The susceptibility of circulating human influenza viruses to tizoxanide, the active metabolite of nitazoxanide

Antiviral Research

Volumn 147, Issue , 2017, Pages 142-148

  Tilmanis, Danielle ^a   van Baalen, Carel ^b   Oh, Ding Yuan ^a,c   Rossignol, Jean Francois ^d   Hurt, Aeron C ^a,e  

^a VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

^b ViroClinics Biosciences BV   (Netherlands)

^c UNIVERSITY OF BALLARAT   (Australia)

^d Romark Laboratories   (United States)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antiviral activity; Focus reduction assay; Influenza; Nitazoxanide; Resistance; Susceptibility

Indexed keywords

HEMAGGLUTININ; NITAZOXANIDE; TIZOXANIDE; ANTIVIRUS AGENT; ENZYME INHIBITOR; SIALIDASE; THIAZOLE DERIVATIVE;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; CELL MIGRATION; CYTOTOXICITY; CYTOTOXICITY ASSAY; DRUG DETERMINATION; EC50; HUMAN; IN VITRO STUDY; INFLUENZA; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA VIRUS; MDCK CELL LINE; NONHUMAN; PRIORITY JOURNAL; VIRUS TITRATION; WORLD HEALTH ORGANIZATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DOG; DRUG EFFECT; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); INFLUENZA B VIRUS; LD50; METABOLISM; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; SERODIAGNOSIS;

ANIMALS; ANTIVIRAL AGENTS; CELL SURVIVAL; DOGS; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; LETHAL DOSE 50; MADIN DARBY CANINE KIDNEY CELLS; NEURAMINIDASE; NEUTRALIZATION TESTS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; THIAZOLES;

EID: 85032281018     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2017.10.002     Document Type: Article

References (33)

1. Ashton, L.V., Callan, R.L., Rao, S., Landolt, G.A., Vitro susceptibility of canine influenza A (H3N8) virus to nitazoxanide and tizoxanide. Veterinary Medicine International 2010, 2010, 891010.
2. Belardo, G., Cenciarelli, O., La Frazia, S., Rossignol, J.F., Santoro, M.G., Synergistic effect of nitazoxanide with neuraminidase inhibitors against influenza a viruses in vitro. Antimicrob. Agents Chemother. 59 (2015), 1061–1069.
3. Belardo, G., La Frazia, S., Cenciarelli, O., Carta, S., Rossignol, J.F., Santoro, M.G., Nitazoxanide, a novel potential anti-influenza drug, acting in synergism with neuraminidase inhibitors. 49th Infectious Disease Society of America Annual Meeting, Boston, Massachusetts USA, Paper 31075, 2011.
4. Broekhuysen, J., Stockis, A., Lins, R.L., De Graeve, J., Rossignol, J.F., Nitazoxanide: pharmacokinetics and metabolism in man. Int. J. Clin. Pharmacol. Ther. 38 (2000), 387–394.
5. Byrn, R.A., Jones, S.M., Bennett, H.B., Bral, C., Clark, M.P., Jacobs, M.D., Kwong, A.D., Ledeboer, M.W., Leeman, J.R., McNeil, C.F., Murcko, M.A., Nezami, A., Perola, E., Rijnbrand, R., Saxena, K., Tsai, A.W., Zhou, Y., Charifson, P.S., Preclinical activity of VX-787, a first-in-class, orally bioavailable inhibitor of the influenza virus polymerase PB2 subunit. Antimicrob. Agents Chemother. 59 (2015), 1569–1582.
6. Costantino, C., Vitale, F., Influenza vaccination in high-risk groups: a revision of existing guidelines and rationale for an evidence-based preventive strategy. J. Prev. Med. Hyg. 57 (2016), E13–E18.
7. de Chassey, B., Meyniel-Schicklin, L., Vonderscher, J., Andre, P., Lotteau, V., Virus-host interactomics: new insights and opportunities for antiviral drug discovery. Genome Med., 6, 2014.
8. Dobson, J., Whitley, R.J., Pocock, S., Monto, A.S., Articles: oseltamivir treatment for influenza in adults: a meta-analysis of randomised controlled trials. Lancet 385 (2015), 1729–1737.
9. Farrukee, R., Leang, S.-K., Butler, J., Lee, R.T.C., Maurer-Stroh, S., Tilmanis, D., Sullivan, S., Mosse, J., Barr, I.G., Hurt, A.C., Influenza viruses with B/Yamagata- and B/Victoria-like neuraminidases are differentially affected by mutations that alter antiviral susceptibility. J. Antimicrob. Chemother. (JAC) 70 (2015), 2004–2012.
10. Fiore, A.E., Fry, A., Shay, D., Gubareva, L., Bresee, J.S., Uyeki, T.M., Antiviral agents for the treatment and chemoprophylaxis of influenza: recommendations of the advisory committee on immunization practices (ACIP). Centers Dis. Control Prev., 2011, 1–27.
11. Haffizulla, J., Hartman, A., Hoppers, M., Resnick, H., Samudrala, S., Ginocchio, C., Bardin, M., Rossignol, J.F., Group, U.S.N.I.C.S., Effect of nitazoxanide in adults and adolescents with acute uncomplicated influenza: a double-blind, randomised, placebo-controlled, phase 2b/3 trial. Lancet. Infect. Dis. 14 (2014), 609–618.
12. Hurt, A.C., The epidemiology and spread of drug resistant human influenza viruses. Curr. Opin. Virol. 8 (2014), 22–29.
13. Hurt, A.C., Besselaar, T.G., Daniels, R.S., Ermetal, B., Fry, A., Gubareva, L., Huang, W., Lackenby, A., Lee, R.T.C., Lo, J., Maurer-Stroh, S., Nguyen, H.T., Pereyaslov, D., Rebelo-de-Andrade, H., Siqueira, M.M., Takashita, E., Tashiro, M., Tilmanis, D., Wang, D., Zhang, W., Meijer, A., Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2014–2015. Antivir. Res. 132 (2016), 178–185.
14. Jones, J.C., Marathe, B.M., Lerner, C., Kreis, L., Gasser, R., Pascua, P.N.Q., Najera, I., Govorkova, E.A., A novel endonuclease inhibitor exhibits broad-spectrum anti-influenza virus activity in vitro. Antimicrob. Agents Chemother. 60 (2016), 5504–5514.
15. Kossyvakis, A., Mentis, A.F.A., Tryfinopoulou, K., Pogka, V., Kalliaropoulos, A., Antalis, E., Lytras, T., Meijer, A., Tsiodras, S., Karakitsos, P., Mentis, A.F., Antiviral susceptibility profile of influenza A viruses keep an eye on immunocompromised patients under prolonged treatment. Eur. J. Clin. Microbiol. Infect. Dis., 2017, 361–371.
16. Koszalka, P., Tilmanis, D., Hurt, A.C., Influenza antivirals currently in late-phase clinical trial. Influenza Other Respir. Viruses, 240–246, 2017.
17. Lambert, L.C., Fauci, A.S., Influenza vaccines for the future. N. Engl. J. Med. 363 (2010), 2036–2044.
18. Li, T.C.M., Chan, M.C.W., Lee, N., Clinical implications of antiviral resistance in influenza. Viruses 7 (2015), 4929–4944.
19. Lin, Y., Gu, Y., Wharton, S.A., Whittaker, L., Gregory, V., Li, X., Metin, S., Cattle, N., Daniels, R.S., Hay, A.J., McCauley, J.W., Optimisation of a micro-neutralisation assay and its application in antigenic characterisation of influenza viruses. Influenza Other Respir. Viruses, 2015, 331–340.
20. Loregian, A., Mercorelli, B., Nannetti, G., Compagnin, C., Palù, G., Antiviral strategies against influenza virus: towards new therapeutic approaches. Cell. Mol. life Sci. 71 (2014), 3659–3683.
21. Louie, J.K., Yang, S., Acosta, M., Yen, C., Samuel, M.C., Schechter, R., Guevara, H., Uyeki, T.M., Treatment with neuraminidase inhibitors for critically ill patients with influenza A (H1N1) pdm09. Clin. Infect. Dis., 2012, 1198–1204.
22. Matrosovich, M., Matrosovich, T., Carr, J., Roberts, N.A., Klenk, H.D., Overexpression of the alpha-2,6-sialyltransferase in MDCK cells increases influenza virus sensitivity to neuraminidase inhibitors. J. Virol. 77 (2003), 8418–8425.
23. Mosmann, T., Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983), 55–63.
24. Naesens, L., Stevaert, A., Vanderlinden, E., Antiviral therapies on the horizon for influenza. Curr. Opin. Pharmacol. 30 (2016), 106–115.
25. Perwitasari, O., Johnson, S., Yan, X., Howerth, E., Shacham, S., Landesman, Y., Baloglu, E., McCauley, D., Tamir, S., Tompkins, S.M., Verdinexor, a novel selective inhibitor of nuclear export, reduces influenza a virus replication in vitro and in vivo. J. Virol. 88 (2014), 10228–10243.
26. Rossignol, J.-F., Review: nitazoxanide: A first-in-class broad-spectrum antiviral agent. Antivir. Res. 110 (2014), 94–103.
27. Rossignol, J.F., Nitazoxanide: a first-in-class indirect-acting antiviral for treatment of respiratory virus infections. Fifth Isirv-Antiviral Group Conference Abstract S10–S17 P58, Shanghai, China, 2017.
28. Rossignol, J.F., La Frazia, S., Chiappa, L., Ciucci, A., Santoro, M.G., Thiazolides, a new class of anti-influenza molecules targeting viral hemagglutinin at the post-translational level. J. Biol. Chem. 284 (2009), 29798–29808.
29. Sleeman, K., Mishin, V.P., Guo, Z., Garten, R.J., Balish, A., Fry, A.M., Villanueva, J., Stevens, J., Gubareva, L.V., Antiviral susceptibility of variant influenza A(H3N2)v viruses isolated in the United States from 2011 to 2013. Antimicrob. Agents Chemother. 58 (2014), 2045–2051.
30. Takashita, E., Meijer, A., Lackenby, A., Gubareva, L., Rebelo-de-Andrade, H., Besselaar, T., Fry, A., Gregory, V., Leang, S.-K., Huang, W., Lo, J., Pereyaslov, D., Siqueira, M.M., Wang, D., Mak, G.C., Zhang, W., Daniels, R.S., Hurt, A.C., Tashiro, M., Global update on the susceptibility of human influenza viruses to neuraminidase inhibitors, 2013–2014. Antivir. Res. 117 (2015), 27–38.
31. Terletskaia-Ladwig, E., Meier, S., Enders, M., Improved high-throughput virus neutralisation assay for antibody estimation against pandemic and seasonal influenza strains from 2009 to 2011. J. Virol. Methods 189 (2013), 341–347.
32. van Baalen, C.A., Jeeninga, R.E., Penders, G.H.W.M., van Gent, B., van Beek, R., Koopmans, M.P.G., Rimmelzwaan, G.F., ViroSpot microneutralization assay for antigenic characterization of human influenza viruses. Vaccine 35 (2017), 46–52.
33. Zhang, J.H., Chung, T.D.Y., Oldenburg, K.R., A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen 4 (1999), 67–73.