Competitive fitness of oseltamivir-sensitive and -resistant highly pathogenic H5N1 influenza viruses in a ferret model

Journal of Virology

Volumn 84, Issue 16, 2010, Pages 8042-8050

  Govorkova, Elena A ^a   Ilyushina, Natalia A ^a,b   Marathe, Bindumadhav M ^a   McClaren, Jennifer L ^a   Webster, Robert G ^a,c  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b D I IVANOVSKY INSTITUTE OF VIROLOGY   (Russian Federation)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OSELTAMIVIR; SIALIDASE;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; FERRET; INFLUENZA VIRUS A H5N1; NONHUMAN; PRIORITY JOURNAL; UPPER RESPIRATORY TRACT; VIRUS MUTATION; VIRUS REPLICATION; VIRUS VIRULENCE;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIVIRAL AGENTS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, VIRAL; FERRETS; INFLUENZA A VIRUS, H5N1 SUBTYPE; MALE; MUTATION, MISSENSE; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; OSELTAMIVIR; RECOMBINATION, GENETIC; RESPIRATORY SYSTEM; SURVIVAL ANALYSIS; VIRAL PROTEINS; VIRULENCE; VIRUS REPLICATION;

ANIMALIA; MUSTELA; ORTHOMYXOVIRIDAE;

EID: 77954981636     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00689-10     Document Type: Article

References (49)

1. Abdel-Ghafar, A. N., T. Chotpitayasunondh, Z. Gao, F. G. Hayden, D. H. Nguyen, M. D. de Jong, A. Naghdaliyev, J. S. Peiris, N. Shindo, S. Soeroso, and T. M. Uyeki. 2008. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med. 358:261-273.
2. Abed, Y., N. Goyette, and G. Boivin. 2004. A reverse genetics study of resistance to neuraminidase inhibitors in an influenza A/H1N1 virus. Antivir. Ther. 9:577-581.
3. Abed, Y., M. Baz, and G. Boivin. 2006. Impact of neuraminidase mutations conferring influenza resistance to neuraminidase inhibitors in the N1 and N2 genetic backgrounds. Antivir. Ther. 11:971-976.
4. Beigel, J. H., J. Farrar, A. M. Han, F. G. Hayden, R. Hyer, M. D. de Jong, S. Lochindarat, T. K. Nguyen, T. H. Nguyen, T. H. Tran, A. Nicoll, S. Touch, and K. Y. Yuen. 2005. Avian influenza A (H5N1) infection in humans. N. Engl. J. Med. 353:1374-1385.
5. Bouvier, N. M., A. C. Lowen, and P. Palese. 2008. Oseltamivir-resistant influenza A viruses are transmitted efficiently among guinea pigs by direct contact but not by aerosol. J. Virol. 82:10052-10058.
6. Carr, J., J. Ives, L. Kelly, R. Lambkin, J. Oxford, D. Mendel, L. Tai, and N. Roberts. 2002. Influenza virus carrying neuraminidase with reduced sensitivity to oseltamivir carboxylate has altered properties in vitro and is compromised for infectivity and replicative ability in vivo. Antiviral Res. 54:79-88. (Pubitemid 34327686)
7. Chotpitayasunondh, T., K. Ungchusak, W. Hanshaoworakul, S. Chunsuthiwat, P. Sawanpanyalert, R. Kijphati, S. Lochindarat, P. Srisan, P. Suwan, Y. Osotthanakorn, T. Anantasetagoon, S. Kanjanawasri, S. Tanupattarachai, J. Weerakul, R. Chaiwirattana, M. Maneerattanaporn, R. Poolsavathitikool, K. Chokephaibulkit, A. Apisarnthanarak, and S. F. Dowell. 2005. Human disease from influenza A (H5N1), Thailand, 2004. Emerg. Infect. Dis. 11: 201-209.
8. Collins, P. J., L. F. Haire, Y. P. Lin, J. Liu, R. J. Russell, P. A. Walker, J. J. Skehel, S. R. Martin, A. J. Hay, and S. J. Gamblin. 2008. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453: 1258-1261.
9. de Jong, M. D., T. T. Tran, H. K. Truong, M. H. Vo, G. J. D. Smith, V. C. Nguyen, V. C. Cam, T. Q. Phan, Q. H. Do, Y. Guan, J. S. M. Peiris, T. H. Tran, and J. Farrar. 2005. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N. Engl. J. Med. 353:2667-2672.
10. Deyde, V. M., T. G. Sheu, A. A. Trujillo, M. Okomo-Adhiambo, R. Garten, A. I. Klimov, and L. V. Gubareva. 2010. Detection of molecular markers of antiviral resistance in influenza A (H5N1) viruses using pyrosequencing method. Antimicrob. Agents Chemother. 54:1102-1110.
11. Dharan, N. J., L. V. Gubareva, J. J. Meyer, M. Okomo-Adhiambo, R. C. McClinton, S. A. Marshall, K. St. George, S. Epperson, L. Brammer, A. I. Klimov, J. S. Bresee, and A. M. Fry for the Oseltamivir-Resistance Working Group. 2009. Infections with oseltamivir-resistant influenza A (H1N1) virus in the United States. JAMA 301:1034-1041.
12. Ferraris, O., and B. Lina. 2008. Mutations of neuraminidase implicated in neuraminidase inhibitors resistance. J. Clin. Virol. 41:13-19.
13. Govorkova, E. A., N. A. Ilyushina, D. A. Boltz, A. Douglas, N. Yilmaz, and R. G. Webster. 2007. Efficacy of oseltamivir therapy in ferrets inoculated with different clades of H5N1 influenza virus. Antimicrob. Agents Chemother. 51:1414-1424.
14. Gubareva, L. V., R. G. Webster, and F. G. Hayden. 2002. Detection of influenza virus resistance to neuraminidase inhibitors by an enzyme inhibition assay. Antiviral Res. 53:47-61.
15. Hatakeyama, S., Y. Sakai-Tagawa, M. Kiso, H. Goto, C. Kawakami, K. Mitamura, Y. Sugaya, and Y. Kawaoka. 2005. Enhanced expression of an α2,6-linked sialic acid on MDCK cells improves isolation of human influenza viruses and evaluation of their sensitivity to a neuraminidase inhibitor. J. Clin. Microbiol. 43:4139-4146.
16. Hayden, F. 2009. Developing new antiviral agents for influenza treatment: what does the future hold? Clin. Infect. Dis. 48:S3-S13.
17. Herlocher, M. L., J. Carr, J. Ives, S. Elias, R. Truscon, N. Roberts, and A. S. Monto. 2002. Influenza virus carrying an R292K mutation in the neuraminidase gene is not transmitted in ferrets. Antiviral Res. 54:99-111.
18. Herlocher, M. L., R. Truscon, S. Elias, H. L. Yen, N. A. Roberts, S. E. Ohmit, and A. S. Monto. 2004. Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. J. Infect. Dis. 190:1627-1630.
19. Hoffmann, E., G. Neumann, Y. Kawaoka, G. Hobom, and R. G. Webster. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc. Natl. Acad. Sci. U. S. A. 97:6108-6113.
20. Hoffmann, E., J. Stech, Y. Guan, R. G. Webster, and D. R. Perez. 2001. Universal primer set for the full-length amplification of all influenza A viruses. Arch. Virol. 146:2275-2289.
21. Hurt, A. C., P. Selleck, N. Komadina, R. Shaw, L. Brown, and I. G. Barr. 2007. Susceptibility of highly pathogenic A (H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res. 73:228-231. (Pubitemid 46273119)
22. Hurt, A. C., J. Ernest, Y.-M. Deng, P. Iannello, T. G. Besselaar, C. Birch, P. Buchy, M. Chittaganpitch, S.-C. Chiu, D. Dwyer, A. Guigoni, B. Harrower, I. P. Kei, T. Kok, C. Lin, K. McPhie, A. Mohd, R. Olveda, T. Panayotou, W. Rawlinson, L. Scott, D. Smith, H. D'Souza, N. Komadina, R. Shaw, A. Kelso, and I. G. Barr. 2009. Emergence and spread of oseltamivir-resistant A (H1N1) influenza viruses in Oceania, South East Asia and South Africa. Antiviral Res. 83:90-93.
23. Hurt, A. C., J. K. Holien, M. Parker, A. Kelso, and I. G. Barr. 2009. Zanamivir-resistant influenza viruses with a novel neuraminidase mutation. J. Virol. 83:10366-10373.
24. Ilyushina, N. A., E. A. Govorkova, T. E. Gray, N. V. Bovin, and R. G. Webster. 2008. Human-like receptor specificity does not affect the neuraminidase inhibitor susceptibility of H5N1 influenza viruses. PLoS Pathog. 4:e1000043.
25. Ilyushina, N. A., A. Hay, N. Yilmaz, A. C. Boon, R. G. Webster, and E. A. Govorkova. 2008. Oseltamivir-ribavirin combination therapy for highly pathogenic H5N1 influenza virus infection in mice. Antimicrob. Agents Chemother. 52:3889-3897.
26. Ives, J. A., J. A. Carr, D. B. Mendel, C. Y. Tai, R. Lambkin, L. Kelly, J. S. Oxford, F. G. Hayden, and N. A. Roberts. 2002. The H274Y mutation in the influenza A/H1N1 neuraminidase active site following oseltamivir phosphate treatment leave virus severely compromised both in vitro and in vivo. Antiviral Res. 55:307-317.
27. Jackson, D., W. Barclay, and T. Zurcher. 2005. Characterization of recombinant influenza B viruses with key neuraminidase inhibitor resistance mutations. J. Antimicrob. Chemother. 55:162-169.
28. Kiso, M., K. Mitamura, Y. Sakai-Tagawa, K. Shiraishi, C. Kawakami, K. Kimura, F. G. Hayden, N. Sugaya, and Y. Kawaoka. 2004. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364:759-765. (Pubitemid 39165094)
29. Lackenby, A., O. Hungnes, S. G. Dudman, A. Meijer, W. J. Paget, A. J. Hay, and M. C. Zambon. 2008. Emergence of resistance to oseltamivir among influenza A (H1N1) viruses in Europe. Euro Surveill. 13:1-3.
30. Le, Q. M., M. Kiso, K. Someya, Y. T. Sakai, T. H. Nguyen, K. H. Nguyen, N. D. Pham, H. H. Ngyen, S. Yamada, Y. Muramoto, T. Horimoto, A. Takada, H. Goto, T. Suzuki, Y. Suzuki, and Y. Kawaoka. 2005. Avian flu: isolation of drug-resistant H5N1 virus. Nature 437:1108.
31. Leigh, M. W., R. J. Connor, S. Kelm, L. G. Baum, and J. C. Paulson. 1995. Receptor specificity of influenza virus influences severity of illness in ferrets. Vaccine 13:1468-1473.
32. Lipsitch, M., T. Cohen, M. Murray, and B. R. Levin. 2007. Antiviral resistance and the control of pandemic influenza. PLoS Med. 4:111-121.
33. Maines, T. R., L. M. Chen, Y. Matsuoka, H. Chen, T. Rowe, J. Ortin, A. Falcón, T. H. Nguyen, L. Q. Mai, E. R. Sedyaningsih, S. Harun, T. M. Tumpey, R. O. Donis, N. J. Cox, K. Subbarao, and J. M. Katz. 2006. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc. Natl. Acad. Sci. U. S. A. 103:12121-12126.
34. Matrosovich, M., T. Matrosovich, J. Carr, N. A. Roberts, and H. D. Klenk. 2003. Overexpression of the α-2,6-sialyltransferase in MDCK cells increases influenza sensitivity to neuraminidase inhibitors. J. Virol. 77:8418-8425.
35. McKimm-Breschkin, J. L. 2005. Management of influenza virus infections with neuraminidase inhibitors: detection, incidence, and implications of drug resistance. Treat. Respir. Med. 4(2):107-116.
36. Moscona, A. 2005. Oseltamivir resistance - disabling our influenza defenses. N. Engl. J. Med. 353:2633-2636.
37. Potier, M., L. Mameli, M. Belisle, L. Dallaire, and S. B. Melancon. 1979. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl- α-N-acetylneuraminate) substrate. Anal. Biochem. 94:287-296.
38. Rameix-Welti, M. A., V. Enouf, F. Cuvelier, P. Jeannin, and S. van der Werf. 2008 Enzymatic properties of the neuraminidase of seasonal H1N1 influenza viruses provide insights for the emergence of natural resistance to oseltamivir. PLoS Pathog. 4:e1000103.
39. Reed, L. J., and H. Muench. 1938. A simple method for estimating fifty percent endpoints. Am. J. Hyg. (Lond.) 27:493-497.
40. Reuman, P. D., S. Keely, and G. M. Schiff. 1989. Assessment of signs of influenza illness in the ferret model. J. Virol. Methods 24:27-34.
41. Saad, M. D., B. R. Boynton, K. C. Earhart, M. M. Mansour, H. L. Niman, N. M. Elsayed, A. L. Nayel, A. S. Abdelghani, H. M. Essmat, E. M. Labib, E. A. Ayoub, and M. R. Monteville. 2007. Detection of oseltamivir resistance mutation N294S in humans with influenza A H5N1. Options for the control of influenza VI. International Medical Press, Ltd., Toronto, Canada.
42. Salomon, R., E. Hoffmann, and R. G. Webster. 2007. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc. Natl. Acad. Sci. U. S. A. 104:12479-12481.
43. Smith, B. J., J. L. Kimm-Breshkin, M. McDonald, R. T. Fernley, J. N. Varghese, and P. M. Colman. 2002. Structural studies of the resistance of influenza virus neuraminidase to inhibitors. J. Med. Chem. 45:2207-2212.
44. World Health Organization. 2007. Avian influenza - situation in Egypt - update. World Health Organization, Geneva, Switzerland. http://www.who.int/csr/ don/2007-01-18/en/index.html.
45. World Health Organization. 2010. Update on oseltamivir-resistant pandemic A (H1N1) 2009 influenza virus: January 2010, p. 37-40. In Weekly Epidemiological Record, vol. 85, issue 6. World Health Organization, Geneva, Switzerland. http://www.who.int/wer/2010/wer8506.pdf.
46. Yen, H. L., L. M. Herlocher, E. Hoffmann, M. N. Matrosovich, A. S. Monto, R. G. Webster, and E. A. Govorkova. 2005. Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob. Agents Chemother. 49:4075-4084.
47. Yen, H. L., A. S. Lipatov, N. A. Ilyushina, E. A. Govorkova, J. Franks, N. Yilmaz, A. Douglas, A. Hay, S. Krauss, J. E. Rehg, E. Hoffmann, and R. G. Webster. 2007. Inefficient transmission of H5N1 influenza viruses in a ferret contact model. J. Virol. 81:6890-6898.
48. Yen, H. L., N. A. Ilyushina, R. Salomon, E. Hoffmann, R. G. Webster, and E. A. Govorkova. 2007. Neuraminidase inhibitor-resistant recombinant A/Vietnam/1203/04 (H5N1) influenza viruses retain their replication efficiency and pathogenicity in vitro and in vivo. J. Virol. 81:12418-12426.
49. Zambon, M., and F. G. Hayden. 2001. Position statement: global neuraminidase inhibitor susceptibility network. Antiviral Res. 49:147-156.