Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants

Nature

Volumn 453, Issue 7199, 2008, Pages 1258-1261

  Collins, Patrick J ^a   Haire, Lesley F ^a   Lin, Yi Pu ^a   Liu, Junfeng ^a   Russell, Rupert J ^b   Walker, Philip A ^a   Skehel, John J ^a   Martin, Stephen R ^a   Hay, Alan J ^a   Gamblin, Steven J ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

OSELTAMIVIR; SIALIC ACID; VIRUS SIALIDASE; ZANAMIVIR;

ANTIBIOTIC RESISTANCE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; INFLUENZA; MUTATION; VIRUS;

ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING; DRUG INHIBITION; ENZYME ACTIVITY; HUMAN; HYDROPHOBICITY; INFLUENZA; INFLUENZA VIRUS; PANDEMIC; PRIORITY JOURNAL; X RAY CRYSTALLOGRAPHY;

ORTHOMYXOVIRIDAE;

EID: 46249111790     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature06956     Document Type: Article

References (35)

1. Kim, C. U. et al. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J. Am. Chem. Soc. 119, 681-690 (1997).
2. von Itzstein, M. et al. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363, 418-423 (1993).
3. Varghese, J. N. et al. Drug design against a shifting target: a structural basis for resistance to inhibitors in a variant of influenza virus neuraminidase. Structure 6, 735-746 (1998).
4. McKimm-Breschkin, J. L. Resistance of influenza viruses to neuraminidase inhibitors-a review. Antiviral Res. 47, 1-17 (2000).
5. Gubareva, L. V., Webster, R. G. & Hayden, F. G. Comparison of the activities of zanamivir, oseltamivir, and RWJ-270201 against clinical isolates of influenza virus and neuraminidase inhibitor-resistant variants. Antimicrob. Agents Chemother. 45, 3403-3408 (2001).
6. de Jong, M. D. et al. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N. Engl. J. Med. 353, 2667-2672 (2005).
7. Yen, H. L. et al. 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 (2007).
8. Lackenby, A. et al. Emergence of resistance to oseltamivir among influenza A(H1N1) viruses in Europe. Euro Surveill. 13 (2008).
9. Murphy, B. R. & Webster, R. G. in Fields Virology 3rd edn (eds Fields, D. B. N., Knipe, M. & Howley, P. M.) 1397-1445 (Lippincott-Raven, Philadelphia, 1996).
10. Varghese, J. N., Laver, W. G. & Colman, P. M. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 303, 35-40 (1983).
11. Baker, A. T., Varghese, J. N., Laver, W. G., Air, G. M. & Colman, P. M. Three-dimensional structure of neuraminidase of subtype N9 from an avian influenza virus. Proteins 2, 111-117 (1987).
12. Burmeister, W. P., Henrissat, B., Bosso, C., Cusack, S. & Ruigrok, R. W. Influenza B virus neuraminidase can synthesize its own inhibitor. Structure 1, 19-26 (1993).
13. Ives, J. et al. Anti-viral drug resistance: An oseltamivir treatment-selected influenza A/N2 virus with a R292K mutation in the neuraminidase gene has reduced infectivity in vivo. J. Clin. Virol. 18, 251-269 (2000).
14. Ives, J. A. L. et al. 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 (2002).
15. Herlocher, M. L. et al. Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. J. Infect. Dis. 190, 1627-1630 (2004).
16. Gubareva, L. V., Kaiser, L., Matrosovich, M. N., Soo-Hoo, Y. & Hayden, F. G. Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J. Infect. Dis. 183, 523-531 (2001).
17. Kiso, M. et al. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Lancet 364, 759-765 (2004).
18. Le, Q. M. et al. Avian flu: isolation of drug-resistant H5N1 virus. Nature 437, 1108 (2005).
19. McKimm-Breschkin, J. L., Selleck, P. W., Usman, T. B. & Johnson, M. A. Reduced sensitivity of influenza A to oseltamivir. Emerg. Infect. Dis. 13, 1354-1357 (2007).
20. Rameix-Welti, M. A. et al. Natural variation can significantly alter the sensitivity of influenza A (H5N1) viruses to oseltamivir. Antimicrob. Agents Chemother. 50, 3809-3815 (2006).
21. Wang, M. Z., Tai, C. Y. & Mendel, D. B. Mechanism by which mutations at His274 alter sensitivity of influenza a virus N1 neuraminidase to oseltamivir carboxylate and zanamivir. Antimicrob. Agents Chemother. 46, 3809-3816 (2002).
22. Yen, H. L. et al. Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob. Agents Chemother. 49, 4075-4084 (2005).
23. Smith, B. J. et al. Structural studies of the resistance of influenza virus neuramindase to inhibitors. J. Med. Chem. 45, 2207-2212 (2002).
24. Varghese, J. N., McKimm-Breschkin, J. L., Caldwell, J. B., Kortt, A. A. & Colman, P. M. The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor. Proteins 14, 327-332 (1992).
25. Russell, R. J. et al. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature 443, 45-49 (2006).
26. Cheung, C. L. et al. Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J. Infect. Dis. 193, 1626-1629 (2006).
27. Gulick, R. M. et al. Treatment with indinavir, zidovudine, and lamivudine in adults with human immunodeficiency virus infection and prior antiretroviral therapy. N. Engl. J. Med. 337, 734-739 (1997).
28. De Clercq, E. The design of drugs for HIV and HCV. Nature Rev. Drug Discov. 6, 1001-1018 (2007).
29. Ha, Y., Stevens, D. J., Skehel, J. J. & Wiley, D. C. X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc. Natl Acad. Sci. USA 98, 11181-11186 (2001).
30. Tai, C. Y. et al. Characterization of human influenza virus variants selected in vitro in the presence of the neuraminidase inhibitor GS 4071. Antimicrob. Agents Chemother. 42, 3234-3241 (1998).
31. Otwinowski, Z. & Minor, W. in Data Collection and Processing (eds Sawyer, L., Isaacs, N. & Bailey, S.) 556-562 (SERC Daresbury Laboratory, Warrington, 1993).
32. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760-763 (1994).
33. Adams, P. D. et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D 58, 1948-1954 (2002).
34. Jones, T. A., Zhou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119 (1991).
35. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).