Mutations in a conserved residue in the influenza virus neuraminidase active site decreases sensitivity to Neu5Ac2en-derived inhibitors

Journal of Virology

Volumn 72, Issue 3, 1998, Pages 2456-2462

  McKimm Breschkin, Jennifer L ^a   Sahasrabudhe, Anjali ^a   Blick, Tony J ^a   McDonald, Mandy ^a   Colman, Peter M ^a   Hart, Graham J ^b   Bethell, Richard C ^b   Varghese, Joseph N ^a  

^a CSIRO   (Australia)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; SIALIDASE INHIBITOR; VIRUS HEMAGGLUTININ; VIRUS SIALIDASE; ZANAMIVIR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME SUBSTRATE COMPLEX; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; VIRUS ADSORPTION; VIRUS MUTATION; VIRUS REPLICATION;

EID: 0031911783     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.3.2456-2462.1998     Document Type: Article

References (27)

1. Blick, T. J., T. Tiong, A. Sahasrabudhe, J. N. Varghese, P. N. Colman, G. J. Hart, R. C. Bethell, and J. L. McKimm-Breschkin. 1995. Generation and characterization of an influenza virus neuraminidase variant with decreased sensitivity to the neuraminidase-specific inhibitor 4-guanidino-Neu5Ac2en. Virology 214:475-484.
2. Colman, P. M., P. A. Hoyne, and M. C. Lawrence. 1993. Sequence and structure alignment of paramyxovirus hemagglutinin-neuraminidase with influenza virus neuraminidase. J. Virol. 67:2972-2980.
3. Gubareva, L. V., R. Bethell, G. J. Hart, K. G. Murti, C. H. Penn, and R. G. Webster. 1996. Characterization of mutants of influenza A virus selected with the neuraminidase inhibitor 4-guanidino-Neu5Ac2en. J. Virol. 70:1818-1827.
4. Gubareva, L. V., M. J. Robinson, R. C. Bethell, and R. G. Webster. 1997. Catalytic and framework mutations in the neuraminidase active site of influenza viruses that are resistant to 4-guanidino-Neu5Ac2en. J. Virol. 71: 3385-3390.
5. Gubareva, L. V., M. K. Brenner, and R. G. Webster. 1997. Molecular characterization of influenza B virus from a patient after treatment with a neuraminidase targeted antiviral, abstr. W6-9. In Abstracts of the 16th Annual Meeting of the American Society of Virology.
6. Hart, G. J., and R. C. Bethell. 1995. 2,3-Didehydro-2,4-dideoxy-4-guanidino-N-acetyl-D-neuraminic acid (4-guanidino-Neu5Ac2en) is a slow binding inhibitor of sialidase from both influenza A virus and influenza B virus. Biochem. Mol. Biol. Int. 36:695-703.
7. Hayden, F. G., J. J. Treanor, R. F. Betts, M. Lobo, J. D. Eisenhart, and E. K. Hussey. 1996. Safety and efficacy of the neuraminidase inhibitor GG167 in experimental human influenza. JAMA 275:295-299.
8. Kim, C. U., W. Lew, M. A. Williams, H. Liu, L. Zhang, S. Swaminathan, N. Bischofberger, M. S. Chen, D. B. Mendel, C. Y. Tain, W. G. Laver, and R. C. Stevens. 1997. 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.
9. Lee, W.-X., P. A. Escarpe, M. S. Chen, W. Lew, M. Williams, L. Zhang, C. U. Kim, N. Bischofberger, K. C. Cundy, E. J. Eisenberg, and D. B. Mendel. 1997. Gs4104 is a highly bioavailable prodrug of the novel potent influenza neuraminidase inhibitor GS 4071, p. A74. In Abstracts of the 10th International Conference on Antiviral Research, 1997.
10. McKimm Breschkin, J. L., J. Caldwell, R. E. Guthrie, and A. A. Kortt. 1991. A new method for the purification of the influenza A virus neuraminidase. J. Virol. Methods 32:121-124.
11. McKimm-Breschkin, J. L., T. J. Blick, A. V. Sahasrabudhe, T. Tiong, D. Marshall, G. J. Hart, R. C. Bethell, and C. R. Penn. 1996. Generation and characterization of variants of the NWS/G70C influenza virus after in vitro passage in 4-amino-Neu5Ac2en and 4-guanidino-Neu5Ac2en. Antimicrob. Agents Chemother. 40:40-46.
12. McKimm-Breschkin, J. L., M. McDonald, T. J. Blick, and P. M. Colman. 1996. Mutation in the influenza virus neuraminidase gene resulting in decreased sensitivity to the neuraminidase inhibitor 4-guanidino-Neu5Ac2en leads to instability of the enzyme. Virology 225:240-242.
13. Meindl, P., and H. Tuppy. 1969. 2-Deoxy-2,3-dehydrosialic acids. I. Synthesis and properties of 2-deoxy-2,3-dehydro-N-acylneuraminic acids and their methyl esters. Monatsh. Chem. 100:1295-1306.
14. Morrison, J. F., and C. T. Walsh. 1988. The behaviour and significance of slow binding enzyme inhibitors. Adv. Enzymol. Relat. Areas Mol. Biol. 61:201-301.
15. Nobusawa, E., T. Aoyama, H. Kato, Y. Suzuki, Y. Tateno, and K. Nakajima. 1991. Comparison of complete amino acid sequences and receptor binding properties among 13 serotypes of hemagglutinins of influenza virus. Virology 182:475-485.
16. Palese, P., and R. W. Compans. 1976. Inhibition of influenza virus replication in tissue culture by 2-deoxy-2,3-dehydro-N-trifluoroacetylneuraminic acid (FANA): mechanism of action. J. Gen. Virol. 33:159-163.
17. Palese, P., and J. L. Schulman. 1977. Inhibitors of viral neuraminidase as potential antiviral drugs, p. 189-205. In J. S. Oxford (ed.), Chemoprophylaxis and viral infections of the respiratory tract. CRC Press, Inc., Cleveland, Ohio.
18. Potier, M., L. Mameli, M. Belislem, L. Dallaire, and S. B. Melanxon. 1979. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-a-D-N-acetylneuraminate) substrate. Anal. Biochem. 94:287-296.
19. Sahasrabudhe, A., T. Blick, and J. L. McKimm-Breschkin. 1996. Influenza virus variants resistant to GG167 with mutations in the haemagglutinin, p. 748-757. In L. E. Brown, A. W. Hamspon, and R. G. Webster (ed.), Options for the control of influenza III. Excerpta Medica. Elsevier Biomedical Press, Amsterdam, The Netherlands.
20. Smith, P. W., S. L. Sollis, P. D. Howes, P. C. Cherry, K. N. Cobley, H. Taylor, A. R. Whittington, J. Scicinski, R. C. Bethell, N. Taylor, T. Skarzynski, A. Cleasby, O. Singh, A. Wonacott, J. Varghese, and P. Colman. 1996. Novel inhibitors of influenza sialidases related to GG167. Structure-activity, crystallographic and molecular dynamics studies with 4H-pyran-2-carboxylic acid 6-carboxamides. Bioorg. Med. Chem. Lett. 6:2931-2936.
21. Sollis, S., P. W. Smith, P. D. Howes, P. C. Cherry, and R. C. Bethell. 1996. Novel inhibitors of influenza sialidase related to GG167. Synthesis of 4-amino and guanidino-4H-pyran-2-carboxylic acid-6-propylamides: selective inhibitors of influenza virus sialidase. Bioorg. Med. Chem. Lett. 6:1805-1808.
22. Staschke, K. A., J. M. Colacino, A. J. Baxter, G. M. Air, A. Bansal, W. J. Hornback, J. E. Munroe, and W. G. Laver. 1995. Molecular basis for resistance of influenza viruses to 4-guanidino-Neu5Ac2en. Virology 214:642-646.
23. Varghese, J. N., J. L. McKimm-Breschkin, J. B. Caldwell, A. A. Kortt, and P. M. Colman. 1992. The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor. Proteins 14:327-332.
24. Varghese, J. N., P. M. Colman, P. W. Smith, S. L. Sollis, T. J. Blick, A. Sahasrabudhe, and J. L. McKimm-Breschkin. A structural basis for resistance to potent neuraminidase inhibitors in a variant of influenza virus neuraminidase. Submitted for publication.
25. von Itzstein, M., W. Y. Wu, G. B. Kok, M. S. Pegg, J. C. Dyason, B. Jin, T. V. Phan, M. L. Smythe, H. F. White, S. W. Oliver, P. M. Colman, J. N. Varghese, D. M. Ryan, J. M. Woods, R. C. Bethell, V. J. Hotham, J. M. Cameron, and C. R. Penn. 1993. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature (London) 363:418-423.
26. Ward, C. W., and T. A. Dopheide. 1980. The Hong Kong (H3) hemagglutinin. Complete amino acid sequence and oligosaccharide distribution for the heavy chain of A/Memphis/102/72, p. 27-38. In G. W. Laver and G. Air (ed.), Structure and variation in influenza virus. Elsevier/North-Holland Publishing Co., New York, N.Y.
27. Woods, J. M., R. C. Bethell, J. A. V. Coates, N. Healy, S. A. Hiscox, B. A. Pearson, M. Ryan, J. Ticehurst, J. Tilling, S. M. Walcott, and C. R. Penn. 1993. 4-Guanidino-2,4-dideoxy-2,3-dehydro-N-acetylneuraminic acid is a highly effective inhibitor both of the sialidase (neuraminidase) and of growth of a wide range of influenza A and B viruses in vitro. Antimicrob. Agents Chemother. 37:1473-1479.