Characterization of orally efficacious influenza drug with high resistance barrier in ferrets and human airway epithelia

Science Translational Medicine

Volumn 11, Issue 515, 2019, Pages

  Toots, Mart ^a   Yoon, Jeong Joong ^a   Cox, Robert M ^a   Hart, Michael ^a   Sticher, Zachary M ^b   Makhsous, Negar ^c   Plesker, Roland ^d   Barrena, Alec H ^a   Reddy, Prabhakar G ^b   Mitchell, Deborah G ^b   Shean, Ryan C ^c   Bluemling, Gregory R ^b   Kolykhalov, Alexander A ^b   Greninger, Alexander L ^c   Natchus, Michael G ^b   Painter, George R ^b,e   Plemper, Richard K ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d PAUL EHRLICH INSTITUT   (Germany)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; EIDD 2801; UNCLASSIFIED DRUG; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG DETERMINATION; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG STRUCTURE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INFLAMMATION; INFLUENZA A; INFLUENZA B; INHIBITORY CONCENTRATION; MONOTHERAPY; MOUSE; MUSTELA PUTORIUS FURO; MUTAGENESIS; NONHUMAN; PANDEMIC INFLUENZA; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; SEASONAL INFLUENZA; VIRUS RESISTANCE; VIRUS SHEDDING; VIRUS TRANSMISSION; ANIMAL; ANTIVIRAL RESISTANCE; CONFOCAL MICROSCOPY; DOG; DRUG EFFECT; GENETICS; HIGH THROUGHPUT SEQUENCING; INFLUENZA; INFLUENZA A VIRUS (H1N1); MDCK CELL LINE; ORTHOMYXOVIRUS INFECTION; PATHOGENICITY;

ANIMALS; ANTIVIRAL AGENTS; DOGS; DRUG RESISTANCE, VIRAL; FEMALE; FERRETS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICROSCOPY, CONFOCAL; ORTHOMYXOVIRIDAE INFECTIONS; RNA, VIRAL;

EID: 85074100570     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aax5866     Document Type: Article

References (44)

1. P. Palese, M. L. Shaw, in Fields Virology, D. M. Knipe, P. M. Howley, Eds. (Wolters Kluwer/ Lippincott Williams & Wilkins, 2007), vol. 2, chap. 47, pp. 1647-1690.
2. G. Neumann, Y. Kawaoka, The first influenza pandemic of the new millennium. Influenza Other Respi. Viruses 5, 157-166 (2011).
3. G. Neumann, T. Noda, Y. Kawaoka, Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931-939 (2009).
4. World Health Organization, Influenza (seasonal) (World Health Organization 2019); www.who.int/news-room/fact-sheets/detail/influenza-(seasonal).
5. R. Garten, L. Blanton, A. I. A. Elal, N. Alabi, J. Barnes, M. Biggerstaff, L. Brammer, A. P. Budd, E. Burns, C. N. Cummings, T. Davis, S. Garg, L. Gubareva, Y. Jang, K. Kniss, N. Kramer, S. Lindstrom, D. Mustaquim, A. O'Halloran, W. Sessions, C. Taylor, X. Xu, V. G. Dugan, A. M. Fry, D. E. Wentworth, J. Katz, D. Jernigan, Update: Influenza activity in the United States during the 2017-18 season and composition of the 2018-19 influenza vaccine. MMWR Morb. Mortal. Wkly Rep. 67, 634-642 (2018).
6. D. M. Skowronski, C. Chambers, G. De Serres, J. A. Dickinson, A. L. Winter, R. Hickman, T. Chan, A. N. Jassem, S. J. Drews, H. Charest, J. B. Gubbay, N. Bastien, Y. Li, M. Krajden, Early season co-circulation of influenza A(H3N2) and B(Yamagata): Interim estimates of 2017/18 vaccine effectiveness, Canada, January 2018. Euro Surveill. 23, 10.2807/1560-7917.ES.2018.23.5.18-00035 (2018).
7. M. Hussain, H. D. Galvin, T. Y. Haw, A. N. Nutsford, M. Husain, Drug resistance in influenza A virus: The epidemiology and management. Infect Drug Resist 10, 121-134 (2017).
8. R. A. Bright, D. Shay, J. Bresee, A. Klimov, N. Cox, J. Ortiz, W. C. Ctr, CDC, High levels of adamantane resistance among influenza A (H3N2) viruses and interim guidelines for use of antiviral agents - United States, 2005-06 influenza season (reprinted by MMWR, vol 55, pp. 44-46, 2006). Jama. J. Am. Med. Assoc. 295, 881-882 (2006).
9. F. G. Hayden, N. Sugaya, N. Hirotsu, N. Lee, M. D. de Jong, A. C. Hurt, T. Ishida, H. Sekino, K. Yamada, S. Portsmouth, K. Kawaguchi, T. Shishido, M. Arai, K. Tsuchiya, T. Uehara, A. Watanabe; Baloxavir Marboxil Investigators Group, Baloxavir marboxil for uncomplicated influenza in adults and adolescents. N. Engl. J. Med. 379, 913-923 (2018).
10. J. J. Yoon, M. Toots, S. Lee, M. E. Lee, B. Ludeke, J. M. Luczo, K. Ganti, R. M. Cox, Z. M. Sticher, V. Edpuganti, D. G. Mitchell, M. A. Lockwood, A. A. Kolykhalov, A. L. Greninger, M. L. Moore, G. R. Painter, A. C. Lowen, S. M. Tompkins, R. Fearns, M. G. Natchus, R. K. Plemper, Orally efficacious broad-spectrum ribonucleoside analog inhibitor of influenza and respiratory syncytial viruses. Antimicrob. Agents Chemother. 62, e00766-18 (2018).
11. N. M. Bouvier, A. C. Lowen, Animal models for influenza virus pathogenesis and transmission. Viruses 2, 1530-1563 (2010).
12. E. A. Govorkova, B. M. Marathe, A. Prevost, J. E. Rehg, R. G. Webster, Assessment of the efficacy of the neuraminidase inhibitor oseltamivir against 2009 pandemic H1N1 influenza virus in ferrets. Antiviral Res. 91, 81-88 (2011).
13. A. C. Marriott, B. K. Dove, C. J. Whittaker, C. Bruce, K. A. Ryan, T. J. Bean, E. Rayner, G. Pearson, I. Taylor, S. Dowall, J. Plank, E. Newman, W. S. Barclay, N. J. Dimmock, A. J. Easton, B. Hallis, N. J. Silman, M. W. Carroll, Low dose influenza virus challenge in the ferret leads to increased virus shedding and greater sensitivity to oseltamivir. PLOS ONE 9, e94090 (2014).
14. T. Enkirch, V. von Messling, Ferret models of viral pathogenesis. Virology 479-480, 259-270 (2015).
15. N. Urakova, V. Kuznetsova, D. K. Crossman, A. Sokratian, D. B. Guthrie, A. A. Kolykhalov, M. A. Lockwood, M. G. Natchus, M. R. Crowley, G. R. Painter, E. I. Frolova, I. Frolov, D-N4-hydroxycytidine is a potent anti-alphavirus compound that induces a high level of mutations in the viral genome. J. Virol. 92, e01965-17 (2018).
16. L. J. Stuyver, T. Whitaker, T. R. McBrayer, B. I. Hernandez-Santiago, S. Lostia, P. M. Tharnish, M. Ramesh, C. K. Chu, R. Jordan, J. X. Shi, S. Rachakonda, K. A. Watanabe, M. J. Otto, R. F. Schinazi, Ribonucleoside analogue that blocks replication of bovine viral diarrhea and hepatitis C viruses in culture. Antimicrob. Agents Chemother. 47, 244-254 (2003).
17. H. Lin, H. Li, H. J. Cho, S. Bian, H. J. Roh, M. K. Lee, J. S. Kim, S. J. Chung, C. K. Shim, D. D. Kim, Air-liquid interface (ALI) culture of human bronchial epithelial cell monolayers as an in vitro model for airway drug transport studies. J. Pharm. Sci. 96, 341-350 (2007).
18. H. Mitchell, D. Levin, S. Forrest, C. A. Beauchemin, J. Tipper, J. Knight, N. Donart, R. C. Layton, J. Pyles, P. Gao, K. S. Harrod, A. S. Perelson, F. Koster, Higher level of replication efficiency of 2009 (H1N1) pandemic influenza virus than those of seasonal and avian strains: Kinetics from epithelial cell culture and computational modeling. J. Virol. 85, 1125-1135 (2011).
19. N. R. Hackett, R. Shaykhiev, M. S. Walters, R. Wang, R. K. Zwick, B. Ferris, B. Witover, J. Salit, R. G. Crystal, The human airway epithelial basal cell transcriptome. PLOS ONE 6, e18378 (2011).
20. N.-H. Wu, W. Yang, A. Beineke, R. Dijkman, M. Matrosovich, W. Baumgartner, V. Thiel, P. Valentin-Weigand, F. D. Meng, G. Herrler, The differentiated airway epithelium infected by influenza viruses maintains the barrier function despite a dramatic loss of ciliated cells. Sci Rep. 6, 39668 (2016).
21. K. Balogh Sivars, U. Sivars, E. Hornberg, H. Zhang, L. Branden, R. Bonfante, S. Huang, S. Constant, I. Robinson, C. J. Betts, P. M. Aberg, A 3D human airway model enables prediction of respiratory toxicity of inhaled drugs in vitro. Toxicol. Sci. 162, 301-308 (2018).
22. S. Sultana, M. Solotchi, A. Ramachandran, S. S. Patel, Transcriptional fidelities of human mitochondrial POLRMT, yeast mitochondrial Rpo41, and phage T7 single-subunit RNA polymerases. J. Biol. Chem. 292, 18145-18160 (2017).
23. L. A. Carolan, S. Rockman, K. Borg, T. Guarnaccia, P. Reading, J. Mosse, A. Kelso, I. Barr, K. L. Laurie, Characterization of the Localized Immune Response in the Respiratory Tract of Ferrets following Infection with Influenza A and B Viruses. J. Virol. 90, 2838-2848 (2015).
24. K. L. Oslund, N. Baumgarth, Influenza-induced innate immunity: Regulators of viral replication, respiratory tract pathology & adaptive immunity. Future Virol. 6, 951-962 (2011).
25. A. Danesh, C. Seneviratne, C. M. Cameron, D. Banner, M. E. Devries, A. A. Kelvin, L. Xu, L. Ran, S. E. Bosinger, T. Rowe, M. Czub, C. B. Jonsson, M. J. Cameron, D. J. Kelvin, Cloning, expression and characterization of ferret CXCL10. Mol. Immunol. 45, 1288-1297 (2008).
26. I. N. Moore, E. W. Lamirande, M. Paskel, D. Donahue, H. Kenney, J. Qin, K. Subbarao, Severity of clinical disease and pathology in ferrets experimentally infected with influenza viruses is influenced by inoculum volume. J. Virol. 88, 13879-13891 (2014).
27. E. J. Schrauwen, S. Herfst, S. Chutinimitkul, T. M. Bestebroer, G. F. Rimmelzwaan, A. D. Osterhaus, T. Kuiken, R. A. Fouchier, Possible increased pathogenicity of pandemic (H1N1) 2009 influenza virus upon reassortment. Emerg. Infect. Dis. 17, 200-208 (2011).
28. J. M. van den Brand, K. J. Stittelaar, L. M. Leijten, G. van Amerongen, J. H. Simon, A. D. Osterhaus, T. Kuiken, Modification of the ferret model for pneumonia from seasonal human influenza A virus infection. Vet. Pathol. 49, 562-568 (2012).
29. Y. Furuta, B. B. Gowen, K. Takahashi, K. Shiraki, D. F. Smee, D. L. Barnard, Favipiravir (T-705), a novel viral RNA polymerase inhibitor. Antiviral Res. 100, 446-454 (2013).
30. Anonymous. Summary of press conference after Tamura (Ministry of Health, Welfare and Labor, Tokyo, Japan (2014); www.mhlw.go.jp/stf/kaiken/daijin/0000054819.html.
31. T. Baranovich, S. S. Wong, J. Armstrong, H. Marjuki, R. J. Webby, R. G. Webster, E. A. Govorkova, T-705 (favipiravir) induces lethal mutagenesis in influenza A H1N1 viruses in vitro. J. Virol. 87, 3741-3751 (2013).
32. T. Daikoku, Y. Yoshida, T. Okuda, K. Shiraki, Characterization of susceptibility variants of influenza virus grown in the presence of T-705. J. Pharmacol. Sci. 126, 281-284 (2014).
33. D. H. Goldhill, A. J. W. Te Velthuis, R. A. Fletcher, P. Langat, M. Zambon, A. Lackenby, W. S. Barclay, The mechanism of resistance to favipiravir in influenza. Proc. Natl. Acad. Sci. U.S.A. 115, 11613-11618 (2018).
34. A. Les, L. Adamowicz, W. Rode, Structure and conformation of N4-hydroxycytosine and N4-hydroxy-5-fluorocytosine. A theoretical ab initio study. Biochim. Biophys. Acta 1173, 39-48 (1993).
35. J. Meng, C. C. Stobart, A. L. Hotard, M. L. Moore, An overview of respiratory syncytial virus. PLOS Pathog. 10, e1004016 (2014).
36. S. Crotty, C. E. Cameron, R. Andino, RNA virus error catastrophe: Direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. U.S.A. 98, 6895-6900 (2001).
37. Z. Jin, L. K. Smith, V. K. Rajwanshi, B. Kim, J. Deval, The ambiguous base-pairing and high substrate efficiency of T-705 (Favipiravir) Ribofuranosyl 5'-triphosphate towards influenza A virus polymerase. PLOS ONE 8, e68347 (2013).
38. I. W. Y. Mak, N. Evaniew, M. Ghert, Lost in translation: Animal models and clinical trials in cancer treatment. Am. J. Transl. Res. 6, 114-118 (2014).
39. H. B. van der Worp, D. W. Howells, E. S. Sena, M. J. Porritt, S. Rewell, V. O'Collins, M. R. Macleod, Can animal models of disease reliably inform human studies? PLOS Med. 7, e1000245 (2010).
40. P. J. K. van Meer, M. Kooijman, C. C. Gispen-de Wied, E. H. M. Moors, H. Schellekens, The ability of animal studies to detect serious post marketing adverse events is limited. Regul. Toxicol. Pharmacol. 64, 345-349 (2012).
41. M. Weisshaar, R. Cox, Z. Morehouse, S. Kumar Kyasa, D. Yan, P. Oberacker, S. Mao, J. E. Golden, A. C. Lowen, M. G. Natchus, R. K. Plemper, Identification and characterization of influenza virus entry inhibitors through dual myxovirus high-throughput screening. J. Virol. 90, 7368-7387 (2016).
42. H. Li, R. Durbin, Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
43. D. C. Koboldt, Q. Zhang, D. E. Larson, D. Shen, M. D. McLellan, L. Lin, C. A. Miller, E. R. Mardis, L. Ding, R. K. Wilson, VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568-576 (2012).
44. K. Wang, M. Li, H. Hakonarson, ANNOVAR: Functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).