Mutational, structural, and kinetic evidence for a dissociative mechanism in the GDP-mannose mannosyl hydrolase reaction

Biochemistry

Volumn 44, Issue 25, 2005, Pages 8989-8997

  Xia, Zuyong ^a   Azurmendi, Hugo F ^a   Lairson, Luke L ^b   Withers, Stephen G ^b   Gabelli, Sandra B ^a   Bianchet, Mario A ^a   Amzel, L Mario ^a   Mildvan, Albert S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINITY; CATALYSIS; DISSOCIATION; ELECTRONS; ENZYMES; HYDROGEN BONDS; HYDROLYSIS; MUTAGENESIS; SUBSTITUTION REACTIONS; SUBSTRATES; SUGARS; X RAYS;

GDP-MANNOSE HYDROLASE (GDPMH); MUTANTS; NUCLEOPHILIC SUBSTITUTION; X-RAY STRUCTURE;

ENZYME KINETICS;

GLUTAMIC ACID; GUANOSINE DIPHOSPHATE; GUANOSINE DIPHOSPHATE ALPHA DEXTRO MANNOSE; GUANOSINE DIPHOSPHATE MANNOSE; GUANOSINE DIPHOSPHATE MANNOSE MANNOSYL HYDROLASE; HISTIDINE; HYDROLASE; MAGNESIUM; UNCLASSIFIED DRUG;

ALKALINITY; AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME MECHANISM; FLUORINATION; HYDROGEN BOND; HYDROLYSIS; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SUBSTITUTION REACTION; WILD TYPE; X RAY CRYSTALLOGRAPHY;

ARGININE; ASPARTIC ACID; CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; GUANOSINE DIPHOSPHATE FUCOSE; GUANOSINE DIPHOSPHATE MANNOSE; HYDROGEN-ION CONCENTRATION; HYDROLASES; HYDROLYSIS; KINETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SUBSTRATE SPECIFICITY; TYROSINE;

EID: 21744459739     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050583v     Document Type: Article

References (34)

1. Mildvan, A. S., Xia, Z., Azurmendi, H. F., Saraswat, V., Legler, P. M., Massiah, M. A., Gabelli, S. B., Bianchet, M. A., Rang, L.-W., and Amzel, L. M. (2005) Structures and mechanisms of Nudix hydrolases, Arch. Biochem. Biophys. 433, 129-143.
2. Frick, D. N., Townsend, B. D., and Bessman, M. J. (1995) A novel GDP-mannose mannosyl hydrolase shares homology with the MutT family of enzymes, J. Biol. Chem. 270, 24086-24091.
3. 2+ complex and mechanism of its pyrophosphohydrolase action, Biochemistry 36, 1199-1211.
4. Legler, P. M., Lee, H. C., Peisach, J., and Mildvan, A. S. (2002) Kinetic and magnetic resonance studies of the role of metal ions in the mechanism of E. coli GDP-mannose mannosyl hydrolase, an unusual Nudix enzyme, Biochemistry 41, 4655-4668.
5. Legler, P. M., Massiah, M. A., and Mildvan, A. S. (2002) Mutational, kinetic, and NMR studies of the mechanism of E. coli GDP-mannose mannosyl hydrolase, an unusual Nudix enzyme, Biochemistry 41, 10834-10848.
6. Gabelli, S. B., Bianchet, M. A., Azurmendi, H. F., Xia, Z., Saraswat, V., Mildvan, A. S., and Amzel, L. M. (2004) Structure and mechanism of GDP-mannose glycosyl hydrolase, a Nudix enzyme that cleaves at carbon instead of phosphorus, Structure 12, 927-935.
7. Legler, P. M., Massiah, M. A., Bessman, M. J., and Mildvan, A. S. (2000) GDP-mannose hydrolase catalyzes nucleophilic substitution at carbon, unlike all other Nudix enzymes, Biochemistry 39, 8603-8608.
8. Gabelli, S. B., Bianchet, M. A., Ohnishi, Y., Ichikawa, Y., Bessman, M. J., and Amzel, L. M. (2002) Mechanism of the Escherichia coli ADP-ribose pyrophosphatase, a Nudix hydrolase, Biochemistry 41, 9279-9285.
9. Withers, S. G. (2001) Mechanism of glycosyl transferases and hydrolases, Carbohydr. Polym. 44, 325-337.
10. Vasella, A., Davies, G. J., and Böhm, M. (2002) Glycosidase mechanisms, Curr. Opin. Chem. Biol. 6, 619-629.
11. Guérin, D. M. A., Lascombe, M.-B., Costabel, M., Souchon, H., Lamzin, V., Béguin, P., and Alzari, P. M. (2002) Atomic (0.94 Å) resolution structure of an inverting glycosidase in complex with substrate, J. Mol. Biol. 315, 1061-1069.
12. Cleland, W. W., and Henge, A. C. (1995) Mechanisms of phosphoryl and acyl transfer, FASEB J. 9, 1585-1594.
13. Mildvan, A. S. (1997) Mechanisms of signaling and related enzymes, Proteins: Struct., Funct., Genet. 29, 401-416.
14. Withers, S. G., Rupitz, K., and Street, I. P. (1988) 2-Deoxy-2-fluoro-D- glycosyl fluorides: A new class of specific mechanism-based glycosidase inhibitors, J. Biol. Chem. 263, 7929-7932.
15. Burkart, M. D., Vincent, S. P., Düffels, A., Murray, B. W., Ley, S. V., and Wong, C.-H. (2000) Chemo-enzymatic synthesis of fluorinated sugar nucleotide: Useful mechanistic probes for glycosyltransferases, Bioorg. Med. Chem. 8, 1937-1946.
16. Xia, Z., Azurmendi, H. F., Gabelli, S. B., Bianchet, M. A., Amzel, L. M., and Mildvan, A. S. (2004) Structural and mutational evidence for a dissociative mechanism in the reaction catalyzed by GDP-mannose mannosyl hydrolase (GDPMH), Poster BIOL-108, 228th National Meeting of the American Chemical Society, Philadelphia, PA, Aug 22-26, 2004.
17. Stick, R. V., and Watts, A. G. (2002) The chameleon of retaining glycoside hydrolases and retaining glycosyl transferases: The catalytic nucleophile, Monatsh. Chem. 133, 541-554.
18. Wong, C.-H., and Hayashi, T. (1998) Process for preparing nucleotide inhibitors of glycosyltransferases, U.S. Patent 5,770,-407; WO Patent 98/25940.
19. Gill, S. C., and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem. 182, 319-326.
20. Saraswat, V., Azurmendi, H. F., and Mildvan, A. S. (2004) Mutational, NMR, and NH exchange studies of the selective binding of 8-oxo-dGMP by the MutT pyrophohydrolase, Biochemistry 43, 3404-3414.
21. Mahuren, J. D., Coburn, S. P., Slominski, A., and Wortsman, J. (2001) Microassay of phosphate provides a general method for measuring the activity of phosphatases using physiological non-chromogenic substrates such as lysophosphatidic acid, Anal. Biochem. 298, 241-245.
22. Czerwinski, R. M., Johnson, W. H., Whitman, C. P., Harris, T. K., Abeygunawardana, C., and Mildvan, A. S. (1997) Kinetic and structural effects of mutations of the catalytic amino-terminal proline in 4-oxalocrotonate tautomerase, Biochemistry 36, 14551-14560.
23. Mildvan, A. S., Weber, D. J., and Kuliopulos, A. (1992) Quantitative interpretations of double mutations of enzymes, Arch. Biochem. Biophys. 294, 327-340.
24. Mildvan, A. S. (2004) Inverse thinking about double mutants of enzymes, Biochemistry 43, 14517-14520.
25. Jensen, H. H., Lyngbye, L., Jensen, A., and Bols, M. (2002) Stereoelectronic substituent effects in polyhydroxylated piperidines and hexahydropyridazines, Chem.-Eur. J. 8, 1218-1226.
26. Dixon, M., Webb, E. C., Thorne, C. J. R., and Tipton, K. F. (1979) Enzymes, 3rd ed., p 163, Academic Press, New York.
27. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM: A program for macromolecular energy, minimization and dynamics calculations, J. Comput. Chem. 4, 187-217.
28. Withers, S. G., MacLennan, D. J., and Street, I. P. (1986) The synthesis and hydrolysis of a series of deoxyfluoro-D-glucopyranosyl phosphates, Carbohydr. Res. 154, 127-144.
29. Zechel, D. L., and Withers, S. G. (2000) Glycosidase mechanisms: Anatomy of a finely tuned catalyst, Acc. Chem. Res. 33, 11-18.
30. Wolfenden, R., Lu, X., and Young, G. (1998) Spontaneous hydrolysis of glycosides, J. Am. Chem. Soc. 120, 6814-6815.
31. Percival, M. D., and Withers, S. G. (1992) Binding energy and catalysis: Deoxyfluoro sugars as probes of hydrogen bonding in phosphoglucomutase, Biochemistry 31, 498-505.
32. 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.
33. Burmeister, W. P., Cottaz, S., Rollin, P., Vasella, A., and Henrissat, B. (2000) High-resolution X-ray crystallography shows that ascorbate is a cofactor for myrosinases and substitutes for the function of the catalytic base, J. Biol. Chem. 275, 39385-39393.
34. Burmeister, W. P., Cottaz, S., Driguez, H., Ion, 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.