Mechanistic requirements for the efficient enzyme-catalyzed hydrolysis of thiosialosides

Biochemistry

Volumn 45, Issue 30, 2006, Pages 9319-9326

  Narine, Arun A ^a   Watson, Jacqueline N ^a   Bennet, Andrew J ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSTS; CONFORMATIONS; ENZYMES; HYDROLYSIS; RATE CONSTANTS; SUBSTRATES;

MUTANT; NUCLEOPHILIC TYROSINE; THIOPHENOL; THIOPHENOXIDE;

ORGANIC COMPOUNDS;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DEGLYCOSYLATION; ENZYME MECHANISM; ENZYME SUBSTRATE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; REACTION ANALYSIS; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

BACTERIAL PROTEINS; CATALYSIS; HYDROLYSIS; MICROMONOSPORA; NEURAMINIDASE; SIALIC ACIDS; SUBSTRATE SPECIFICITY;

MICROMONOSPORA VIRIDIFACIENS;

EID: 33746659791     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0607507     Document Type: Article

References (61)

1. Saito, M., and Yu, R. K. (1995) Biochemistry and function of sialidases, in Biology of the Sialic Acids (Rosenberg, A., Ed.) pp 261-313, Plenum Press, New York.
2. Henrissat, B. (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities, Biochem. J. 280, 309-316.
3. Henrissat, B., and Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities, Biochem. J. 293, 781-788.
4. Henrissat, B., and Bairoch, A. (1996) Updating the sequence-based classification of glycosyl hydrolases, Biochem. J. 316, 695-696.
5. Vimr, E. R. (1994) Microbial sialidases: Does bigger always mean better?, Trends Microbiol. 2, 271-277.
6. Koshland, D. E., Jr. (1953) Stereochemistry and the mechanism of enzymic reactions, Biol. Rev. 28, 416-436.
7. 1-NMR-spectroscopic evidence for the release of N-acetyl-α-D- neuraminic acid as the 1st product of neuraminidase action, Biol. Chem. Hoppe-Seyler 361, 697-702.
8. Chong, A. K. J., Pegg, M. S., Taylor, N. R., and von Itzstein, M. (1992) Evidence for a sialosyl cation transition-state complex in the reactivity of sialidase from influenza virus, Eur. J. Biochem. 207, 335-343.
9. 1H NMR evidence that Salmonella typhimurium sialidase hydrolyzes sialosides with overall retention of configuration, J. Am. Chem. Soc. 117, 4214-4217.
10. Davies, G., Sinnott, M. L., and Withers, S. G. (1998) Glycosyl transfer, in Comprehensive Biological Catalysis (Sinnott, M. L., Ed.) pp 119-209, Academic Press, San Diego.
11. Watson, J. N., Dookhun, V., Borgford, T. J., and Bennet, A. J. (2003) Mutagenesis of the conserved active-site tyrosine changes a retaining sialidase into an inverting sialidase, Biochemistry 42, 12682-12690.
12. Watts, A. G., Damager, I., Amaya, M. L., Buschiazzo, A., Alzari, P., Frasch, A. C., and Withers, S. G. (2003) Trypanosoma cruzi trans-sialidase operates through a covalent sialyl-enzyme intermediate: Tyrosine is the catalytic nucleophile, J. Am. Chem. Soc. 125, 7532-7533.
13. Watts, A. G., and Withers, S. G. (2004) 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.
14. Watts, A. G., Oppezzo, P., Withers, S. G., Alzari, P. M., and Buschiazzo, A. (2006) Structural and kinetic analysis of two covalent sialosyl-enzyme intermediates on Trypanosoma rangeli sialidase, J. Biol. Chem. 281, 4149-4155.
15. Newstead, S., Watson, J. N., Knoll, T. L., Bennet, A. J., and Taylor, G. (2005) Structure and mechanism of action of an inverting mutant sialidase, Biochemistry 44, 9117-9122.
16. Watson, J. N., Newstead, S., Narine, A., Taylor, G., and Bennet, A. J. (2005) Two nucleophilic mutants of the Micromonospora viridifaciens sialidase operate with retention of configuration via two different mechanisms, ChemBioChem 6, 1999-2004.
17. Varghese, J. N., and 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.
18. Watson, J. N., Newstead, S., Dookhun, V., Taylor, G., and Bennet, A. J. (2004) Contribution of the active site aspartic acid to catalysis in the bacterial neuraminidase from Micromonospora viridifaciens, FEBS Lett. 577, 265-269.
19. Sakurada, K., Ohta, T., and Hasegawa, M. (1992) Cloning, expression, and characterization of the Micromonospora viridifiaciens neuraminidase gene in Streptomyces lividans, J. Bacteriol. 174, 6896-6903.
20. Albery, W. J., and Knowles, J. R. (1976) Evolution of enzyme function and development of catalytic efficiency, Biochemistry 15, 5631-5640.
21. Watson, J. N., Knoll, T. L., Chen, J. H., Chou, D. T. H., Borgford, T. J., and Bennet, A. J. (2005) Use of conformationally restricted pyridinium α-D-N-acetylneuraminides to probe specificity in bacterial and viral sialidases, Biochem. Cell Biol. 83, 115-122.
22. Gaskell, A., Crennell, S., and Taylor, G. (1995) The three domains of a bacterial sialidase: A β-propeller, an immunoglobulin module and a galactose-binding jellyroll, Structure 3, 1197-1205.
23. Newstead, S. L., Watson, J. N., Bennet, A. J., and Taylor, G. (2005) Galactose recognition by the carbohydrate-binding module of a bacterial sialidase, Acta Crystallogr. D 61, 1483-1491.
24. Sulzenbacher, G., Driguez, H., Henrissat, B., Schulein, M., and Davies, G. J. (1996) Structure of the Fusarium oxysporum endoglucanase I with a nonhydrolyzable substrate analogue: Substrate distortion gives rise to the preferred axial orientation for the leaving group, Biochemistry 35, 15280-15287.
25. Czjzek, M., Cicek, M., Zamboni, V., Burmeister, W. P., Bevan, D. R., Henrissat, B., and Esen, A. (2001) Crystal structure of a monocotyledon (maize ZMGlu1) β-glucosidase and a model of its complex with p-nitrophenyl β-D-thioglucoside, Biochem. J. 354, 37-46.
26. Wilson, J. C., Kiefel, M. J., Angus, D. I., and von Itzstein, M. (1999) Investigation of the stability of thiosialosides toward hydrolysis by sialidases using NMR spectroscopy, Org. Lett. 1, 443-446.
27. Eschenfelder, V., and Brossmer, R. (1987) Synthesis of p-nitrophenyl 5-acetamido-3,5-dideoxy-α-D-glycero-D-galacto-2-nonulopyranosidonic acid, a chromogenic substrate for sialidases, Carbohydr. Res. 162, 294-297.
28. Rothermel, J., and Faillard, H. (1990) Phase-transfer-catalyzed synthesis of aryl α-ketosides of N-acetylneuraminic acid. A 2-methylfluoran-6-yl glycoside of N-acetylneuraminic acid, 2-methyl-6-(5-acetamido-3,5-dideoxy- α-D-glycero-D-galacto-nonulopyranosylonic acid)xanthene-9-spiro-1′- isobenzofuran-3′-one, a new substrate for neuraminidase assay, Carbohydr. Res. 196, 29-40.
29. Sun, X. L., Kanie, Y., Guo, C. T., Kanie, O., Suzuki, Y., and Wong, C. H. (2000) Syntheses of C-3-modified sialylglycosides as selective inhibitors of influenza hemagglutinin and neuraminidase, Eur. J. Org. Chem., 2643-2653.
30. Cao, S. D., Meunier, S. J., Andersson, F. O., Letellier, M., and Roy, R. (1994) Mild stereoselective syntheses of thioglycosides under PTC conditions and their use as active and latent glycosyl donors, Tetrahedron: Asymmetry 5, 2303-2312.
31. Zanini, D., and Roy, R. (1998) Practical synthesis of starburst PAMAM alpha-thiosialodendrimers for probing multivalent carbohydrate-lectin binding properties, J. Org. Chem. 63, 3486-3491.
32. Ellman, G. L., Courtney, K. D., Andres, V. J., and Featherstone, R. M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity, Biochem. Pharmacol. 7, 88-95.
33. Lee, T. S., Massova, I., Kuhn, B., and Kollman, P. A. (2000) QM and QM-E simulations on reactions of relevance to enzyme catalysis: trypsin, catechol O-methyltransferase, β-lactamase and pseudouridine synthase, J. Chem. Soc., Perkin Trans. 2, 409-415.
34. Roy, R., and Laferriere, C. A. (1990) Synthesis of protein conjugates and analogues of N-acetylneuraminic acid, Can. J. Chem. 68, 2045-2054.
35. Groves, D. R., Bradley, S. J., Rose, F. J., Kiefel, M. J., and von Itzstein, M. (1999) How pure is your thiosialoside? A reinvestigation into the HPLC purification of thioglycosides of N-acetylneuraminic acid, Glycoconjugate J. 16, 13-17.
36. Dalby, K. N., and Jencks, W. P. (1997) General acid catalysis of the reversible addition of thiolate anions to cyanamide, J. Chem. Soc., Perkin Trans. 2, 1555-1563.
37. Zhou, Y., Guo, X. C., Yi, T., Yoshimoto, T., and Pei, D. H. (2000) Two continuous spectrophotometric assays for methionine aminopeptidase, Anal. Biochem. 280, 159-165.
38. Capon, B. (1969) Mechanism in carbohydrate chemistry, Chem. Rev. 69, 407-498.
39. Driguez, H. (2001) Thiooligosaccharides as tools for structural biology, ChemBioChem 2, 311-318.
40. Kiefel, M. J., Beisner, B., Bennett, S., Holmes, I. D., and von Itzstein, M. (1996) Synthesis and biological evaluation of N-acetylneuraminic acid-based rotavirus inhibitors, J. Med. Chem. 39, 1314-1320.
41. Barr, B. K., and Holewinski, R. J. (2002) 4-methyl-7-thioumbelliferyl- β-D-cellobioside: A fluorescent, nonhydrolyzable substrate analogue for cellulases, Biochemistry 41, 4447-4452.
42. Piyachomkwan, K, and Penner, M. H. (1998) Aryl thioglycoside-based affinity purification of exo-acting cellulases, Anal. Biochem. 255, 223-235.
43. Rich, J. R., and Bundle, D. R. (2004) S-linked ganglioside analogues for use in conjugate vaccines, Org. Lett. 6, 897-900.
44. Sabesan, S., Neira, S., Davidson, F., Duus, J. O., and Bock, K. (1994) Synthesis and enzymatic and NMR-studies of novel sialoside probes: Unprecedented, selective neuraminidase hydrolysis of and inhibition by C-6-(methyl)-Gal sialosides, J. Am. Chem. Soc. 116, 1616-1634.
45. Park, S., Lee, M. R., Pyo, S. J., and Shin, I. (2004) Carbohydrate chips for studying high-throughput carbohydrate-protein interactions, J. Am. Chem. Soc. 126, 4812-4819.
46. Reese, E. T., Clapp, R. C., and Mandels, M. (1958) A thioglucosidase in fungi, Arch. Biochem. Biophys. 75, 228-242.
47. Meulenbeld, G. H., and Hartmans, S. (2001) Thioglucosidase activity from Sphingobacterium sp strain OTG1, Appl. Biochem. Biotechnol. 56, 700-706.
48. Goodman, I., Fouts, J. R., Bresnick, E., Menegas, R., and Hitchings, G. H. (1959) Mammalian thioglycosidase, Science 130, 450-451.
49. Burmeister, W. P., Cottaz, S., Driguez, H., Iori, R., Palmieri, S., and Henrissat, B. (1997) The crystal structures of Sinapis alba myrosinase and a covalent glycosyl-enzyme intermediate provide insights into the substrate recognition and active-site machinery of an S-glycosidase, Structure 5, 663-675.
50. Macauley, M. S., Stubbs, K. A., and Vocadlo, D. J. (2005) O-GlcNAcase catalyzes cleavage of thioglycosides without general acid catalysis, J. Am Chem. Soc. 127, 17202-17203.
51. Privalova, I. M., and Khorlin, A. Y. (1969) Substrates and inhibitors of neuraminidase. I. Synthesis of O-, S-, and N-ketosides of N-acetyl-D-neuraminic acid, Izv. Akad. Nauk SSSR 12, 2785-2792.
52. Khorlin, A. Y., Privalova, I. M., Zakstelskaya, L. Y., Molibog, E. V., and Evstigneeva, N. A. (1970) Synthetic inhibitors of Vibrio cholerae neuraminidase and neuraminidases of some influenza virus strains, FEBS Lett. 8, 17-19.
53. Suzuki, Y., Sato, K., Kiso, M., and Hasegawa, A. (1990) New ganglioside analogues that inhibit influenza-virus sialidase, Glycoconjugate J. 7, 349-356.
54. Amaya, M. F., Buschiazzo, A., Nguyen, T., and Alzari, P. M. (2003) The high-resolution structures of free and inhibitor-bound Trypanosoma rangeli sialidase and its comparison with T. cruzi trans-sialidase, J. Mol. Biol. 325, 773-784.
55. Guo, X., Laver, W. G., Vimr, E., and 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.
56. Chou, D. T. H., Watson, J. N., Scholte, A. A., Borgford, T. J., and Bennet, A. J. (2000) Effect of neutral pyridine leaving groups on the mechanisms of influenza type A viral sialidase-catalyzed and the spontaneous hydrolysis reactions of α-D-N-acetyl-neuraminides, J. Am. Chem. Soc. 122, 8357-8364.
57. Fersht, A. (1985) Enzyme Structure and Mechanism, 2nd ed., pp 147-154, W. H. Freeman, New York.
58. Jahn, M., Marles, J., Warren, R. A. J., and Withers, S. G. (2003) Thioglycoligases: Mutant glycosidases for thioglycoside synthesis, Angew. Chem., Int. Ed. Engl. 42, 352-354.
59. Jahn, M., Chen, H. M., Mullegger, J., Marles, J., Warren, R. A. J., and Withers, S. G. (2004) Thioglycosynthases: double mutant glycosidases that serve as scaffolds for thioglycoside synthesis, Chem. Commun., 274-275.
60. Jencks, W. P., and Salvesen, K. (1971) Equilibrium deuterium isotope effects on ionization of thiol acids, J. Am. Chem. Soc. 93, 4433-4436.
61. Wilson, J. M., Bayer, R. J., and Hupe, D. J. (1977) Structure-reactivity correlations for thiol-disulfide interchange reaction, J. Am. Chem. Soc. 99, 7922-7926.