Comparison of daclatasvir resistance barriers on NS5A from hepatitis C virus genotypes 1 to 6: Implications for cross-genotype activity

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 9, 2014, Pages 5155-5163

  Wang, Chunfu ^a   Jia, Lingling ^a   O'Boyle II, Donald R ^a   Sun, Jin Hua ^a   Rigat, Karen ^a   Valera, Lourdes ^a   Nower, Peter ^a   Huang, Xin ^a   Kienzle, Bernadette ^a   Roberts, Susan ^a   Gao, Min ^a   Fridell, Robert A ^a  

^a BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DACLATASVIR; MK 5172; PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; BMS-790052; IMIDAZOLE DERIVATIVE; NS-5 PROTEIN, HEPATITIS C VIRUS; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; HEPATITIS C; HEPATITIS C VIRUS GENOTYPE 1; HEPATITIS C VIRUS GENOTYPE 2; HEPATITIS C VIRUS GENOTYPE 3; HEPATITIS C VIRUS GENOTYPE 4; HEPATITIS C VIRUS GENOTYPE 5; HEPATITIS C VIRUS GENOTYPE 6; HUMAN; IN VITRO STUDY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPLICON; DRUG EFFECTS; GENETICS; GENOTYPE; HEPACIVIRUS;

AMINO ACID SUBSTITUTION; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; GENOTYPE; HEPACIVIRUS; IMIDAZOLES; PROTEASE INHIBITORS; REPLICON; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84906087908     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02788-14     Document Type: Article

References (31)

1. Gao M, Nettles RE, Belema M, Snyder LB, Nguyen VN, Fridell RA, Serrano-Wu MH, Langley DR, Sun J-H, O'Boyle DR, II, Lemm JA, Wang C, Knipe JO, Chien C, Colonno RJ, Grasela DM, Meanwell NA, Hamann LG. 2010. Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 465:96-100. http://dx.doi.org/10.1038/nature08960.
2. Fridell RA, Qiu D, Wang C, Valera L, Gao M. 2010. Resistance analysis of the hepatitisCvirus 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.
3. Fridell RA, Wang C, Sun J-H, O'Boyle DR, 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 hepatitis C virus 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.
4. Nettles RE, Gao M, Bifano M, Chung E, Persson A, Marbury TC, Goldwater R, DeMicco MP, Rodriguez-Torres M, Vutikullird A, Fuentes E, Lawitz E, Lopez-Talavera JC, Grasela DM. 2011. Multiple ascending dose study of BMS-790052, a nonstructural protein 5A replication complex inhibitor, in patients infected with hepatitis C virus genotype 1. Hepatology 54:1956-1965. http://dx.doi.org/10.1002/hep.24609.
5. Pol S, Ghalib RH, Rustgi VK, Martorell C, Everson GT, Tatum HA, Hézode C, Lim JK, Bronowicki J-P, Abrams GA, Bräu N, Morris DW, Thuluvath PJ, Reindollar RW, Yin PD, Diva U, Hindes R, McPhee F, Hernandez D, Wind-Rotolo M, Hughes EA, Schnittman S. 2012. Daclatasvir for previously untreated chronic hepatitis C genotype-1 infection: a randomised, parallel-group, double-blind, placebo-controlled, dose-finding, phase 2a trial. Lancet Infect. Dis. 12:671-677. http://dx.doi.org/10.1016/S1473-3099(12)70138-X.
6. Chayama K, Takahashi S, Toyota J, Karino Y, Ikeda K, Ishikawa H, Watanabe H, McPhee F, Hughes E, Kumada H. 2012. Dual therapy with the nonstructural protein 5A inhibitor, daclatasvir, and the nonstructural protein 3 protease inhibitor, asunaprevir, in hepatitis C virus genotype 1b-infected null responders. Hepatology 55:742-748. http://dx.doi.org/10.1002/hep.24724.
7. Lok AS, Gardiner DF, Lawitz E, Martorell C, Everson GT, Ghalib R, Reindollar R, Rustgi V, McPhee F, Wind-Rotolo M, Persson A, Zhu K, Dimitrova DI, Eley T, Guo T, Grasela DM, Pasquinelli C. 2012. Preliminary study of two antiviral agents for hepatitis C genotype 1. N. Engl. J. Med. 366:216-224. http://dx.doi.org/10.1056/NEJMoa1104430.
8. McPhee F, Hernandez D, Yu F, Ueland J, Monikowski A, Carifa A, Falk P, Wang C, Fridell R, Eley T, Zhou N, Gardiner D. 2013. Resistance analysis of hepatitis C virus genotype 1 prior treatment null responders receiving daclatasvir and asunaprevir. Hepatology 58:902-911. http://dx.doi.org/10.1002/ hep.26388.
9. Cuevas JM, Gonzalez-Candelas F, Moya A, Sanjuan R. 2009. Effect of ribavirin on the mutation rate and spectrum of hepatitis C virus in vivo. J. Virol. 83:5760-5764. http://dx.doi.org/10.1128/JVI.00201-09.
10. Guedj J, Rong L, Dahari H, Perelson AS. 2010. A perspective on modelling hepatitis C virus infection. J. Viral Hepat. 17:825-833. http://dx.doi.org/10. 1111/j.1365-2893.2010.01348.x.
11. Simmonds P. 2004. Genetic diversity and evolution of hepatitis C virus - 15 years on. J. Gen. Virol. 85:3173-3188. http://dx.doi.org/10.1099/vir.0.80401- 0.
12. Sulkowski MS, Gardiner DF, Rodriguez-Torres M, Reddy KR, Hassanein T, Jacobson I, Lawitz E, Lok AS, Hinestrosa F, Thuluvath PJ, Schwartz H, Nelson DR, Everson GT, Eley T, Wind-Rotolo M, Huang S-P, Gao M, Hernandez D, McPhee F, Sherman D, Hindes R, Symonds W, Pasquinelli C, Grasela DM. 2014. Daclatasvir plus sofosbuvir for previously treated or untreated chronic HCV infection. N. Engl. J. Med. 370:211-221. http://dx.doi.org/10.1056/NEJMoa1306218.
13. Wang C, Huang H, Valera L, Sun J-H, O'Boyle DR, Nower PT, Jia L, Qiu D, Huang X, Altaf A, Gao M, Fridell RA. 2012. Hepatitis C virus RNA elimination and development of resistance in replicon cells treated with BMS-790052. Antimicrob. Agents Chemother. 56:1350-1358. http://dx.doi.org/10.1128/AAC.05977- 11.
14. Fridell RA, Qiu D, Valera L, Wang C, Rose RE, Gao M. 2011. Distinct functions of NS5A in hepatitis C virus RNA replication uncovered by studies with the NS5A inhibitor BMS-790052. J. Virol. 85:7312-7320. http://dx.doi.org/10. 1128/JVI.00253-11.
15. Wang C, Valera L, Jia L, Kirk MJ, Gao M, Fridell RA. 2013. In vitro activity of daclatasvir on hepatitisCvirus genotype 3 NS5A. Antimicrob. Agents Chemother. 57:611-613. http://dx.doi.org/10.1128/AAC.01874-12.
16. Wang C, Jia L, Huang H, Qiu D, Valera L, Huang X, Sun J-H, Nower PT, O'Boyle DR, Gao M, Fridell RA. 2012. In vitro activity of BMS-790052 on hepatitis C virus genotype 4 NS5A. Antimicrob. Agents Chemother. 56:1588-1590. http://dx.doi.org/10.1128/AAC.06169-11.
17. Smuts HE, Kannemeyer J. 1995. Genotyping of hepatitis C virus in South Africa. J. Clin. Microbiol. 33:1679-1681.
18. Naamani KA, Sinani SA, Deschênes M. 2013. Epidemiology and treatment of hepatitis C genotypes 5 and 6. Can. J. Gastroenterol. Hepatol. 27:e8-e12.
19. Summa V, Ludmerer SW, McCauley JA, Fandozzi C, Burlein C, Claudio G, Coleman PJ, DiMuzio JM, Ferrara M, Di Filippo M, Gates AT, Graham DJ, Harper S, Hazuda DJ, McHale C, Monteagudo E, Pucci V, Rowley M, Rudd MT, Soriano A, Stahlhut MW, Vacca JP, Olsen DB, Liverton NJ, Carroll SS. 2012. MK-5172, a selective inhibitor of hepatitis C virus NS3/4a protease with broad activity across genotypes and resistant variants. Antimicrob. Agents Chemother. 56:4161-4167. http://dx.doi.org/10.1128/AAC.00324-12.
20. Yanagi M, Purcell RH, Emerson SU, Bukh J. 1999. Hepatitis C virus: an infectious molecular clone of a second major genotype (2a) and lack of viability of intertypic 1a and 2a chimeras. Virology 262:250-263. http://dx.doi.org/10. 1006/viro.1999.9889.
21. Lemm JA, O'Boyle D, II, Liu M, Nower PT, Colonno R, Deshpande MS, Snyder LB, Martin SW, St Laurent DR, Serrano-Wu MH, Romine JL, Meanwell NA, Gao M. 2010. Identification of hepatitis C virus NS5A inhibitors. J. Virol. 84:482-491. http://dx.doi.org/10.1128/JVI.01360-09.
22. O'Boyle DR, II, Nower PT, Sun J-H, Fridell R, Wang C, Valera L, Gao M. 2013. A 96-well based analysis of replicon elimination with the HCV NS5A replication complex inhibitor daclatasvir. J. Virol. Methods 193:68-76. http://dx.doi.org/10.1016/j.jviromet.2013.04.024.
23. Combet C, Garnier N, Charavay C, Grando D, Crisan D, Lopez J, Dehne-Garcia A, Geourjon C, Bettler E, Hulo C, Mercier PL, Bartenschlager R, Diepolder H, Moradpour D, Pawlotsky J-M, Rice CM, Trepo C, Penin F, Deleage G. 2007. euHCVdb: the European Hepatitis C Virus database. Nucleic Acids Res. 35:D363-D366. http://dx.doi.org/10.1093/nar/gkl970.
24. Wang C, Sun J-H, O'Boyle DR, Nower P, Valera L, Roberts S, Fridell RA, Gao M. 2013. Persistence of resistant variants in hepatitis C virus-infected patients treated with the NS5A replication complex inhibitor daclatasvir. Antimicrob. Agents Chemother. 57:2054-2065. http://dx.doi.org/10.1128/AAC.02494- 12.
25. Sun J-H, O'Boyle DR, II, Zhang Y, Wang C, Nower P, Valera L, Roberts S, Nettles RE, Fridell RA, Gao M. 2012. Impact of a baseline polymorphism on the emergence of resistance to the hepatitis C virus nonstructural protein 5a replication complex inhibitor, BMS-790052. Hepatology 55:1692-1699. http://dx.doi.org/10.1002/hep.25581.
26. Scheel TKH, Gottwein JM, Mikkelsen LS, Jensen TB, Bukh J. 2011. RecombinantHCVvariants with NS5A from genotypes 1-7 have different sensitivities to an NS5A inhibitor but not interferon-α. Gastroenterology 140:1032-1042.e1036. http://dx.doi.org/10.1053/j.gastro.2010.11.036.
27. Gottwein JM, Jensen SB, Li Y-P, Ghanem L, Scheel TKH, Serre SBN, Mikkelsen L, Bukh J. 2013. Combination treatment with hepatitis C virus protease and NS5A inhibitors is effective against recombinant genotype 1a, 2a, and 3a viruses. Antimicrob. Agents Chemother. 57:1291-1303. http://dx.doi.org/10.1128/ AAC.02164-12.
28. O'Boyle DR, II, Sun J-H, Nower PT, Lemm JA, Fridell RA, Wang C, Romine JL, Belema M, Nguyen VN, Laurent DRS, Serrano-Wu M, Snyder LB, Meanwell NA, Langley DR, Gao M. 2013. Characterizations of HCV NS5A replication complex inhibitors. Virology 444:343-354. http://dx.doi.org/10.1016/j.virol.2013.06.032.
29. Targett-Adams P, Graham EJS, Middleton J, Palmer A, Shaw SM, Lavender H, Brain P, Tran TD, Jones LH, Wakenhut F, Stammen B, Pryde D, Pickford C, Westby M. 2011. Small molecules targeting hepatitis C virus-encoded NS5A cause subcellular redistribution of their target: insights into compound modes of action. J. Virol. 85:6353-6368. http://dx.doi.org/10.1128/JVI.00215-11.
30. Ascher DB, Wielens J, Nero TL, Doughty L, Morton CJ, Parker MW. 2014. Potent hepatitis C inhibitors bind directly to NS5A and reduce its affinity for RNA. Sci. Rep. 4:4765. http://dx.doi.org/10.1038/srep04765.
31. Li Y-P, Ramirez S, Humes D, Jensen SB, Gottwein JM, Bukh J. 2014. Differential sensitivity of 5′UTR-NS5A recombinants of hepatitis C virus genotypes 1-6 to protease and NS5A inhibitors. Gastroenterology 146:812-821.e4. http://dx.doi.org/10.1053/j.gastro.2013.11.009.