Evolution of simeprevir-resistant variants over time by ultra-deep sequencing in HCV genotype 1b

Journal of Medical Virology

Volumn 86, Issue 8, 2014, Pages 1314-1322

  Akuta, Norio ^a   Suzuki, Fumitaka ^a   Sezaki, Hitomi ^a   Suzuki, Yoshiyuki ^a   Hosaka, Tetsuya ^a   Kobayashi, Masahiro ^a   Kobayashi, Mariko ^a   Saitoh, Satoshi ^a   Ikeda, Kenji ^a   Kumada, Hiromitsu ^a  

^a TORANOMON HOSPITAL   (Japan)

Author keywords

HCV; Resistant variants; Simeprevir; Ultra deep sequence

Indexed keywords

ARGININE; GLUTAMINE; HISTIDINE; INTERLEUKIN 28B; LEUCINE; METHIONINE; PEGINTERFERON; PEGINTERFERON ALPHA2A; PEGINTERFERON ALPHA2A PLUS RIBAVIRIN; RIBAVIRIN; SIMEPREVIR; VIRUS RNA; ALPHA INTERFERON; ANTIVIRUS AGENT; FUSED HETEROCYCLIC RINGS; SULFONAMIDE;

ADULT; AGED; AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ANTIVIRAL THERAPY; ARTICLE; CLINICAL ARTICLE; CONSENSUS SEQUENCE; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS SUBTYPE 1B; HUMAN; MALE; MIDDLE AGED; NONHUMAN; NUCLEOTIDE SEQUENCE; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); TIME; ULTRA DEEP SEQUENCING; VIRUS DETECTION; VIRUS LOAD; CLINICAL TRIAL; DRUG EFFECTS; GENETICS; HEPACIVIRUS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; JAPAN; PHASE 2 CLINICAL TRIAL; TREATMENT FAILURE; VIROLOGY; YOUNG ADULT;

ADULT; AGED; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; FEMALE; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HETEROCYCLIC COMPOUNDS, 3-RING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INTERFERON-ALPHA; JAPAN; MALE; MIDDLE AGED; RIBAVIRIN; RNA, VIRAL; SULFONAMIDES; TREATMENT FAILURE; VIRAL LOAD; YOUNG ADULT;

EID: 84901789510     PISSN: 01466615     EISSN: 10969071     Source Type: Journal    
DOI: 10.1002/jmv.23966     Document Type: Article

References (36)

1. Akuta N, Suzuki F, Sezaki H, Suzuki Y, Hosaka T, Someya T, Kobayashi M, Saitoh S, Watahiki S, Sato J, Matsuda M, Kobayashi M, Arase Y, Ikeda K, Kumada H. 2005. Association of amino acid substitution pattern in core protein of hepatitis C virus genotype1b high viral load and non-virological response to interferon-ribavirin combination therapy. Intervirology 48:372-380.
2. Akuta N, Suzuki F, Kawamura Y, Yatsuji H, Sezaki H, Suzuki Y, Hosaka T, Kobayashi M, Kobayashi M, Arase Y, Ikeda K, Kumada H. 2007. Predictive factors of early and sustained responses to peginterferon plus ribavirin combination therapy in Japanese patients infected with hepatitis C virus genotype 1b: Amino acid substitutions in the core region and low-density lipoprotein cholesterol levels. J Hepatol 46:403-410.
3. Akuta N, Suzuki F, Hirakawa M, Kawamura Y, Yatsuji H, Sezaki H, Suzuki Y, Hosaka T, Kobayashi M, Kobayashi M, Saitoh S, Arase Y, Ikeda K, Chayama K, Nakamura Y, Kumada H. 2010. Amino acid substitution in hepatitis C virus core region and genetic variation near the interleukin 28B gene predict viral response to telaprevir with peginterferon and ribavirin. Hepatology 52:421-429.
4. Akuta N, Suzuki F, Seko Y, Kawamura Y, Sezaki H, Suzuki Y, Hosaka T, Kobayashi M, Hara T, Kobayashi M, Saitoh S, Arase Y, Ikeda K, Kumada H. 2013. Emergence of telaprevir-resistant variants detected by ultra-deep sequencing after triple therapy in patients infected with HCV genotype 1. J Med Virol 85:1028-1036.
5. Akuta N, Suzuki F, Fukushima T, Kawamura Y, Sezaki H, Suzuki Y, Hosaka T, Kobayashi M, Hara T, Kobayashi M, Saitoh S, Arase Y, Ikeda K, Kumada H. 2014. Utility of detection of telaprevir-resistant variants for prediction of efficacy of treatment of hepatitis C virus genotype 1 infection. J Clin Microbiol 52:193-200.
6. Bartenschlager R, Lohmann V. 2000. Replication of hepatitis C virus. J Gen Virol 81:1631-1648.
7. 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.
8. Drafting Committee for Hepatitis Management Guidelines, the Japan Society of Hepatology. 2014. JSH Guidelines for the Management of Hepatitis C Virus Infection: A 2014 Update for Genotype 1. Hepatol Res 44:59-70.
9. Elliott AM, Radecki J, Moghis B, Li X, Kammesheidt A. 2012. Rapid detection of the ACMG/ACOG-recommended 23 CFTR disease-causing mutations using ion torrent semiconductor sequencing. J Biomol Tech 23:24-30.
10. Forns X, Lawitz E, Zeuzem S, Gane EJ, Bronowicki J, Andreone P, Horban A, Brown AS, Peeters M, Lenz O, Ouwerkerk-Mahadevan S, Scott JA, Kalmeijer R, De La Rosa G, Sinha R, Beumont-Mauviel M. 2013. Simeprevir (TMC435) with peg-interferon α-2a/ribavirin for treatment of chronic HCV genotype 1 infection in patients who relapsed after previous interferon-based therapy: Efficacy and safety in patient sub-populations in the PROMISE phase III trial. Poster 1092 presented at the 64st Annual Meeting of American Association for the Study of Liver Diseases (AASLD), Washington, DC. USA. 1-5 November, 2013.
11. 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-naïve genotype 1 hepatitis C: The randomized PILLAR study. Hepatology 58:1918-1929.
12. Fujino H, Imamura M, Nagaoki Y, Kawakami Y, Abe H, Hayes CN, Kan H, Fukuhara T, Kobayashi T, Masaki K, Ono A, Nakahara T, Honda Y, Naeshiro N, Urabe A, Yokoyama S, Miyaki D, Murakami E, Kawaoka T, Hiraga N, Tsuge M, Hiramatsu A, Hyogo H, Aikata H, Takahashi S, Miki D, Ochi H, Ohishi W, Chayama K. Hiroshima Liver Study Group. 2013. Predictive value of the IFNL4 polymorphism on outcome of telaprevir, peginterferon, and ribavirin therapy for older patients with genotype 1b chronic hepatitis C. J Gastroenterol [Epub ahead of print].
13. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ, Sulkowski M, McHutchison JG, Goldstein DB. 2009. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461:399-401.
14. Hayashi N, Okanoue T, Tsubouchi H, Toyota J, Chayama K, Kumada H. 2012. Efficacy and safety of telaprevir, a new protease inhibitor, for difficult-to-treat patients with genotype 1 chronic hepatitis C. J Viral Hepat 19:e134-e142.
15. Hayashi N, Seto C, Kato M, Komada Y, Goto S. 2014. Once-daily simeprevir (TMC435) with peginterferon/ribavirin for treatment-naïve hepatitis C genotype 1-infected patients in Japan: The DRAGON study. J Gastroenterol 49:138-147.
16. Hézode C, Forestier N, Dusheiko G, Ferenci P, Pol S, Goeser T, Bronowicki JP, Bourlière M, Gharakhanian S, Bengtsson L, McNair L, George S, Kieffer T, Kwong A, Kauffman RS, Alam J, Pawlotsky JM, Zeuzem S. PROVE2 Study Team. 2009. Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med 360:1839-1850.
17. Hiraga N, Imamura M, Abe H, Hayes CN, Kono T, Onishi M, Tsuge M, Takahashi S, Ochi H, Iwao E, Kamiya N, Yamada I, Tateno C, Yoshizato K, Matsui H, Kanai A, Inaba T, Tanaka S, Chayama K. 2011. Rapid emergence of telaprevir resistant hepatitis C virus strain from wildtype clone in vivo. Hepatology 54:781-788.
18. Karino Y, Toyota J, Ikeda K, Suzuki F, Chayama K, Kawakami Y, Ishikawa H, Watanabe H, Hernandez D, Yu F, McPhee F, Kumada H. 2013. Characterization of virologic escape in hepatitis C virus genotype 1b patients treated with the direct-acting antivirals daclatasvir and asunaprevir. J Hepatol 58:646-654.
19. Kato N, Hijikata M, Ootsuyama Y, Nakagawa M, Ohkoshi S, Sugimura T, Shimotohno K. 1990. Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc Natl Acad Sci USA 87:9524-9528.
20. Kawakami Y, Suzuki F, Karino Y, Toyota J, Kumada H, Chayama K. 2013. Telaprevir is effective given every 12 hours at 750 mg with peginterferon-alfa-2b and ribavirin to Japanese patients with HCV-1b IL28B rs8099917 TT. Antivir Ther [Epub ahead of print].
21. Kumada H, Toyota J, Okanoue T, Chayama K, Tsubouchi H, Hayashi N. 2012. Telaprevir with peginterferon and ribavirin for treatment-naive patients chronically infected with HCV of genotype 1 in Japan. J Hepatol 56:78-84.
22. Lenz O, de Bruijne J, Vijgen L, Verbinnen T, Weegink C, Van Marck H, Vandenbroucke I, Peeters M, Simmen K, Fanning G, Verloes R, Picchio G, Reesink H. 2012. Efficacy of re-treatment with TMC435 as combination therapy in hepatitis C virus-infected patients following TMC435 monotherapy. Gastroenterology 143:1176-1178.
23. McHutchison JG, Everson GT, Gordon SC, Jacobson IM, Sulkowski M, Kauffman R, McNair L, Alam J, Muir AJ. PROVE1 Study Team. 2009. Telaprevir with peginterferon and ribavirin for chronic HCV genotype 1 infection. N Engl J Med 360:1827-1838.
24. McHutchison JG, Manns MP, Muir AJ, Terrault NA, Jacobson IM, Afdhal NH, Heathcote EJ, Zeuzem S, Reesink HW, Garg J, Bsharat M, George S, Kauffman RS, Adda N, Di Bisceglie AM. PROVE3 Study Team. 2010. Telaprevir for previously treated chronic HCV infection. N Engl J Med 362:1292-1303.
25. Nasu A, Marusawa H, Ueda Y, Nishijima N, Takahashi K, Osaki Y, Yamashita Y, Inokuma T, Tamada T, Fujiwara T, Sato F, Shimizu K, Chiba T. 2011. Genetic heterogeneity of hepatitis C virus in association with antiviral therapy determined by ultra-deep sequencing. PLoS ONE 6:e24907.
26. Ninomiya M, Ueno Y, Funayama R, Nagashima T, Nishida Y, Kondo Y, Inoue J, Kakazu E, Kimura O, Nakayama K, Shimosegawa T. 2012. Use of illumina deep sequencing technology to differentiate hepatitis C virus variants. J Clin Microbiol 50:857-866.
27. Ohnishi Y, Tanaka T, Ozaki K, Yamada R, Suzuki H, Nakamura Y. 2001. A high-throughput SNP typing system for genome-wide association studies. J Hum Genet 46:471-477.
28. Ozeki I, Akaike J, Karino Y, Arakawa T, Kuwata Y, Ohmura T, Sato T, Kamiya N, Yamada I, Chayama K, Kumada H, Toyota J. 2011. Antiviral effects of peginterferon alpha-2b and ribavirin following 24-week monotherapy of telaprevir in Japanese hepatitis C patients. J Gastroenterol 46:929-937.
29. Prokunina-Olsson L, Muchmore B, Tang W, Pfeiffer RM, Park H, Dickensheets H, Hergott D, Porter-Gill P, Mumy A, Kohaar I, Chen S, Brand N, Tarway M, Liu L, Sheikh F, Astemborski J, Bonkovsky HL, Edlin BR, Howell CD, Morgan TR, Thomas DL, Rehermann B, Donnelly RP, O'Brien TR. 2013. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat Genet 45:164-171.
30. Romano KP, Ali A, Royer WE, Schiffer CA. 2010. Drug resistance against HCV NS3/4A inhibitors is defined by the balance of substrate recognition versus inhibitor binding. Proc Natl Acad Sci USA 107:20986-20991.
31. Suppiah V, Moldovan M, Ahlenstiel G, Berg T, Weltman M, Abate ML, Bassendine M, Spengler U, Dore GJ, Powell E, Riordan S, Sheridan D, Smedile A, Fragomeli V, Müller T, Bahlo M, Stewart GJ, Booth DR, George J. 2009. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat Genet 41:1100-1104.
32. Suzuki A, Yamada R, Chang X, Tokuhiro S, Sawada T, Suzuki M, Nagasaki M, Nakayama-Hamada M, Kawaida R, Ono M, Ohtsuki M, Furukawa H, Yoshino S, Yukioka M, Tohma S, Matsubara T, Wakitani S, Teshima R, Nishioka Y, Sekine A, Iida A, Takahashi A, Tsunoda T, Nakamura Y, Yamamoto K. 2003. Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginie deminase 4, are associated with rheumatoid arthritis. Nat Genet 34:395-402.
33. Suzuki F, Sezaki H, Akuta N, Suzuki Y, Seko Y, Kawamura Y, Hosaka T, Kobayashi M, Saito S, Arase Y, Ikeda K, Kobayashi M, Mineta R, Watahiki S, Miyakawa Y, Kumada H. 2012. Prevalence of hepatitis C virus variants resistant to NS3 protease inhibitors or the NS5A inhibitor (BMS-790052) in hepatitis patients with genotype 1b. J Clin Virol 54:352-354.
34. Tanaka Y, Nishida N, Sugiyama M, Kurosaki M, Matsuura K, Sakamoto N, Nakagawa M, Korenaga M, Hino K, Hige S, Ito Y, Mita E, Tanaka E, Mochida S, Murawaki Y, Honda M, Sakai A, Hiasa Y, Nishiguchi S, Koike A, Sakaida I, Imamura M, Ito K, Yano K, Masaki N, Sugauchi F, Izumi N, Tokunaga K, Mizokami M. 2009. Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat Genet 41:1105-1109.
35. Vogel U, Szczepanowski R, Claus H, Jünemann S, Prior K, Harmsen D. 2012. Ion torrent personal genome machine sequencing for genomic typing of Neisseria meningitidis for rapid determination of multiple layers of typing information. J Clin Microbiol 50:1889-1894.
36. 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.