The structures of Salmonella typhimurium LT2 neuraminidase and its complexes with three inhibitors at high resolution

Journal of Molecular Biology

Volumn 259, Issue 2, 1996, Pages 264-280

  Crennell, Susan J ^a   Garman, Elspeth F ^b   Philippon, Cedric ^c   Vasella, Andrea ^c   Laver, W Graeme ^d   Vimr, Eric R ^e   Taylor, Garry L ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ETH ZURICH   (Switzerland)

^d Biology and Environment   (Australia)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Inhibitor complexes; Neuraminidase; Salmonella typhimurium; Sialic acid derivatives

Indexed keywords

3 DEOXY 2,3 DEHYDRO N ACETYL NEURAMINIC ACID; ARGININE; ASPARTIC ACID; GLUTAMIC ACID; N ACETYLNEURAMINIC ACID; OXYGEN; PHOSPHONIC ACID DERIVATIVE; POTASSIUM ION; SIALIDASE; SIALIDASE INHIBITOR; SOLVENT; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME STRUCTURE; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM;

BACTERIA (MICROORGANISMS); INFLUENZA VIRUS; SALMONELLA TYPHIMURIUM; TYPHIMURIUM;

EID: 0029937503     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0318     Document Type: Article

References (56)

1. Ada, G. L. French, E. L. & Lind, P. E. (1961). Purification and properties of neuraminidase from Vibrio cholerae. J. Gen. Microbiol. 24, 409-421.
2. Angus, D. I. & von Itzstein, M. (1995). Towards the synthesis of sialic acid-based Salmonella typhimurium sialidase inhibitors. Carbohydrate Res. 274, 279-283.
3. Aymard-Henry, M., Coleman, M. T., Dowdle, W. R., Laver, W. G., Schild, G. C. & Webster, R. G. (1973). Influenza virus neuraminidase and neuraminidase-inhibition test procedures. Bull. World Health Organisat. 48, 199-202.
4. Blick, T. J., Tiong, T., Sahasrabudhe, A., Varghese, J. N., Colman, P. M., Hart, G. J., Bethell, R. C. & McKimm-Breschkin, J. L. (1995). Generation and characterisation of an influenza virus neuraminidase variant with decreased sensitivity to the neuraminidase-specific inhibitor 4-guanidino-Neu5Ac2en. Virology, 214, 475-484.
5. Bossart-Whitaker, P., Carson, M., Babu, Y. S., Smith, C. D., Laver, W. G. & Air, G. M. (1993). Three-dimensional structure of influenza A N9 neuraminidase and its complex with the inhibitor 2-deoxy 2,3-dehydro-N-acetyl neuraminic acid. J. Mol. Biol. 232, 1069-1083.
6. Brünger, A. T. (1988). Crystallographic refinement by simulated annealing: application to a 2.8 Å resolution structure of aspartate aminotransferase. J. Mol. Biol. 203, 803-816.
7. Burmeister, W. P., Ruigrok, R. W. H. & Cusack, S. (1992). The 2.2 Å resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. EMBO J. 11, 49-56.
8. Burmeister, W. P., Henrissat, B., Bosso, C., Cusack, S. & Ruigrok, R. W. H. (1993). Influenza B virus neuraminidase can synthesize its own inhibitor. Structure, 1, 19-26.
9. Burmeister, W. P., Cusack, S. & Ruigrok, R. W. H. (1994). Calcium is needed for the thermostability of influenza B virus neuraminidase. J. Gen. Virol. 75, 381-388.
10. (1979). The SERC (U.K.) Collaborative Computing Project no. 4: a suite of programs for protein crystallography. Daresbury Lab., Warrington, UK.
11. Chong, A. K. J., Pegg, M. S. & von Itzstein, M. (1991). Influenza virus sialidase: effect of calcium on steady-state kinetic parameters. Biochim. Biophys. Acta, 1077, 65-71.
12. Chong, A. K. J., Pegg, M. S., Taylor, N. R. & von Itzstein, M. (1992). Evidence for a sialosyl cation transition-state complex in the reaction of sialidase from influenza virus. Eur. J. Biochem. 207, 335-343.
13. Colman, P. M. (1989). Neuraminidase: enzyme and antigen. In The Influenza Viruses (Klug, R. M., ed.), pp. 175-218. Plenum Publishing Corporation, New York.
14. Colman, P. M. (1994). Influenza virus neuraminidase: structure, antibodies and inhibitors. Protein Sci. 3, 1687-1696.
15. Corfield, A. P., Higa, H., Paulson, J. C. & Schauer, R. (1983). The specificity of viral and bacterial sialidases for α(2 → 3) and α(2 → 6)-linked sialic acids in glycoproteins. Biochim. Biophys. Acta, 744, 121-126.
16. Corfield, A. P., Hoskins, L. C., Wagner, S. A. & Clamp, J. R. (1990). Production of sialic acid metabolising enzymes by strains of human fecal bacteria. Gastroenterology, 98, A443.
17. Corfield, A. P., Lambre, C. R., Michalski, J.-C. & Schauer, R. (1992). Role of sialidases and sialic acids in molecular recognition phenomena. In Conferences Philippe Laudat 1991 pp. 113-134, Institut National de la Sante et de la Recherche Medicale, INSERM, Paris.
18. Crennell, S. J., Garman, E. F., Laver, W. G., Vimr, E. R. & Taylor, G. L. (1993). Crystal structure of a bacterial sialidase (from Salmonella typhimurium LT2) shows the same fold as an influenza virus neuraminidase. Proc. Natl Acad. Sci. USA, 90, 9852-9856.
19. Crennell, S. J., Garman, E. F., Laver, W. G., Vimr, E. R. & Taylor, G. L. (1994). Crystal structure of Vibro cholerae neuraminidase reveals dual lectin-like domains in addition to the catalytic domain. Structure, 2, 535-544.
20. Ferrari, J., Harris, R. & Warner, T. G. (1994). Cloning and expression of a soluble sialidase from Chinese hamster ovary cells: sequence alignment similarities to bacterial sialidases. Glycobiology, 4, 367-373.
21. Galen, J. E., Ketley, J. M., Fansano, A., Richardson, S. H., Wasserman, S. S. & Kaper, J. B. (1992). Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect. Immun. 60, 406-415.
22. Gaskell, A., Crennell, S. J. & Taylor, G. L. (1995). The three domains of a bacterial sialidase: a β-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure, 3, 1197-1205.
23. Guo, X. & Sinnott, M. L. (1993a). A kinetic-isotope effect study of catalysis by Vibrio cholerae neuraminidase. Biochem. J. 294, 653-656.
24. Guo, X. & Sinnott, M. L. (1993b). Salmonella typhimurium neuraminidase acts with inversion of configuration. Biochem. J. 296, 291-292.
25. Guo, X., Laver, W. G., Vimr, E. R. & Sinnott, M. L. (1994). 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.
26. Holzer, C. T., von Itzstein, M., Jin, B., Pegg, M. S., Stewart, W. P. & Wu, W.-Y. (1993). Inhibition of sialidases from viral, bacterial and mammalian sources by analogues of 2-deoxy-2,3-didehydro-N-acetylneuraminic acid modified at the C-4 position. Glycoconjugate J. 10, 40-44.
27. Hoyer, L. L., Roggentin, P., Schauer, R. & Vimr, E. R. (1991). Purification and properties of cloned Salmonella typhimurium LT2 sialidase with virus-typical kinetic preference for sialyl α2 → 3 linkages. J. Biochem. 110, 462-467.
28. Hoyer, L. L., Hamilton, A.C., Steenbergen, S. M. & Vimr, E. R. (1992). Cloning, sequencing and distribution of Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol. Microbiol. 6, 873-884.
29. Janakiraman, M. N., White, C. C., Laver, W. G., Air, G. M & Luo, M. (1984). Structure of influenza virus neuraminidase B/Lee/40 complexed with sialic acid and a dehydro-analog at 1.8 Å resolution: implications for the catalytic mechanism. Biochemistry, 33, 8172-8179.
30. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
31. Kabsch, W. J. (1993). Automatic processing of rotation diffraction data from crystals of initially unknown cell constants. J. Appl. Crystallog. 26, 795-800.
32. Kabsch, W. J. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
33. Luzatti, P. V. (1952). Traitement statistique des erreurs dans la determination des structures cristallines. Acta Crystallog. sect. A, 5, 802-810.
34. Meindl, P., Bodo, G., Palese, P., Schulman, J. & Tuppy, H. (1974). Inhibition of neuraminidase activity by derivatives of 2-deoxy-2,3-dehydro-N-acetylneuraminic acid. Virology, 58, 457-463.
35. Otwinowski, Z. (1993). Oscillation data reduction program. In Data Collection and Processing, Proceedings of CCP4 Study Weekend (Sawyer, L., Isaacs, N. & Bailey, S., eds), pp. 56-62, S.E.R.C. Daresbury Laboratory U.K.
36. Pereira, M. E. A., Meija, J. S., Ortega-Barria, E., Matzitevich, D. & Prioli, R. P. (1991). The Trypanosoma cruzi neuraminidase contains sequences similar to bacterial neuraminidases, YWTD repeats of the low density lipoprotein receptor and type III modules of fibronectin. J. Exp. Med. 174, 179-191.
37. Poppe, L., Stuike-Prill, R., Meyer, B. & van Halbeek, H. (1992). The solution conformation of sialyl-α(2 → 6)-lactose studied by modern NMR techniques and Monte Carlo simulations. J. Biomolecular NMR, 2, 109-136.
38. Quanta 3.0 Parameter Handbook. (1990). Polygen Corporation USA.
39. Roggentin, P., Rothe, B., Kaper, J. B., Galen, J., Lawrisuk, L., Vimr, E. R. & Schauer, R. (1989). Conserved sequences in bacterial and viral sialidases. Glycoconj. J. 6, 349-353.
40. Roggentin, P., Schauer, R., Hoyer, L. L. & Vimr, E. R. (1993). The sialidase superfamily and its spread by horizontal gene transfer. Mol. Microbiol. 9, 915-921.
41. Staschke, K. A., Colacino, J. M., Baxter, A. J., Air, G. M., Bansal, A., Hornbeck, W. J., Munroe, J. E. & Laver, W. G. (1995). Molecular basis for the resistance of influenza viruses to 4-guanidino-Neu5Ac2en. Virology, 214, 642-646.
42. Taylor, G. L., Vimr, E. R., Garman, E. F. & Laver, W. G. (1992). Purification, crystallisation and preliminary crystallographic study of neuraminidase from Vibrio cholerae and Salmonella typhimurium. J. Mol. Biol. 266, 1287-1290.
43. Taylor, N. R. & von Itzstein, M. (1994). Molecular modeling studies on ligand binding to sialidase from influenza virus and the mechanism of catalysis. J. Med. Chem. 37, 616-624.
44. Tripos Associates Inc. (1992). Sybyl Modeling Molecular Software, St. Louis, MO.
45. Tronrud, D. E., Ten Eyck, L. F. & Matthews, B. W. (1987). An efficient general-purpose least-squares refinement program for macromolecular structures. Acta Crystallog. sect. A, 43, 489-501.
46. Tulip, W. R., Varghese, J. N., Baker, A. T., von Donkelaar, A., Laver, W. G., Webster, R. G. & Colman, P. M. (1991). Refined atomic structures of N9 subtype influenza virus neuraminidase and escape mutants. J. Mol. Biol. 221, 487-497.
47. Varghese, J. N. & Colman, P. M. (1991). Three-dimensional structure of the neuraminidase of influenza virus A/Tokyo/3/67 at 2.2 Å resolution. J. Mol. Biol. 221, 473-486.
48. Varghese, J. N., Laver, W. G. & Colman, P. M. (1983). Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature, 303, 35-40.
49. Varghese, J. N., McKimm-Breschkin, J., Caldwell, J. B., Kortt, A. A. & Colman, P. M. (1992). The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor. Proteins: Struct. Funct. Genet. 14, 327-332.
50. Varghese, J. N., Epa, V. C. & Colman, P. M. (1995). Three-dimensional structure of the complex of 4-guanidino-Neu5Ac2en and influenza virus neuraminidase. Protein Sci. 4, 1081-1087.
51. Vimr, E. R., Lawrisuk, L., Galen, J. & Kaper, J. B. (1988). Cloning and expression of the Vibrio cholerae neuraminidase gene nanH in Escherichia coli. J. Bacteriol. 170, 1495-1504.
52. von Itzstein, M., Wu, W.-Y., Kok, G. B., Pegg, M. S., Dyason, J. C., Jin, B., Phan, T. V., Smythe, M. L., White, H. F., Oliver, S. W., Colman, P. M., Varghese, J. N., Ryan, D. M., Woods, J. M., Bethall, R. C., Hotham, V. J., Cameron, J. M. & Penn, C. R. (1993). Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature, 363, 418-423.
53. Walliman, K. & Vasella, A. (1990). Phosphonic acid analogues of the N-acetyl-2-deoxyneuraminic acids: synthesis and inhibition of Vibrio cholerae sialidase. Helvet. Chim. Acta, 73, 1359-1372.
54. Warner, T. G., Harris, R., McDowell, R. & Vimr, E. R. (1992). Photolabeling of Salmonella typhimurium LT2 sialidase: identification of a peptide with a predicted structural similarity to the active sites of influenza sialidase. Biochem. J. 285, 957-964.
55. White, C. L., Janakiraman, M. N., Laver, W. G., Philippon, C., Vasella, A., Air, G. M. & Luo, M. (1995). A sialic acid-derived phosphonate analog inhibits different strains of influenza virus neuraminidase with different efficiencies. J. Mol. Biol. 245, 623-634.
56. 1H NMR evidence that Salmonella typhimurium sialidase hydrolyses sialosides with overall retention of configuration. J. Am. Chem. Soc. 117, 4214-4217.