In vitro activity of simeprevir against hepatitis C virus genotype 1 clinical isolates and its correlation with NS3 sequence and site-directed mutants

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 12, 2015, Pages 7548-7557

  Verbinnen, Thierry ^a   Fevery, Bart ^a   Vijgen, Leen ^a   Jacobs, Tom ^a   De Meyer, Sandra ^a   Lenz, Oliver ^a  

^a JANSSEN RESEARCH FOUNDATION   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 3; PEGINTERFERON; RIBAVIRIN; SIMEPREVIR; ANTIVIRUS AGENT; CHIMERIC PROTEIN; NS3 PROTEIN, HEPATITIS C VIRUS; PROTEINASE INHIBITOR; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CASE REPORT; DRUG TREATMENT FAILURE; EC50; HEPATITIS C; HEPATITIS C VIRUS GENOTYPE 1; HUMAN; IN VITRO SELECTION; IN VITRO STUDY; MONOTHERAPY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REPLICON; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; VIRUS ISOLATION; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL SENSITIVITY TEST; TREATMENT FAILURE; VIROLOGY;

AMINO ACID SUBSTITUTION; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; GENE EXPRESSION; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; MICROBIAL SENSITIVITY TESTS; MUTAGENESIS, SITE-DIRECTED; MUTANT CHIMERIC PROTEINS; POLYMORPHISM, GENETIC; PROTEASE INHIBITORS; REPLICON; SIMEPREVIR; TREATMENT FAILURE; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84954493585     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01444-15     Document Type: Article

References (35)

1. Pawlotsky JM. 2014. New hepatitis C virus (HCV) drugs and the hope for a cure: concepts in anti-HCV drug development. Semin Liver Dis 34:22-29. http://dx.doi.org/10.1055/s-0034-1371007.
2. Manns M, Marcellin P, Poordad F, de Araujo ES, Buti M, Horsmans Y, Janczewska E, Villamil F, Scott J, Peeters M, Lenz O, Ouwerkerk-Mahadevan S, De La Rosa G, Kalmeijer R, Sinha R, Beumont-Mauviel M. 2014. Simeprevir with pegylated interferon alfa 2a or 2b plus ribavirin in treatment-naive patients with chronic hepatitis C virus genotype 1 infection (QUEST-2): a randomised, double-blind, placebo-controlled phase 3 trial. Lancet 384:414-426. http://dx.doi.org/10.1016/S0140-6736 (14)60538-9.
3. Jacobson IM, Dore GJ, Foster GR, Fried MW, Radu M, Rafalsky VV, Moroz L, Craxi A, Peeters M, Lenz O, Ouwerkerk-Mahadevan S, De La Rosa G, Kalmeijer R, Scott J, Sinha R, Beumont-Mauviel M. 2014. Simeprevir with pegylated interferon alfa 2a plus ribavirin in treatment-naive patients with chronic hepatitis C virus genotype 1 infection (QUEST-1): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet 384:403-413. http://dx.doi.org/10.1016/S0140-6736(14)60494-3.
4. Forns X, Lawitz E, Zeuzem S, Gane E, Bronowicki JP, Andreone P, Horban A, Brown A, Peeters M, Lenz O, Ouwerkerk-Mahadevan S, Scott J, De La Rosa G, Kalmeijer R, Sinha R, Beumont-Mauviel M. 2014. Simeprevir with peginterferon and ribavirin leads to high rates of SVR in patients withHCVgenotype 1 who relapsed after previous therapy: a phase 3 trial. Gastroenterology 146:1669-1679.e3. http://dx.doi.org/10.1053/j.gastro.2014.02.051.
5. Lawitz E, Sulkowski MS, Ghalib R, Rodriguez-Torres M, Younossi ZM, Corregidor A, DeJesus E, Pearlman B, Rabinovitz M, Gitlin N, Lim JK, Pockros PJ, Scott JD, Fevery B, Lambrecht T, Ouwerkerk-Mahadevan S, Callewaert K, Symonds WT, Picchio G, Lindsay KL, Beumont M, Jacobson IM. 2014. Simeprevir plus sofosbuvir, with or without ribavirin, to treat chronic infection with hepatitis C virus genotype 1 in nonresponders to pegylated interferon and ribavirin and treatment-naive patients: the COSMOS randomised study. Lancet 384:1756-1765. http://dx.doi.org/10.1016/S0140-6736(14)61036-9. (Erratum, Lancet 384:1748.).
6. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, Layden TJ, Perelson AS. 1998. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282:103-107. http://dx.doi.org/10.1126/science.282.5386.103.
7. Bartels DJ, Sullivan JC, Zhang EZ, Tigges AM, Dorrian JL, De Meyer S, Takemoto D, Dondero E, Kwong AD, Picchio G, Kieffer TL. 2013. Hepatitis C virus variants with decreased sensitivity to direct-acting antivirals (DAAs) were rarely observed in DAA-naive patients prior to treatment. J Virol 87:1544-1553. http://dx.doi.org/10.1128/JVI.02294-12.
8. Alves R, Queiroz AT, Pessoa MG, da Silva EF, Mazo DF, Carrilho FJ, Carvalho-Filho RJ, de Carvalho IM. 2013. The presence of resistance mutations to protease and polymerase inhibitors in hepatitis C virus sequences from the Los Alamos databank. J Viral Hepat 20:414-421. http: //dx.doi.org/10.1111/jvh.12051.
9. Lenz O, Verbinnen T, Fevery B, Tambuyzer L, Vijgen L, Peeters M, Buelens A, Ceulemans H, Beumont M, Picchio G, De Meyer S. 2015. Virology analyses of HCV isolates from genotype 1-infected patients treated with simeprevir plus peginterferon/ribavirin in phase IIb/III studies. J Hepatol 62:1008-1014. http://dx.doi.org/10.1016/j.jhep.2014.11.032.
10. Pozo F, Lina B, Andrade HR, Enouf V, Kossyvakis A, Broberg E, Daniels R, Lackenby A, Meijer A, Community Network of Reference Laboratories for Human Influenza in Europe. 2013. Guidance for clinical and public health laboratories testing for influenza virus antiviral drug susceptibility in Europe. J Clin Virol 57:5-12. http://dx.doi.org/10.1016/j.jcv.2013.01.009.
11. Durantel D, Brunelle M-N, Gros E, Carrouée-Durantel S, Pichoud C, Villet S, Trepo C, Zoulim F. 2005. Resistance of human hepatitis B virus to reverse transcriptase inhibitors: from genotypic to phenotypic testing. J Clin Virol 34(Suppl 1):S34-S43. http://dx.doi.org/10.1016/S1386-6532 (05)80008-3.
12. Vandamme AM, Camacho RJ, Ceccherini-Silberstein F, de Luca A, Palmisano L, Paraskevis D, Paredes R, Poljak M, Schmit JC, Soriano V, Walter H, Sönnerborg A, European HIV Drug Resistance Guidelines Panel. 2011. European recommendations for the clinical use of HIV drug resistance testing: 2011 update. AIDS Rev 13:77-108. http://www.aidsreviews.com/files/2011-13-2-077-108.pdf.
13. Reesink HW, Fanning GC, Farha KA, Weegink C, Van Vliet A, Van 't Klooster G, Lenz O, Aharchi F, Mariën K, Van Remoortere P, de Kock H, Broeckaert F, Meyvisch P, Van Beirendonck E, Simmen K, Verloes R. 2010. Rapid HCV-RNA decline with once daily TMC435: a phase I study in healthy volunteers and hepatitis C patients. Gastroenterology 138:913-921. http://dx.doi.org/10.1053/j.gastro.2009.10.033.
14. Manns M, Reesink H, Berg T, Dusheiko G, Flisiak R, Marcellin P, Moreno C, Lenz O, Meyvisch P, Peeters M, Sekar V, Simmen K, Verloes R. 2011. Rapid viral response of once-daily TMC435 plus pegylated interferon/ ribavirin in hepatitis C genotype-1 patients: a randomized trial. Antivir Ther 16:1021-1033. http://dx.doi.org/10.3851/IMP1894.
15. Fried MW, Buti M, Dore GJ, Flisiak R, Ferenci P, Jacobson I, Marcellin P, Manns M, Nikitin I, Poordad F, Sherman M, Zeuzem S, Scott J, Gilles L, Lenz O, Peeters M, Sekar V, De Smedt G, Beumont-Mauviel M. 2013. Once-daily simeprevir (TMC435) with pegylated interferon and ribavirin in treatment-naive genotype 1 hepatitis C: the randomized PILLAR study. Hepatology 58:1918-1929. http://dx.doi.org/10.1002/hep.26641.
16. Zeuzem S, Berg T, Gane E, Ferenci P, Foster GR, Fried MW, Hezode C, Hirschfield GM, Jacobson I, Nikitin I, Pockros PJ, Poordad F, Scott J, Lenz O, Peeters M, Sekar V, De Smedt G, Sinha R, Beumont-Mauviel M. 2014. Simeprevir increases rate of sustained virologic response among treatment-experienced patients with HCV genotype-1 infection: a phase IIb trial. Gastroenterology 146:430-441.e6. http://dx.doi.org/10.1053/j.gastro.2013.10.058.
17. Koletzki D, Pattery T, Fevery B, Vanhooren L, Stuyver LJ. 2013. Amplification and sequencing of the hepatitis C virus NS3/4A protease and the NS5B polymerase regions for genotypic resistance detection of clinical isolates of subtypes 1a and 1b. Methods Mol Biol 1030:137-149. http://dx.doi.org/10.1007/978-1-62703-484-5-12.
18. Vijgen L, Verbeeck J, Van Kerckhove B, Berke JM, Koletzki D, Fanning G, Lenz O. 2013. A cellular replicon-based phenotyping assay to determine susceptibility of hepatitis C virus clinical isolates to NS3/4A protease inhibitors. Methods Mol Biol 1030:105-117. http://dx.doi.org/10.1007 /978-1-62703-484-5-9.
19. Lenz O, Verbinnen T, Lin TI, Vijgen L, Cummings MD, Lindberg J, Berke JM, Dehertogh P, Fransen E, Scholliers A, Vermeiren K, Ivens T, Raboisson P, Edlund M, Storm S, Vrang L, de Kock H, Fanning GC, Simmen KA. 2010. In vitro resistance profile of the hepatitis C virus NS3/4A protease inhibitor TMC435. Antimicrob Agents Chemother 54: 1878-1887. http://dx.doi.org/10.1128/AAC.01452-09.
20. Qi X, Bae A, Liu S, Yang H, Sun SC, Harris J, Delaney W, Miller M, Mo H. 2009. Development of a replicon-based phenotypic assay for assessing the drug susceptibilities of HCV NS3 protease genes from clinical isolates. Antiviral Res 81:166-173. http://dx.doi.org/10.1016/j.antiviral.2008.11.002.
21. Sheaffer AK, Lee MS, Hernandez D, Chaniewski S, Yu F, Falk P, Friborg J, Zhai G, McPhee F. 2011. Development of a chimeric replicon system for phenotypic analysis of NS3 protease sequences from HCV clinical isolates. Antivir Ther 16:705-718. http://dx.doi.org/10.3851/IMP1825.
22. Verbinnen T, Jacobs T, Vijgen L, Ceulemans H, Neyts J, Fanning G, Lenz O. 2012. Replication capacity of minority variants in viral populations can affect the assessment of resistance in HCV chimeric replicon phenotyping assays. J Antimicrob Chemother 67:2327-2337. http://dx.doi.org/10.1093/jac/dks234.
23. Vangeneugden T, Laenen A, Geys H, Renard D, Molenberghs G. 2005. Applying concepts of generalizability theory on clinical trial data to investigate sources of variation and their impact on reliability. Biometrics 61: 295-304. http://dx.doi.org/10.1111/j.0006-341X.2005.031040.x.
24. Harrigan PR, Montaner JS, Wegner SA, Verbiest W, Miller V, Wood R, Larder BA. 2001. World-wide variation in HIV-1 phenotypic susceptibility in untreated individuals: biologically relevant values for resistance testing. AIDS 15:1671-1677. http://dx.doi.org/10.1097/00002030-200109070-00010.
25. Fridell RA, Qiu D, Wang C, Valera L, Gao M. 2010. Resistance analysis of the hepatitis C virus NS5A inhibitor BMS-790052 in an in vitro replicon system. Antimicrob Agents Chemother 54:3641-3650. http://dx.doi.org /10.1128/AAC.00556-10.
26. Fridell RA, Wang C, Sun JH, O'Boyle DR 2nd, Nower P, Valera L, Qiu D, Roberts S, Huang X, Kienzle B, Bifano M, Nettles RE, Gao M. 2011. Genotypic and phenotypic analysis of variants resistant to hepatitisCvirus nonstructural protein 5A replication complex inhibitor BMS-790052 in humans: in vitro and in vivo correlations. Hepatology 54:1924-1935. http: //dx.doi.org/10.1002/hep.24594.
27. Sarrazin C, Kieffer TL, Bartels D, Hanzelka B, Müh U, Welker M, Wincheringer D, Zhou Y, Chu HM, Lin C, Weegink C, Reesink H, Zeuzem S, Kwong AD. 2007. Dynamic hepatitis C virus genotypic and phenotypic changes in patients treated with the protease inhibitor telaprevir. Gastroenterology 132:1767-1777. http://dx.doi.org/10.1053/j.gastro.2007.02.037.
28. Susser S, Welsch C, Wang Y, Zettler M, Domingues FS, Karey U, Hughes E, Ralston R, Tong X, Herrmann E, Zeuzem S, Sarrazin C. 2009. Characterization of resistance to the protease inhibitor boceprevir in hepatitis C virus-infected patients. Hepatology 50:1709-1718. http://dx.doi.org/10.1002/hep.23192.
29. Kieffer TL, De Meyer S, Bartels DJ, Sullivan JC, Zhang EZ, Tigges A, Dierynck I, Spanks J, Dorrian J, Jiang M, Adiwijaya B, Ghys A, Beumont M, Kauffman RS, Adda N, Jacobson IM, Sherman KE, Zeuzem S, Kwong AD, Picchio G. 2012. Hepatitis C viral evolution in genotype 1 treatment-naive and treatment-experienced patients receiving telaprevirbased therapy in clinical trials. PLoS One 7:e34372. http://dx.doi.org/10.1371/journal.pone.0034372.
30. Tong X, Chase R, Skelton A, Chen T, Wright-Minogue J, Malcolm BA. 2006. Identification and analysis of fitness of resistance mutations against the HCV protease inhibitor SCH 503034. Antiviral Res 70:28-38. http: //dx.doi.org/10.1016/j.antiviral.2005.12.003.
31. Janssen Therapeutics. 2013. Olysio (simeprevir): prescribing information. Janssen Therapeutics, Titusville, NJ. https://www.olysio.com/shared/product /olysio/prescribing-information.pdf.
32. Janssen Cilag International NV. 2011. Incivo (telaprevir): summary of product characteristics. Janssen Cilag International NV, Beerse, Belgium. http:// www.ema.europa.eu/docs/en-GB/document-library/EPAR-Product-Information/human/002313/WC500115529.pdf.
33. Palanisamy N, Danielsson A, Kokkula C, Yin H, Bondeson K, Wesslén L, Duberg AS, Lennerstrand J. 2013. Implications of baseline polymorphisms for potential resistance to NS3 protease inhibitors in hepatitis C virus genotypes 1a, 2b and 3a. Antiviral Res 99:12-17. http://dx.doi.org/10.1016/j.antiviral.2013.04.018.
34. Janssen Cilag International NV. 2015. Olysio (simeprevir): summary of product characteristics. Janssen Cilag International NV, Beerse, Belgium. https://www.medicines.org.uk/emc/medicine/28888/SPC/OLYSIO-150mg-hard-capsules/.
35. Ogert RA, Howe JA, Vierling JM, Kwo PY, Lawitz EJ, McCone J, Schiff ER, Pound D, Davis MN, Gordon SC, Ravendhran N, Rossaro L, Jacobson IM, Ralston R, Chaudhri E, Qiu P, Pedicone LD, Brass CA, Albrecht JK, Barnard RJ, Hazuda DJ, Howe AY. 2013. Resistanceassociated amino acid variants associated with boceprevir plus pegylated interferon-alpha2b and ribavirin in patients with chronic hepatitis C in the SPRINT-1 trial. Antivir Ther 18:387-397. http://dx.doi.org/10.3851 /IMP2549.