Influenza neuraminidase operates via a nucleophilic mechanism and can be targeted by covalent inhibitors

Nature Communications

Volumn 4, Issue , 2013, Pages

  Vavricka, Christopher J ^a,b   Liu, Yue ^b   Kiyota, Hiromasa ^c   Sriwilaijaroen, Nongluk ^d,e   Qi, Jianxun ^b   Tanaka, Kosuke ^c   Wu, Yan ^b   Li, Qing ^b,f   Li, Yan ^b   Yan, Jinghua ^b   Suzuki, Yasuo ^e   Gao, George F ^a,b,f,g  

^a Research Network of Immunity and Health (RNIH)   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

^c TOHOKU UNIVERSITY   (Japan)

^d THAMMASAT UNIVERSITY   (Thailand)

^e CHUBU UNIVERSITY   (Japan)

^f UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^g CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

[No Author keywords available]

Indexed keywords

N ACETYL 2,3 DIDEHYDRO 2 DEOXYNEURAMINIC ACID; NUCLEOPHILE; SIALIDASE INHIBITOR; TYROSINE; UNCLASSIFIED DRUG; VIRUS SIALIDASE;

CATALYSIS; CRYSTALLOGRAPHY; DRUG DEVELOPMENT; ENZYME ACTIVITY; INFLUENZA; INHIBITOR;

ANTIVIRAL ACTIVITY; ARTICLE; CATALYSIS; CONTROLLED STUDY; COVALENT BOND; CRYSTALLOGRAPHY; ENZYME INHIBITION; INFLUENZA VIRUS A; INFLUENZA VIRUS B; NONHUMAN; NUCLEOPHILICITY;

ANIMALS; ANTIVIRAL AGENTS; BIOCATALYSIS; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, VIRAL; ENZYME INHIBITORS; FLUORESCENCE; HUMANS; KINETICS; MADIN DARBY CANINE KIDNEY CELLS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTANT PROTEINS; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; ORTHOMYXOVIRIDAE; OSELTAMIVIR; TYROSINE; VIRUS REPLICATION; ZANAMIVIR;

EID: 84874604902     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2487     Document Type: Article

References (52)

1. Imai, M. et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486, 420-428 (2012)
2. Herfst, S. et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336, 1534-1541 (2012)
3. Guan, Y. et al. The emergence of pandemic influenza viruses. Protein Cell 1, 9-13 (2010)
4. Gao, G. F. & Sun, Y. It is not just AIV: from avian to swine-origin influenza virus. Sci. China Life Sci. 53, 151-153 (2010)
5. Jagger, B. W. et al. An overlapping protein-coding region in influenza A virus segment 3 modulates the host response. Science 337, 199-204 (2012)
6. Vavricka, C. J. et al. Special features of the 2009 pandemic swine-origin influenza A H1N1 hemagglutinin and neuraminidase. Chin. Sci. Bull. 56, 1747-1752 (2011)
7. Sun, Y. et al. In silico characterization of the functional and structural modules of the hemagglutinin protein from the swine-origin influenza virus A (H1N1)-2009. Sci. China Life Sci. 53, 633-642 (2010)
8. von Itzstein, M. Influenza Virus Sialidase-A Drug Discovery Target (Springer, Basel, 2012)
9. Centers for Disease Control and Prevention. Influenza activity-United States and worldwide, 2007-08 season. Morb. Mortal. Wkly. Rep. 58, 115-119 (2009)
10. von Itzstein, M. et al. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363, 418-423 (1993) (Pubitemid 23179386)
11. 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 antiinfluenza activity. J. Am. Chem. Soc. 119, 681-690 (1997) (Pubitemid 27101232)
12. Yamashita, M. et al. CS-8958, a prodrug of the new neuraminidase inhibitor R-125489, shows long-acting anti-influenza virus activity. Antimicrob. Agents Chemother. 53, 186-192 (2009)
13. Chong, A. K., Pegg, M. S., Taylor, N. R. & von Itzstein, M. Evidence for a sialosyl cation transition-state complex in the reaction of sialidase from influenza virus. Eur. J. Biochem. 207, 335-343 (1992)
14. Taylor, N. R. & von Itzstein, M. Molecular modeling studies on ligand binding to sialidase from influenza virus and the mechanism of catalysis. J. Med. Chem. 37, 616-624 (1994) (Pubitemid 24102181)
15. Rye, C. S. & Withers, S. G. Glycosidase mechanisms. Curr. Opin. Chem. Biol. 4, 573-580 (2000)
16. Guo, X., Laver, W. G., Vimir, E. & Sinnott, M. L. Catalysis by two sialidases with the same protein fold but different stereochemical courses: a mechanistic comparison of the enzymes from influenza A virus and Salmonella typhimurium. J. Am. Chem. Soc 116, 5572-5578 (1994)
17. Watson, J. N., Dookhun, V., Borgford, T. J. & Bennet, A. J. Mutagenesis of the conserved active-site tyrosine changes a retaining sialidase into an inverting sialidase. Biochemistry 42, 12682-12690 (2003) (Pubitemid 37337560)
18. Watts, A. G., Oppezzo, P., Withers, S. G., Alzari, P. M. & Buschiazzo, A. Structural and kinetic analysis of two covalent sialosyl-enzyme intermediates on Trypanosoma rangeli sialidase. J. Biol. Chem. 281, 4149-4155 (2006) (Pubitemid 43847842)
19. Chan, J. et al. Bacterial and viral sialidases: contribution of the conserved active site glutamate to catalysis. Biochemistry 51, 433-441 (2012)
20. Chou, D. T. H., Watson, J. N., Scholte, A. A., Borgford, T. J. & Bennet, A. J. Effect of neutral pyridine leaving groups on the mechanisms of influenza type A viral sialidase-catalyzed and spontaneous hydrolysis reactions of a-D-Nacetylneuraminides. J. Am. Chem. Soc. 122, 8357-8364 (2000)
21. Burmeister, W. P., Henrissat, B., Bosso, C., Cusack, S. & Ruigrok, R. W. H. Influenza B virus neuraminidase can synthesize its own inhibitor. Structure 1, 19-26 (1993)
22. Ghate, A. A. & Air, G. M. Site-directed mutagenesis of catalytic residues of influenza virus neuraminidase as an aid to drug design. Europ. J. Biochem. 258, 320-331 (1998) (Pubitemid 28557895)
23. Thomas, A., Jourand, D., Bret, C., Amara, P. & Field, M. J. Is there a covalent intermediate in the viral neuraminidase reaction? A hybrid potential freeenergy study. J. Am. Chem. Soc. 121, 9693-9702 (1999)
24. Xu, G. G. et al. Three Streptococcus pneumoniae sialidases: three different products. J. Am. Chem. Soc. 133, 1718-1721 (2011)
25. Lentz, M. R., Webster, R. G. & Air, G. M. Site-directed mutation of the activesite of influenza neuraminidase and implications for the catalytic mechanism. Biochemistry 26, 5351-5358 (1987)
26. Watts, A. G. & Withers, S. G. The synthesis of some mechanistic probes for sialic acid processing enzymes and the labeling of a sialidase from Trypanosoma rangeli. Can. J. Chem. 82, 1581-1588 (2004) (Pubitemid 40333285)
27. Nakajima, T., Hori, H., Ohrui, H., Meguro, H. & Ido, T. Synthesis of N-acetyl-3-fluoro-neuraminic acids. Agr. Biol. Chem. Tokyo 52, 1209-1215 (1988)
28. Tsuchiya, T. Chemistry and developments of fluorinated carbohydrates. Adv. Carbohydr. Chem. Biochem. 48, 91-277 (1990)
29. Hagiwara, T., Kijimasuda, I., Ido, T., Ohrui, H. & Tomita, K. Inhibition of bacterial and viral sialidases by 3-fluoro-N-acetylneuraminic acid. Carbohydr. Res. 263, 167-172 (1994) (Pubitemid 24297423)
30. Ikeda, K. et al. 2b, 3b-difluorosialic acid derivatives structurally modified at the C-4 position: synthesis and biological evaluation as inhibitors of human parainfluenza virus type 1. Carbohydr. Res. 339, 1367-1372 (2004) (Pubitemid 38542961)
31. Swaminathan, K. & Downard, K. M. Anti-viral binding to influenza neuraminidase byMALDI mass spectrometry. Anal. Chem. 84, 3725-3730 (2012)
32. Collins, P. J. et al. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature 453, 1258-1261 (2008) (Pubitemid 351913590)
33. 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) (Pubitemid 28301207)
34. Singh, J., Petter, R. C., Baillie, T. A. & Whitty, A. The resurgence of covalent drugs. Nat. Chem. Biol. 10, 307-317 (2011)
35. Amaro, R. E., Cheng, X., Ivanov, I., Xu, D. & McCammon, J. A. Characterizing loop dynamics and ligand recognition in human-and avian-type influenza neuraminidases via generalized born molecular dynamics and end-point free energy calculations. J. Am. Chem. Soc. 131, 4702-4709 (2009)
36. Hatakeyama, S. et al. Enhanced expression of an a2, 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 (2005) (Pubitemid 41129710)
37. Sriwilaijaroen, N. et al. Mechanisms of the action of povidone-iodine against human and avian influenza A viruses: its effects on hemagglutination and sialidase activities. Virol. J. 6, 124 (2009)
38. Xu, X., Zhu, X., Dwek, R. A., Stevens, J. & Wilson, I. A. Structural characterization of the 1918 influenza virus H1N1 neuraminidase. J. Virol. 82, 10493-10501 (2008) (Pubitemid 352691147)
39. Zhang, W. et al. Crystal structure of the swine-origin A (H1N1)-2009 influenza A virus hemagglutinin (HA) reveals similar antigenicity to that of the 1918 pandemic virus. Protein Cell 1, 459-467 (2010)
40. Li, Q. et al. The 2009 pandemic H1N1 neuraminidase N1 lacks the 150-cavity in its active site. Nat. Struct. Mol. Biol. 17, 1266-1268 (2010)
41. Vavricka, C. J. et al. Structural and functional analysis of laninamivir and its octanoate prodrug reveals group specific mechanisms for influenza NA inhibition. PLoS Pathog. 7, e1002249 (2011)
42. Potier, M., Mameli, L., Belisle, M., Dallaire, L. & Melancon, S. B. Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-a-D- Nacetylneuraminate) substrate. Anal. Biochem. 94, 287-296 (1979) (Pubitemid 9173017)
43. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Method. Enzymol. 276, 307-326 (1997) (Pubitemid 27085611)
44. Read, R. J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57, 1373-1382 (2001) (Pubitemid 36117185)
45. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994)
46. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997) (Pubitemid 27235885)
47. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004) (Pubitemid 41742764)
48. Adams, P. D. et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010)
49. Laskowski, R. A., Macarthur, M. W., Moss, D. S. & Thornton, J. M. Procheck -a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291 (1993)
50. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63 (1983) (Pubitemid 14203433)
51. Sriwilaijaroen, N. et al. Antiviral effects of Psidium guajava Linn. (guava) tea on the growth of clinical isolated H1N1 viruses: Its role in viral hemagglutination and neuraminidase inhibition. Antivir. Res. 94, 139-146 (2012)
52. Hayden, F. G., Cote, K. M. & Douglas, Jr. R. G. Plaque inhibition assay for drug susceptibility testing of influenza viruses. Antimicrob. Agents Chemother. 17, 865-870 (1980). (Pubitemid 10112539)