In vitro and in vivo efficacy of fluorodeoxycytidine analogs against highly pathogenic avian influenza H5N1, seasonal, and pandemic H1N1 virus infections

Antiviral Research

Volumn 92, Issue 2, 2011, Pages 329-340

  Kumaki, Yohichi ^a   Day, Craig W ^a   Smee, Donald F ^a   Morrey, John D ^a   Barnard, Dale L ^a  

^a UTAH STATE UNIVERSITY   (United States)

Author keywords

2' Deoxy 2' fluorocytidine; BALB c mouse; Fluorodeoxyribonucleosides; H5N1 avian influenza virus; Pandemic H1N1 virus

Indexed keywords

2' AZIDO 2' DEOXYCYTIDINE; 2' DEOXY 2' FLUOROADENOSINE; 2' FLUORO 2' DEOXYCYTIDINE; 2' FLUORO 2' DEOXYGUANOSINE; 2' FLUORO 2' DEOXYURIDINE; 2' IODO 2' DEOXYCYTIDINE; CYTIDINE DERIVATIVE; FLUCYTOSINE DEOXYRIBOSIDE; GEMCITABINE; NEUTRAL RED; OSELTAMIVIR; RIBAVIRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ARTICLE; CELL STRAIN; CONTROLLED STUDY; DRUG EFFICACY; DRUG TOLERABILITY; FEMALE; HISTOPATHOLOGY; IC 50; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA A (H5N1); INFLUENZA B; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; INFLUENZA VIRUS B; LETHAL DOSE; LUNG WEIGHT; MAXIMUM TOLERATED DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; TREATMENT RESPONSE; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; DEOXYCYTIDINE; DOGS; FEMALE; HISTOCYTOCHEMISTRY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INJECTIONS, INTRAPERITONEAL; LUNG; MICE; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; VIRAL LOAD;

AVES; AVIAN INFLUENZA VIRUS; MUS; ORTHOMYXOVIRIDAE;

EID: 80054853586     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2011.09.001     Document Type: Article

References (58)

1. Aoki F.Y., Boivin G., Roberts N. Influenza virus susceptibility and resistance to oseltamivir. Antiviral Ther. 2007, 12:603-616.
2. Bajramovic J.J., Volmer R., Syan S., Pochet S., Gonzalez-Dunia D. 2'-Fluoro-2'-deoxycytidine inhibits Borna disease virus replication and spread. Antimicrob. Agents Chemother. 2004, 48:1422-1425.
3. Bianchi V., Borella S., Calderazzo F., Ferraro P., Chieco Bianchi L., Reichard P. Inhibition of ribonucleotide reductase by 2'-substituted deoxycytidine analogs: possible application in AIDS treatment. Proc. Natl. Acad. Sci. USA 1994, 91:8403-8407.
4. Bjursell G., Skoog L., Thelander L., Söderman G. 2'-Deoxy-2'-azidocytidine inhibits the initiation of polyoma DNA synthesis. Proc. Natl. Acad. Sci. USA 1977, 74:5310-5313.
5. Bland M. An Introduction to Medical Statistics 2000, Oxford University Press, Oxford, New York. third ed.
6. Blandin M., Tran-Dinh-Son S., Catlin J.C., Guschlbauer W. Nucleoside conformations. 16. Nuclear magnetic resonance and circular dichroism studies on pyrimidine-2'-fluoro-2'-deoxyribonucleosides. Biochim. Biophys. Acta 1974, 361:249-256.
7. Centers for Disease Control and Prevention, 1997. Isolation of Avian Influenza A(H5N1) Viruses from Humans - Hong Kong, May-December 1997. MMWR 46, pp. 1204-1207.
8. Centers for Disease Control and Prevention, 1998a. Isolation of Avian Influenza A(H5N1) Viruses from Humans - Hong Kong, May-December 1997. JAMA 279, pp. 263-264.
9. Centers for Disease Control and Prevention, 1998b. Update: Isolation of Avian Influenza A(H5N1) Viruses from Humans - Hong Kong, 1997-1998. JAMA 279, pp. 347-348.
10. Centers for Disease Control and Prevention, 1998c. Update: Isolation of Avian Influenza A(H5N1) Viruses from Humans - Hong Kong, 1997-1998. MMWR 46, pp. 1245-1247.
11. Chen H., Cheung C.L., Tai H., Zhao P., Chan J.F., Cheng V.C., Chan K.H., Yuen K.Y. Oseltamivir-resistant influenza A pandemic (H1N1) 2009 virus, Hong Kong. Emerg. Infect. Dis. 2009, 15:1970-1972.
12. Claas E.C., Osterhaus A.D., van Beek R., De Jong J.C., Rimmelzwaan G.F., Senne D.A., Krauss S., Shortridge K.F., Webster R.G. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 1998, 351:472-477.
13. De Clercq E., Beres J., Bentrude W.G. Potent activity of 5-fluoro-2'-deoxyuridine and related compounds against thymidine kinase-deficient (TK-) herpes simplex virus: targeted at thymidylate synthase. Mol. Pharmacol. 1987, 32:286-292.
14. Dunnett C.W., Tamhane A.C. Comparisons between a new drug and active and placebo controls in an efficacy clinical trial. Stat. Med. 1992, 11:1057-1063.
15. Furuta Y., Takahashi K., Fukuda Y., Kuno M., Kamiyama T., Kozaki K., Nomura N., Egawa H., Minami S., Watanabe Y., Narita H., Shiraki K. In vitro and in vivo activities of anti-influenza virus compound T-705. Antimicrob. Agents Chemother. 2002, 46:977-981.
16. Furuta Y., Takahashi K., Kuno-Maekawa M., Sangawa H., Uehara S., Kozaki K., Nomura N., Egawa H., Shiraki K. Mechanism of action of T-705 against influenza virus. Antimicrob. Agents Chemother. 2005, 49:981-986.
17. Giacca M., Borella S., Calderazzo F., Bianchi L.C., D'Agaro P., Rampazzo C., Bianchi V., Reichard P. Synergistic antiviral action of ribonucleotide reductase inhibitors and 3'-azido-3'-deoxythymidine on HIV type 1 infection in vitro. AIDS Res. Hum. Retroviruses 1996, 12:677-682.
18. Govorkova E.A., Leneva I.A., Goloubeva O.G., Bush K., Webster R.G. Comparison of efficacies of RWJ-270201, zanamivir, and oseltamivir against H5N1, H9N2, and other avian influenza viruses. Antimicrob. Agents Chemother. 2001, 45:2723-2732.
19. Gubareva L.V., McCullers J.A., Bethell R.C., Webster R.G. Characterization of Influenza A/HongKong/156/97 (H5N1) Virus in a Mouse Model and Protective Effect of Zanamivir on H5N1 Infection in Mice. J. Infect. Dis. 1998, 178:1592-1596.
20. Hatta M., Hatta Y., Kim J.H., Watanabe S., Shinya K., Nguyen T., Lien P.S., Le Q.M., Kawaoka Y. Growth of H5N1 influenza A viruses in the upper respiratory tracts of mice. PLoS Pathog. 2007, 3:1374-1379.
21. Hayden F.G. Pandemic influenza: is an antiviral response realistic?. Ped. Infect. Dis. J. 2004, 23:S262-269.
22. Heinemann V., Schulz L., Issels R.D., Plunkett W. Gemcitabine: a modulator of intracellular nucleotide and deoxynucleotide metabolism. Semin. Oncol. 1995, 22:11-18.
23. Hernandez, J.E., Adiga, R., Armstrong, R., Bazan, J., Bonilla, H., Bradley, J., Dretler, R., Ison, M.G., Mangino, J.E., Maroushek, S., Shetty, A.K., Wald, A., Ziebold, C., Elder, J., Hollister, A.S., Sheridan, W., and on behalf of the eIND Peramivir Investigators, 2011. Clinical experience in adults and children treated with intravenous peramivir for 2009 influenza A (H1N1) under an Emergency IND Program in the United States. Clin. Infect. Dis. 52, 695-706.
24. Jaccard J., Becker M.A., Wood G. Pairwise multiple comparison procedures: a review. Psycholog. Bull. 1984, 96:589-596.
25. Jakeman K.J., Tisdale M., Russell S., Leone A., Sweet C. Efficacy of 2'-deoxy-2'-fluororibosides against influenza A and B viruses in ferrets. Antimicrob. Agents Chemother. 1994, 38:1864-1867.
26. Kumaki Y., Wandersee M.K., Smith A.J., Zhou Y., Simmons G., Nelson N.M., Bailey K.W., Vest Z.G., Li J.K., Chan P.K., Smee D.F., Barnard D.L. Inhibition of severe acute respiratory syndrome coronavirus replication in a lethal SARS-CoV BALB/c mouse model by stinging nettle lectin, Urtica dioica agglutinin. Antiviral Res. 2011, 90-22-32.
27. Kwon H.I., Song M.S., Pascua P.N.Q., Baek Y.H., Lee J.H., Hong S.-P., Rho J.-B., Kim J.-K., Poo H., Kim C.-J., Choi Y.K. Genetic characterization and pathogenicity assessment of highly pathogenic H5N1 avian influenza viruses isolated from migratory wild birds in 2011, South Korea. Virus Res. 2011, 160:305-315.
28. Lee E.T., Wang J.W. Statistical Methods for Survival Data Analysis 2003, Wiley-Interscience, Hoboken, N.J. third ed.
29. Leneva I.A., Roberts N., Govorkova E.A., Goloubeva O.G., Webster R.G. The neuraminidase inhibitor GS4104 (oseltamivir phosphate) is efficacious against A/Hong Kong/156/97 (H5N1) and A/Hong Kong/1074/99 (H9N2) influenza viruses. Antiviral Res. 2000, 48:101-115.
30. Lu X., Tumpey T.M., Morken T., Zaki S.R., Cox N.J., Katz J.M. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J. Virol. 1999, 73:5903-5911.
31. Moscona A. Neuraminidase inhibitors for influenza. New England J Med 2005, 353:1363-1373.
32. Naughtin M., Dyason J.C., Mardy S., Sorn S., von Itzstein M., Buchy P. Neuraminidase inhibitor sensitivity and receptor-binding specificity of Cambodian clade 1 highly pathogenic H5N1 influenza virus. Antimicrob. Agents Chemother. 2011, 55:2004-2010.
33. Preziosi P. Influenza pharmacotherapy: present situation, strategies and hopes. Expert Opin. Pharmacother. 2011, 12:1523-1549.
34. Puthavathana P., Auewarakul P., Charoenying P.C., Sangsiriwut K., Pooruk P., Boonnak K., Khanyok R., Thawachsupa P., Kijphati R., Sawanpanyalert P. Molecular characterization of the complete genome of human influenza H5N1 virus isolates from Thailand. J. Gen. Virol. 2005, 86:423-433.
35. Reed L.J., Muench N. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 1938, 27:493-497.
36. Richardson F.C., Kuchta R.D., Mazurkiewicz A., Richardson K.A. Polymerization of 2'-fluoro- and 2'-O-methyl-dNTPs by human DNA polymerase [alpha], polymerase [gamma], and primase. Biochem. Pharmacol. 2000, 59:1045-1052.
37. Sai K., Saito Y. Ethnic differences in the metabolism, toxicology and efficacy of three anticancer drugs. Expert Opin. Drug Metab. Toxicol. 2011, 7:967-988.
38. Shao J., Zhou B., Chu B., Yen Y. Ribonucleotide reductase inhibitors and future drug design. Curr. Cancer Drug Targets 2006, 6:409-431.
39. Shi J., Du J., Ma T., Pankiewicz K.W., Patterson S.E., Tharnish P.M., McBrayer T.R., Stuyver L.J., Otto M.J., Chu C.K., Schinazi R.F., Watanabe K.A. Synthesis and anti-viral activity of a series of d- and l-2'-deoxy-2'-fluororibonucleosides in the subgenomic HCV replicon system. Bioorg. Med. Chem. 2005, 13:1641-1652.
40. Sidwell R.W., Bailey K.W., Wong M.H., Barnard D.L., Smee D.F. In vitro and in vivo influenza virus-inhibitory effects of viramidine. Antiviral Res. 2005, 68:10-17.
41. Sidwell R.W., Bailey K.W., Wong M.H., Huffman J.H. In vitro and in vivo sensitivity of a non-mouse-adapted influenza A (Beijing) virus infection to amantadine and ribavirin. Chemotherapy 1995, 41:455-461.
42. Sidwell R.W., Barnard D.L., Day C.W., Smee D.F., Bailey K.W., Wong M.H., Morrey J.D., Furuta Y. Efficacy of orally administered T-705 on lethal avian influenza A (H5N1) virus infections in mice. Antimicrob. Agents Chemother. 2007, 51:845-851.
43. Sidwell R.W., Smee D.F. In vitro and in vivo assay systems for study of influenza virus inhibitors. Antiviral Res. 2000, 48:1-16.
44. Sidwell R.W., Smee D.F., Huffman J.H., Barnard D.L., Bailey K.W., Morrey J.D., Babu Y.S. In vivo influenza virus-inhibitory effects of the cyclopentane neuraminidase inhibitor RJW-270201. Antimicrob. Agents Chemother. 2001, 45:749-757.
45. Skoog L., Bjursell G., Thelander L., Hagerstrom T., Hobbs J., Eckstein F. 2'-Deoxy-2'-azidocytidine, a new inhibitor of DNA replication in mammalian cells. Eur. J. Biochem. 1977, 72:371-378.
46. Smee D.F., Huffman J.H., Morrison A.C., Barnard D.L., Sidwell R.W. Cyclopentane neuraminidase inhibitors with potent in vitro anti-influenza virus activities. Antimicrob. Agents Chemother. 2001, 45:743-748.
47. Smith D.B., Kalayanov G., Sund C., Winqvist A., Maltseva T., Leveque V.J.P., Rajyaguru S., Pogam S.L., Najera I., Benkestock K., Zhou X.-X., Kaiser A.C., Maag H., Cammack N., Martin J.A., Swallow S., Johansson N.G., Klumpp K., Smith M. The design, synthesis, and antiviral activity of monofluoro and difluoro analogues of 4'-azidocytidine against hepatitis C virus replication: the discovery of 4'-azido-2'-deoxy-2'-fluorocytidine and 4'-azido-2'-dideoxy-2',2'-difluorocytidine. J. Med. Chem. 2009, 52:2971-2978.
48. Stuyver L.J., McBrayer T.R., Whitaker T., Tharnish P.M., Ramesh M., Lostia S., Cartee L., Shi J., Hobbs A., Schinazi R.F., Watanabe K.A., Otto M.J. Inhibition of the subgenomic hepatitis C virus replicon in huh-7 cells by 2'-deoxy-2'-fluorocytidine. Antimicrob. Agents Chemother. 2004, 48:651-654.
49. Suarez D.L., Perdue M.L., Cox N., Rowe T., Bender C., Huang J., Swayne D.E. Comparisons of highly virulent H5N1 influenza A viruses isolated from humans and chickens from Hong Kong. J. Virol. 1998, 72:6678-6688.
50. Suguitan A.L., McAuliffe J., Mills K.L., Jin H., Duke G., Lu B., Luke C.J., Murphy B., Swayne D.E., Kemble G., Subbarao K. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med. 2006, 3:e360.
51. Thorlund K., Awad T., Boivin G., Thabane L. Systematic review of influenza resistance to the neuraminidase inhibitors. BMC Infect. Dis. 2011, 11:134-146.
52. Tisdale M., Appleyard G., Tuttle J.V., Nelson D.J., Nusinoff-Lehrman S., Al Nakib W., Stables J.N., Purifoy D.J.M., Powell K.L., Darby G. Antiviral Chem. Chemother. 1993, 4:281-287.
53. Tisdale M., Ellis M., Klumpp K., Court S., Ford M. Inhibition of influenza virus transcription by 2'-deoxy-2'-fluoroguanosine. Antimicrob. Agents Chemother. 1995, 39:2454-2458.
54. Trampuz A., Prabhu R.M., Smith T.F., Baddour L.M. Avian influenza: a new pandemic threat?. Mayo Clin. Proc. 2004, 79:523-530.
55. Tuttle J.V., Tisdale M., Krenitsky T.A. Purine 2'-deoxy-2'-fluororibosides as antiinfluenza virus agents. J. Med. Chem. 1993, 36:119-125.
56. Ujike M., Ejima M., Anraku A., Shimabukuro K., Obuchi M., Kishida N., Hong X., Takashita E., Fujisaki S., Yamashita K., Horikawa H., Kato Y., Oguchi A., Fujita N., Tashiro M., Odagiri T. Monitoring and characterization of oseltamivir-resistant pandemic (H1N1) 2009 virus, Japan, 2009-2010. Emerging. Infect. Dis. 2011, 17:470-479.
57. Verity, E.E., Camuglia, S., Agius, C.T., Ong, C., Shaw, R., Barr, I., Middleton, D., Rockman, S., in press. Rapid generation of pandemic influenza virus vaccine candidate strains using synthetic DNA. Influenza Other Respi. Viruses. [Epub ahead of print]. doi:10.1111/j.1750-2659.2011.00273.x.
58. Wohlrab F., Jamieson A.T., Hay J., Mengel R., Guschlbauer W. The effect of 2'-fluoro-2'-deoxycytidine on herpes virus growth. Biochim. Biophys. Acta 1985, 824:233-242.