Natural prevalence of hepatitis C virus (HCV) variants resistant to protease and polymerase inhibitors in patients infected with HCV genotype 1 in Tunisia

Journal of Medical Virology

Volumn 86, Issue 8, 2014, Pages 1350-1359

  Larousse, Jameleddine Aissa ^a,b,c   Trimoulet, Pascale ^b,c   Recordon Pinson, Patricia ^b,c   Papuchon, Jennnifer ^b,c   Azzouz, Mohamed Mssadak ^d   Ben Mami, Nabyl ^e   Cheikh, Imed ^f   Triki, Henda ^a   Fleury, Hervé ^b,c  

^a PASTEUR INSTITUTE OF TUNIS   (Tunisia)

^b University Victor Segalen   (France)

^c BORDEAUX UNIVERSITY HOSPITAL   (France)

^d Hopital Mohamed Tahar Maamouri   (Tunisia)

^e Bougatfa Hospital   (Tunisia)

^f LA RABTA HOSPITAL   (Tunisia)

Author keywords

NS5B NNIs); Polymerase inhibitors (NS5B NIs; Protease inhibitors (PIs); Resistance mutations

Indexed keywords

2' DEOXY 2' FLUORO 2' METHYLCYTIDINE; 4' AZIDOCYTIDINE; AMINO ACID; BILB 1941; BOCEPREVIR; CILUPREVIR; DANOPREVIR; NARLAPREVIR; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 5B; PROTEINASE INHIBITOR; PSI 352938; RNA DIRECTED RNA POLYMERASE INHIBITOR; SCH 446211; SIMEPREVIR; TEGOBUVIR; TELAPREVIR; TMC 453; UNCLASSIFIED DRUG;

ADULT; AGED; AMINO ACID SUBSTITUTION; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; ENZYME SUBSTRATE COMPLEX; FEMALE; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS GENOTYPE 1; HUMAN; MAJOR CLINICAL STUDY; MALE; MUTATION; PHYLOGENY; TREATMENT OUTCOME; TUNISIA; VIRAL GENETICS; VIRUS ISOLATION; VIRUS RESISTANCE; VIRUS STRAIN; ADOLESCENT; ANTIVIRAL RESISTANCE; DRUG EFFECTS; EPIDEMIOLOGY; GENETICS; HEPACIVIRUS; HEPATITIS C, CHRONIC; ISOLATION AND PURIFICATION; MIDDLE AGED; MISSENSE MUTATION; PREVALENCE; VERY ELDERLY; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; DRUG RESISTANCE, VIRAL; FEMALE; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; MALE; MIDDLE AGED; MUTATION, MISSENSE; PREVALENCE; TUNISIA; YOUNG ADULT;

EID: 84901829768     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23958     Document Type: Article

References (39)

1. Alves R, Queiroz ATL, Pessoa MG, da Silva EF, Mazo DF, Carrilho FJ, Carvahlo-Filko 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.
2. Bartels DJ, Zhou Y, Zhang EZ, Marcial M, Byrn RA, Pfeiffer T, Tigges AM, Adiwijaya BS, Lin C, Kwong AD, Kieffer TL. 2008. Natural preavalence of hepatitis C virus variants with decreased sensibility to NS3-4A protease inhibitors treatment-naïve subjects. J Infect Dis 198:800-807.
3. Bartels DJ, Sullvian 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 were rarely observed in DAA-naïve patients prior to treatment. J Virol 87:1544-1553.
4. Beaulieu PL. 2009. Recent advances in the development of NS5B polymerase inhibitors for the treatment of virus infection. Expert Opin Ther Pat 19:145-164.
5. Djebbi A, Mejri S, Thiers V, Triki H. 2004. Phylogenetic analysis of hepatitis C virus isolates from Tunisian patients. Eur J Epidemiol 19:555-562.
6. Gorgi Y, Yalaoui S, Ben Nejma HL, Azzouz MM, Hsairi M, Ben Khelifa H, Ayed K. 1998. Detection of the hepatitis C virus in the general population of Tunisia. Bull Soc Pathol Exot 91:177.
7. Halfon P, Locarnini S. 2011. Hepatitis C virus resistance to protease inhibitors. J Hepatol 55:192-206.
8. Halfon P, Sarrazin C. 2012. Future treatment of chronic hepatitis C with direct acting antivirals: Is resistance important? Liver Int 32:79-87.
9. Hezode C, Forestier N, Dusheiko G, Ferrenci P, Pol S, Goesern T, Bronowicki JP, Bourliere M, Gharakhanian S, Bengtsson L, McNair L, George S, Kieffer T, Kwong A, Kauffman RS, Alam J, Pawlotsky JM, Zeuzem S. 2009. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med 360:1839-1850.
10. Howe AY, Cheng H, Johann S, Mullen S, Chunduru SK, Young DC, Bard J, Chopra R, Krishnamurthy G, Mansour T, O'Connell J. 2008. Molecur mechanism of hepatitis C virus replicon variants with reduced susceptibility to a benzofuran inhibitor, HCV-796. Antimicrob Agents Chemother 52:3327-3338.
11. Kukolj G, McGibbon GA, McKercher G, Marquis M, Lefèbre S, Thauvette L, Gauthier J, Goulet S, Poupart MA, Beaulieu PL. 2005. Binding sites characterization and resistance to a class of non-nucleoside inhibitors of the hepatitis C virus NS5B polymerase. J Biol Chem 280:39260-39267.
12. Kuntzen T, Timm J, Berical A, Lennon N, Berlin AM, Young SK, Lee B, Heckerman D, Carlson J, Reyor LL, Kleyman M, McMahon CM, Birch C, Wiesch JS, Ledlie T, Koehrsen M, Kodira C, Roberts AD, Lauer GM, Rosen HR, Bihl F, Cerny A, Spengler U, Liu Z, Kim AY, Xing Y, Schneidewind A, Madey MA, Fleckenstein JF, Park VM, Galagan JE, Nusbaum C, Walker BD, Lake-Bakaar GV, Daar ES, Jacobson IM, Gomperts ED, Edlin BR, Donfield SM, Chung RT, Talal AH, Marion T, Birren BW, Henn MR, Allen TD. 2008. Naturally occurring dominant resistance mutations hepatitis C virus protease and polymerase inhibitors in treatment-naïve patients. Hepatology 48:1769-1778.
13. Kwo PY, Lawitz EJ, McCone J, Schiff ER, Vierling JM, Pound D, Davis MN, Galati JS, Gordon SC, Ravendhran N, Rassaro L, Anderson FH, Jacobson IM, Rubin R, Kourry K, Pedicone LD, Brass CA, Chaudhri E, Albrecht JK. 2010. Efficacy of boceprevir, an NS3 protease inhibitor in combination with peginterferon alfa-2b and ribavirin in treatment-naïve patients with genotype 1 hepatitis C infect (SPRITN-1): An open-label, randomized, multicentre phase 2 trial. Lancet 376:705-716.
14. Lam AM, Espiridu C, Bansal S, Micolochick Steuer HM, Zennou V, Otto MJ, Furman PA. 2011. Hepatitis C virus nucleotide inhibitors PSI-352938 and PSI-353661 exhibit a novel mechanism of resistance requiring multiple mutations within replicon RNA. J Virol 85:12334-12342.
15. Lange CM, Sarrazin C, Zeuzem S. 2010. Review article: Specifically target anti-viral therapy for hepatitis C-a new area in therapy. Aliment Pharmacol Ther 32:14-28.
16. Le Pogam S, Jiang WR, Leveque V, Rajyaguru S, Ma H, Jiang S, Singer M, Ali S, Klumpp K, Smith D, Symons J, Cammack N, Najera I. 2006. In vitro selected Con1 subgenomic replicons resitant to2'-C methyl-cytidine or to R1479 show lack of crioss resistance. Virology 351:349-359.
17. Le Pogam S, Seshaadri A, Kosaka A, Chiu S, Kang H, Hu S, Rajyaguru S, Symons J, Cammack N, Najera I. 2008. Existence of hepatitis C virus NS5B variants naturally resistant to non-nucleoside, but not to nucleoside, polymerase inhibitors among untreated patients. J Antimicrob Chemother 61:1205-1216.
18. Legrand-Abravanel F, Henquell C, Le Guillou-Guillemette H, Balan V, Mirand A, Dubois M, Lunel-Fabiani F, Payan C, Izopet J. 2009. Naturally occurring substitutions conferring resistance to hepatitis C virus polymerase inhibitors in treatment-naïve patients infected with genotype 1-5. Antivir Ther 14:723-730.
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 Koch H, Fanning GC, Simmen KA. 2010. In vitro resistance profile of the hepatitis virus NS3/4A protease inhibitor TMC435. Antimicrob Agents Chemother 54:1878-1887.
20. Letunic I, Bork P. 2007. Interactive Tree Of Life (iTOL): An online tool for phylogenetic tree display and annotation. Bioinformatics 23:127-128.
21. Lopez-Labrador FX, Moya A, Gonzalez-Candelas F. 2008. Mapping natural polymorphisms of hepatitis C virus NS3/4A protease and antiviral resistance to inhibitors in worldwide isolates. Antivir Ther 13:481-494.
22. Lul L, Dekhtyar T, Masse S, Pithawalla R, Krishann P, He W, Ng T, Koev G, Stewart K, Larson D, Bosse T, Wagner R, Pilot-Matias T, Mo H, Molla A. 2007. Identification and characterization of mutations conferring resistance to an HCV RNA-dependent RNA polymerase inhibitor in vitro. Antiviral Res 76:93-97.
23. Mo H, Lu L, Pilot-Matias T, Mondal R, Masse S, Dekhtyar T, Ng T, Koev G, Stoll V, Stewart KD, Pratt J, Doner P, Pockway T, Maring C, Molla A. 2005. Mutations conferring resistance to a hepatitis C virus HCV RNA dependent RNA polymerase inhibitor alone or in combination with an HCV serine protease inhibitor in vitro. Antimicrob Agents Chemother 49:4305-4314.
24. Murakami E, Bao H, Ramesh M, McBrayer TR, Whitaker T, Micolochick Steuer HM, Schinazi RF, Stuyver LJ, Obikhold A, Otton MJ, Furman PA. 2007. Mechanism of activation of β-D-2'-fluoro-2'-C-methylcytidine and inhibition of hepatitis virus NS5B RNA polymerase. Antimicrob Agents Chemother 51:503-509.
25. Pawlostsky JM. 2011. Treatment failure and resistance with direct acting antiviral drugs against hepatitis C virus. Hepatology 53:1742-1751.
26. Reesink HW, Fanning GC, Farha KA, Weegink C, Van Valiet A, Van'T Klooster G, Lenz O, Aharchi F, Marien K, Van Remoortere P, de Koch H, Broeckaert F, Meyvisch P, Van Beirendonck E, Simmen K, Verloes R. 2010. Rapid HCV RNA decline with one daily TM C435: A phase I study in healthy volunteers and hepatitis C patients. Gastroenterology 138:913-921.
27. Sarrazin C, Kieffer TL, Bartels D, Hanzelka B, Muh U, Welker M, Wincherringer D, Zhou Y, Chu HM, Lin C, Weegink C, Reesink H, Zeuzem S, Kwong AD. 2007. Dynamic hepatitis C virus genotypic and phynotypic changes in patients treated with the protease inhibitor telaprevir. Gastroenterology 132:1767-1777.
28. Shi ST, Herlihy KJ, Grahan JP, Fuhrman SA, Doan C, Parge H, Hichey M, Gao J, Yu X, Chau F, Gonzalez J, Li H, Lewis C, Patick AK, Duggal R. 2008. In vitro resistance study of AG-021541, a noval nonnucleoside inhibitor of the hepatitis C virus RNA-dependent RNA polymerase. Antimicrob Agents Chemother 52:675-683.
29. Shindo H, Maekawa S, Komase K, Suekiv R, Mirua M, Kadokura M, Shindo K, Amemiya F, Kitamura T, Nakayama Y, Inoue T, Sakamato M, Okada SI, Asahiya Y, Izumi N, Honda M, Kaneko S, Enomoto N. 2012. Characterization of naturally occurring protease inhibitor resistance mutations in genotype 1b hepatitis C virus patients. Hepatol Int 6:482-490.
30. Smith DB, Martin JA, Klumpp K, Baker SJ, Blomgren PA, Devos R, Granycome C, Hang J, Hobbs CJ, Jiang WR, Laxtron C, Le Pogam S, Leveque V, Ma H, Maile G, Merrett JH, Picota A, Sarma K, Smith M, Swallow S, Symons J, Vesey D, Najera I, Cammaack N. 2007. Design, synthesis and antiviral properties of 4'substituted ribonucleosides as inhibitors of hepatitis C virus replication: The discovery of 1479. Bioorg Med Chem Lett 17:2570-2576.
31. Susser S, Welsch C, Wang Y, Zettler M, Domingues FS, Karey U, Hughes E, Ralston R, Tong X, Herrmann E, Zeuzen S, Sarrazin C. 2009. Characterization of resistance to the protease inhibitor boceprevir in hepatitis C virus infected patients. Hepatology 50:1709-1718.
32. Tong X, Guo Z, Wright Minogue J, Xia E, Prongay A, Madison V, Qiu P, Venkatraman S, Velazguez FS, Njoroge FG, Malcolm BA. 2006. Impact of the naturally occurring variants of HCV protease on the binding of different classes of protease inhibitors. Biochemistry 45:1353-1361.
33. Triki H, Said N, Ben Salah A, Arrouji A, Ben Ahmed F, Bouguerra A, Hmida S, Dhahri R, Dellagi K. 1997. Seroepidemiology of hepatitis B, C and delta viruses in Tunisia. Trans R Soc Trop Med Hyg 91:11-14.
34. Trimoulet P, Belzynce C, Faure M, Wittkop L, Reigadas S, Dupon M, Ragnaud JM, Feury H, Neau D. 2011. Hepatitis C virus (HCV) protease variability and anti-HCV protease inhibitor resistance in HIV/HCV coinfected patients. HIV Med 12:506-509.
35. Troke PJ, Lewis M, Simpson P, Gore K, Hammond J, Craiq C, Westby M. 2012. Characterization of resistance to the nonnucleoside NS5B inhibitor Filibuvir in Hepatitis C virus infected patients. Antimicrob Agents Chemother 56:1331-1341.
36. Vallet S, Viron F, Henquell C, Le Guillou-Guillemette H, Lagathu G, Abravanenel F, Trimoulet P, Soussan P, Schvoerer E, Rosenberg A, Gouriou S, Colson P, Izopet J, Payan C. 2011. NS3 protease polymorphism and natural resistance to protease inhibitor in French patients infected with HCV genotype 1-5. Antivir Ther 16:1093-1102.
37. Vicenti I, Rosi A, Saladini F, Meini G, Pippi F, Rossetti B, Sidella L, Di Giambenedetto S, Almi P, De Luca A, Caudai C, Zazzi M. 2012. Naturally occurring hepatitis C virus HCV NS3/4A protease inhibitor resistance-related mutations in HCV genotype &-infected subject in Italy. J Antimicrob Chemother 67:984-987.
38. Zeuzem S, Buggisch P, Agarwal K, Marcellin P, Sereni D, Klinker H, Moreno C, Zarski JP, LHorsmans Y, Mo H, Arterburn S, Knox S, Oldach D, McHutchison JP, Manns MP, Foster GR. 2012. The protease inhibitor, GS-9256 and non-nucleoside polymerase inhibitor tegobuvir alone, with ribavirin, or pegylated interferon plus ribavirin in hepatitis C. Hepatology 55:749-758.
39. Zhou Y, Bartels DJ, Hanzelka BL, Muh U, Wei Y, Chu HM, Tigges AM, Brennan DL, Rao BG, Swenson L, Kwong AD, Lin C. 2008. Phenotypic characterization of resistance Val 36 variants of hepatitis C virus NS3-4A serine protease. Antimicrob Agents Chemother 52:110-120.