unpredictable: transmission of drug-resistant HIV. Nat. Med. 7 9 (2001) 1016-1020
4. Borman A.M., Paulous S., and Clavel F. Resistance of human immunodeficiency virus type 1 to protease inhibitors: selection of resistance mutations in the presence and absence of the drug. J. Gen. Virol. 77 Pt 3 (1996) 419-426
5. Boyer N., and Marcellin P. Pegylated interferon: new progress in treatment for chronic hepatitis C. Gastroenterol. Clin. Biol. 24 8-9 (2000) 767-769
6. Brenner B.G., Routy J.P., Petrella M., Moisi D., Oliveira M., Detorio M., Spira B., Essabag V., Conway B., Lalonde R., Sekaly R.P., and Wainberg M.A. Persistence and fitness of multidrug-resistant human immunodeficiency virus type 1 acquired in primary infection. J. Virol. 76 4 (2002) 1753-1761
7. Cabot B., Martell M., Esteban J.I., Piron M., Otero T., Esteban R., Guardia J., and Gomez J. Longitudinal evaluation of the structure of replicating and circulating hepatitis C virus quasispecies in nonprogressive chronic hepatitis C patients. J. Virol. 75 24 (2001) 12005-12013
8. Carrillo A., Stewart K.D., Sham H.L., Norbeck D.W., Kohlbrenner W.E., Leonard J.M., Kempf D.J., and Molla A. In vitro selection and characterization of human immunodeficiency virus type 1 variants with increased resistance to ABT-378, a novel protease inhibitor. J. Virol. 72 9 (1998) 7532-7541
9. Condra J.H., Schleif W.A., Blahy O.M., Gabryelski L.J., Graham D.J., Quintero J.C., Rhodes A., Robbins H.L., Roth E., Shivaprakash M., et al. In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature 374 6522 (1995) 569-571
10. Croteau G., Doyon L., Thibeault D., McKercher G., Pilote L., and Lamarre D. Impaired fitness of human immunodeficiency virus type 1 variants with high-level resistance to protease inhibitors. J. Virol. 71 2 (1997) 1089-1096
11. Eastman P.S., Mittler J., Kelso R., Gee C., Boyer E., Kolberg J., Urdea M., Leonard J.M., Norbeck D.W., Mo H., and Markowitz M. Genotypic changes in human immunodeficiency virus type 1 associated with loss of suppression of plasma viral RNA levels in subjects treated with ritonavir (Norvir) monotherapy. J. Virol. 72 6 (1998) 5154-5164
12. Farci P., Strazzera R., Alter H.J., Farci S., Degioannis D., Coiana A., Peddis G., Usai F., Serra G., Chessa L., Diaz G., Balestrieri A., and Purcell R.H. Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc. Natl. Acad. Sci. U.S.A. 99 5 (2002) 3081-3086
13. Foy E., Li K., Wang C., Sumpter Jr. R., Ikeda M., Lemon S.M., and Gale Jr. M. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300 5622 (2003) 1145-1148
14. Harrigan P.R., Montaner J.S., Wegner S.A., Verbiest W., Miller V., Wood R., and Larder B.A. World-wide variation in HIV-1 phenotypic susceptibility in untreated individuals: biologically relevant values for resistance testing. Aids 15 13 (2001) 1671-1677
15. Hirsch M.S., Conway B., D'Aquila R.T., Johnson V.A., Brun-Vezinet F., Clotet B., Demeter L.M., Hammer S.M., Jacobsen D.M., Kuritzkes D.R., Loveday C., Mellors J.W., Vella S., and Richman D.D. Antiretroviral drug resistance testing in adults with HIV infection: implications for clinical management. International AIDS Society-USA Panel. JAMA 279 24 (1998) 1984-1991
16. Hoofnagle J.H. Management of hepatitis C: current and future perspectives. J. Hepatol. 31 Suppl. 1 (1999) 264-268
17. Krieger N., Lohmann V., and Bartenschlager R. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J. Virol. 75 10 (2001) 4614-4624
18. Lahser F.C., Wright-Minogue J., Skelton A., and Malcolm B.A. Quantitative estimation of viral fitness using Pyrosequencing. Biotechniques 34 (2003) 26-28
19. Lech W.J., Wang G., Yang Y.L., Chee Y., Dorman K., McCrae D., Lazzeroni L.C., Erickson J.W., Sinsheimer J.S., and Kaplan A.H. In vivo sequence diversity of the protease of human immunodeficiency virus type 1: presence of protease inhibitor-resistant variants in untreated subjects. J. Virol. 70 3 (1996) 2038-2043
20. Lin C., Gates C.A., Rao B.G., Brennan D.L., Fulghum J.R., Luong Y.P., Frantz J.D., Lin K., Ma S., Wei Y.Y., Perni R.B., and Kwong A.D. In vitro studies of cross-resistance mutations against two hepatitis C virus serine protease inhibitors, VX-950 and BILN 2061. J. Biol. Chem. 280 44 (2005) 36784-36791
21. Lin C., Lin K., Luong Y.P., Rao B.G., Wei Y.Y., Brennan D.L., Fulghum J.R., Hsiao H.M., Ma S., Maxwell J.P., Cottrell K.M., Perni R.B., Gates C.A., and Kwong A.D. In vitro resistance studies of hepatitis C virus serine protease inhibitors, VX-950 and BILN 2061: structural analysis indicates different resistance mechanisms. J. Biol. Chem. 279 17 (2004) 17508-17514
22. Lohmann V., Korner F., Koch J., Herian U., Theilmann L., and Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285 5424 (1999) 110-113
23. Lu L., Pilot-Matias T.J., Stewart K.D., Randolph J.T., Pithawalla R., He W., Huang P.P., Klein L.L., Mo H., and Molla A. Mutations conferring resistance to a potent hepatitis C virus serine protease inhibitor in vitro. Antimicrob. Agents Chemother. 48 6 (2004) 2260-2266
24. Maguire M.F., Guinea R., Griffin P., Macmanus S., Elston R.C., Wolfram J., Richards N., Hanlon M.H., Porter D.J., Wrin T., Parkin N., Tisdale M., Furfine E., Petropoulos C., Snowden B.W., and Kleim J.P. Changes in human immunodeficiency virus type 1 Gag at positions L449 and P453 are linked to I50V protease mutants in vivo and cause reduction of sensitivity to amprenavir and improved viral fitness in vitro. J. Virol. 76 15 (2002) 7398-7406
25. Malcolm, B.A., Liu, R., Lahser, F., Agrawal, S., Belanger, B., Butkiewicz, N., Chase, R., Gheyas, F., Hart, A., Hesk, D., Ingravallo, P., Jiang, C., Kong, R., Lu, J., Pichardo, J., Prongay, A., Skelton, A., Tong, X., Venkatraman, S., Xia, E., Girijavallabhan, V., Njoroge, F.G., SCH 503034, a mechanism-based inhibitor of Hepatitis C virus NS3 protease suppresses polyprotein maturation and enhances the antiviral activity of interferon a in replicon cells, Antimicrob. Agents Chemother., in press.
26. Mammano F., Petit C., and Clavel F. Resistance-associated loss of viral fitness in human immunodeficiency virus type 1: phenotypic analysis of protease and gag coevolution in protease inhibitor-treated patients. J. Virol. 72 9 (1998) 7632-7637
27. Maree A.F., Keulen W., Boucher C.A., and De Boer R.J. Estimating relative fitness in viral competition experiments. J. Virol. 74 23 (2000) 11067-11072
28. Markowitz M., Mo H., Kempf D.J., Norbeck D.W., Bhat T.N., Erickson J.W., and Ho D.D. Selection and analysis of human immunodeficiency virus type 1 variants with increased resistance to ABT-538, a novel protease inhibitor. J. Virol. 69 2 (1995) 701-706
29. Martell M., Esteban J.I., Quer J., Genesca J., Weiner A., Esteban R., Guardia J., and Gomez J. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J. Virol. 66 5 (1992) 3225-3229
30. Martinez-Picado J., Savara A.V., Shi L., Sutton L., and D'Aquila R.T. Fitness of human immunodeficiency virus type 1 protease inhibitor-selected single mutants. Virology 275 2 (2000) 318-322
31. Molla A., Korneyeva M., Gao Q., Vasavanonda S., Schipper P.J., Mo H.M., Markowitz M., Chernyavskiy T., Niu P., Lyons N., Hsu A., Granneman G.R., Ho D.D., Boucher C.A., Leonard J.M., Norbeck D.W., and Kempf D.J. Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat. Med. 2 7 (1996) 760-766
32. Morrison J.F., and Walsh C.T. The behavior and significance of slow-binding enzyme inhibitors. Adv. Enzymol. Relat. Areas Mol. Biol. 61 (1988) 201-301
33. Nakabayashi H., Taketa K., Miyano K., Yamane T., and Sato J. Growth of human hepatoma cells lines with differentiated functions in chemically defined medium. Cancer Res. 42 9 (1982) 3858-3863
34. Paolucci S., Baldanti F., Campanini G., Zavattoni M., Cattaneo E., Dossena L., and Gerna G. Analysis of HIV drug-resistant quasispecies in plasma, peripheral blood mononuclear cells and viral isolates from treatment-naive and HAART patients. J. Med. Virol. 65 2 (2001) 207-217
35. Romano L., Venturi G., Giomi S., Pippi L., Valensin P.E., and Zazzi M. Development and significance of resistance to protease inhibitors in HIV-1-infected adults under triple-drug therapy in clinical practice. J. Med. Virol. 66 2 (2002) 143-150
36. Taremi S.S., Beyer B., Maher M., Yao N., Prosise W., Weber P.C., and Malcolm B.A. Construction, expression, and characterization of a novel fully activated recombinant single-chain hepatitis C virus protease. Protein Sci. 7 10 (1998) 2143-2149
37. Tisdale M., Myers R.E., Maschera B., Parry N.R., Oliver N.M., and Blair E.D. Cross-resistance analysis of human immunodeficiency virus type 1 variants individually selected for resistance to five different protease inhibitors. Antimicrob. Agents Chemother. 39 8 (1995) 1704-1710
38. Tokita H., Okamoto H., Iizuka H., Kishimoto J., Tsuda F., Miyakawa Y., and Mayumi M. 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 Pt 8 (1998) 1847-1857
39. Trozzi C., Bartholomew L., Ceccacci A., Biasiol G., Pacini L., Altamura S., Narjes F., Muraglia E., Paonessa G., Koch U., De Francesco R., Steinkuhler C., and Migliaccio G. In vitro selection and characterization of hepatitis C virus serine protease variants resistant to an active-site peptide inhibitor. J. Virol. 77 6 (2003) 3669-3679
40. Yang S.H., Lee C.G., Song M.K., and Sung Y.C. Internal cleavage of hepatitis C virus NS3 protein is dependent on the activity of NS34A protease. Virology 268 1 (2000) 132-140
41. Yi M., Tong X., Skelton A., Chase R., Chen T., Prongay A., Bogen S.L., Saksena A.K., Njoroge F.G., Veselenak R.L., Pyles R.B., Bourne N., Malcolm B.A., and Lemon S.M. Mutations conferring resistance to SCH6, a novel hepatitis C virus NS3/4A protease inhibitor: reduced RNA replication fitness and partial rescue by second-site mutations. J. Biol. Chem. (2005)
42. Zhang R., Beyer B.M., Durkin J., Ingram R., Njoroge F.G., Windsor W.T., and Malcolm B.A. A continuous spectrophotometric assay for the hepatitis C virus serine protease. Anal. Biochem. 270 2 (1999) 268-275
43. Zhang Y.M., Imamichi H., Imamichi T., Lane H.C., Falloon J., Vasudevachari M.B., and Salzman N.P. Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its Gag substrate cleavage sites. J. Virol. 71 9 (1997) 6662-6670