NMR spectroscopic characterization of a β-(1,4)-glycosidase along its reaction pathway: Stabilization upon formation of the glycosy 1-enzyme intermediate

Biochemistry

Volumn 46, Issue 7, 2007, Pages 1759-1770

  Poon, David K Y ^c   Ludwiczek, Martin L ^c   Schubert, Mario ^b   Kwan, Emily M ^c   Withers, Stephen G ^c   McIntosh, Lawrence P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ETH ZURICH   (Switzerland)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

CHAIN CHEMICAL SHIFT PERTURBATIONS; DYNAMIC PROPERTIES; MICROSECOND TIME SCALES; TRYPTOPHAN SIDE CHAINS;

CHEMICAL MODIFICATION; CRYSTALLOGRAPHY; ENZYME INHIBITION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; REACTION KINETICS; THERMODYNAMIC PROPERTIES;

ENZYMES;

2,4 DINITROPHENOL; 2,4 DINITROPHENYL 2 DEOXY 2 FLUORO BETA CELLOBIOSIDE; AMIDE; BETA (1,4) GLYCOSIDASE; CELLOBIOSE; GLYCOSIDASE; INDOLE; NITROGEN 15; THERMOLYSIN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ALPHA CHAIN; ARTICLE; BETA CHAIN; CATALYSIS; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HYDROLYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; REACTION ANALYSIS; THERMODYNAMICS;

APOENZYMES; BETA-GLUCOSIDASE; BINDING SITES; CATALYTIC DOMAIN; CELLULOMONAS; CIRCULAR DICHROISM; GLUCOSIDES; HEAT; HYDROLYSIS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN DENATURATION; THERMODYNAMICS; THERMOLYSIN;

EID: 33847058858     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061694c     Document Type: Article

References (56)

1. Rye, C. S., and Withers, S. G. (2000) Glycosidase mechanisms, Curr. Opin. Chem. Biol. 4, 573-580.
2. Zechel, D. L., and Withers, S. G. (2001) Dissection of nucleophilic and acid-base catalysis in glycosidases, Curr. Opin. Chem. Biol. 5, 643-649.
3. Henrissat, B., and Davies, G. (1997) Structural and sequence-based classification of glycoside hydrolases, Curr. Opin. Struct. Biol. 7, 637-644.
4. Coutinho, P. M., and Henrissat, B. (1999) Carbohydrate-active enzymes: An integrated database approach, in Recent advances in carbohydrate bioengineering (Gilbert, H. J., Davies, G., Henrissat, B., and Svensson, B., Eds.) pp 3-12, The Royal Society of Chemistry, Cambridge, U.K.
5. Notenboom, V., Birsan, C., Warren, R. A. J., Withers, S. G., and Rose, D. R. (1998) Exploring the cellulose/xylan specificity of the β-1,4-glycanase cex from Cellulomonas fimi through crystallography and mutation, Biochemistry 37, 4751-4758.
6. White, A., Withers, S. G., Gilkes, N. R., and Rose, D. R. (1994) Crystal structure of the catalytic domain of the β-1,4-glycanase cex from Cellulomonas fimi, Biochemistry 33, 12546-12552.
7. White, A., Tull, D., Johns, K., Withers, S. G., and Rose, D. R. (1996) Crystallographic observation of a covalent catalytic intermediate in a β-glycosidase, Nat. Struct. Biol. 3, 149-154.
8. Connelly, G. P., Withers, S. G., and McIntosh, L. P. (2000) Analysis of the dynamic properties of Bacillus circulans xylanase upon formation of a covalent glycosyl-enzyme intermediate, Protein Sci. 9, 512-524.
9. O'Neill, G. P., Kilburn, D. G., Warren, R. A., and Miller, R. C., Jr. (1986) Overproduction from a cellulase gene with a high guanosine-plus-cytosine content in Escherichia coli, Appl. Environ. Microbiol. 52, 737-743.
10. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein, Protein Sci. 4, 2411-2423.
11. McCarter, J. D., Adam, M. J., Braun, C., Namchuk, M., Tull, D., and Withers, S. G. (1993) Syntheses of 2-deoxy-2-fluoro monosaccharide and oligosaccharide glycosides from glycals and evaluation as glycosidase inhibitors, Carbohydr. Res. 249, 77-90.
12. Tull, D., and Withers, S. G. (1994) Mechanisms of cellulases and xylanases: A detailed kinetic study of the exo-β-1,4-glycanase from Cellulomonas fimi, Biochemistry 33, 6363-6370.
13. N-detected triple resonance TROSY-based experiments, J. Biomol. NMR 13, 3-10.
14. 13C-labeled proteins via scalar couplings, J. Am. Chem. Soc. 115, 11054-11055.
15. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRpipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
16. Goddard, T. D., and Kneeler, D. G. (1999) Sparky 3, University of California, San Francisco.
17. 15N chemical-shift referencing in biomolecular NMR, J. Biomol. NMR 6, 135-140.
18. 15N NMR relaxation, Biochemistry 33, 5984-6003.
19. Palmer, A. G., III (1998) Curvefit, Columbia University, New York.
20. Lipari, G., and Szabo, A. (1982) Model-free approach to the interpretation of nuclear magnetic-resonance relaxation in macromolecules. 1. Theory and range of validity, J. Am. Chem. Soc. 104, 4546-4559.
21. 15N inverse detected heteronuclear NMR spectroscopy: Application to staphylococcal nuclease, Biochemistry 28, 8972-8979.
22. Mandel, A. M., Akke, M., and Palmer, A. G., III (1995) Backbone dynamics of Escherichia coli ribonuclease H1: Correlations with structure and function in an active enzyme, J. Mol. Biol. 246, 144-163.
23. Dosset, P., Hus, J. C., Marion, D., and Blackledge, M. (2001) A novel interactive tool for rigid-body modeling of multi-domain macromolecules using residual dipolar couplings, J. Biomol. NMR 20, 223-231.
24. Hu, W., Lee, K. C., and Cross, T. A. (1993) Tryptophans in membrane-proteins: Indole ring orientations and functional implications in the gramicidin channel, Biochemistry 32, 7035-7047.
25. Goldman, M. (1984) Interference effects in the relaxation of a pair of unlike spin-1/2 nuclei, J. Magn. Reson. 60, 437-452.
26. Mulder, F. A. A., Hon, B., Mittermaier, A., Dahlquist, F. W., and Kay, L. E. (2002) Slow internal dynamics in proteins: Application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme, J. Am. Chem. Soc. 124, 1443-1451.
27. Zhang, Y. Z. (2006) Protein and peptide structure and interactions studied by hydrogen exchange and NMR, Ph.D. Thesis, University of Pennsylvania, Philadelphia.
28. Bai, Y. W., Milne, J. S., Mayne, L., and Englander, S. W. (1993) Primary structure effects on peptide group hydrogen-exchange, Proteins 17, 75-86.
29. Connelly, G. P., Bai, Y. W., Jeng, M. F., and Englander, S. W. (1993) Isotope effects in peptide group hydrogen-exchange, Proteins 17, 87-92.
30. Pace, C. N., Shirley, B. A., and Thomson, J. A. (1989) Measuring the conformational stability of a protein, in Protein Structure: A Practical Approach (Creighton, T. E., Ed.) pp 311-330, IRL Press, Oxford, U.K.
31. Park, C., and Marqusee, S. (2004) Probing the high energy states in proteins by proteolysis, J. Mol. Biol. 343, 1467-1476.
32. Vadrevu, R., Falzone, C. J., and Matthews, C. R. (2003) Partial NMR assignments and secondary structure mapping of the isolated of subunit of Escherichia coli tryptophan synthase, a 29-kD TIM barrel protein, Protein Sci. 12, 185-191.
33. Tugarinov, V., Muhandiram, R., Ayed, A., and Kay, L. E. (2002) Four-dimensional NMR spectroscopy of a 723-residue protein: Chemical shift assignments and secondary structure of malate synthase G, J. Am. Chem. Soc. 124, 10025-10035.
34. Massi, F., Wang, C., and Palmer, A. G., III (2006) Solution NMR and computer simulation studies of active site loop motion in triosephosphate isomerase, Biochemistry 45, 10787-10794.
35. 15N multidimensional NMR to study the structure and dynamics of proteins, Annu. Rev. Biophys. Biomol. Struct. 27, 357-406.
36. 15N NMR relaxation, Prog. Nucl. Magn. Reson. Spectrosc. 31, 63-105.
37. de la Torre, J. G., Huertas, M. L., and Carrasco, B. (2000) HYDRONMR: Prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations, J. Magn. Reson. 147, 138-146.
38. Boehr, D. D., Dyson, H. J., and Wright, P. E. (2006) An NMR perspective on enzyme dynamics, Chem. Rev. 106, 3055-3079.
39. Englander, S. W., Sosnick, T. R., Englander, J. J., and Mayne, L. (1996) Mechanisms and uses of hydrogen exchange, Curr. Opin. Struct. Biol. 6, 18-23.
40. Nagano, N., Orengo, C. A., and Thornton, J. M. (2002) One fold with many functions: The evolutionary relationships between TIM barrel families based on their sequences, structures and functions, J. Mol. Biol. 327,741-765.
41. Tugarinov, V., and Kay, L. E. (2003) Quantitative NMR studies of high molecular weight proteins: Application to domain orientation and ligand binding in the 723 residue enzyme malate synthase G, J. Mol. Biol. 327, 1121-1133.
42. Tugarinov, V., Hwang, P. M., and Kay, L. E. (2004) Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins, Annu. Rev. Biochem. 73, 107-146.
43. 2H NMR relaxation studies of the 723-residue enzyme malate synthase G reveal a dynamic binding Interface, Biochemistry 44, 15970-15977.
44. Street, I. P., Kempton, J. B., and Withers, S. G. (1992) Inactivation of a β-glucosidase through the accumulation of a stable 2-deoxy-2-fluoro- α-D-glucopyranosyl enzyme intermediate: A detailed investigation, Biochemistry 31, 9970-9978.
45. Nikolova, P. V., Creagh, A. L., Duff, S. J. B., and Haynes, C. A. (1997) Thermostability and irreversible activity loss of exoglucanase/xylanase Cex from Cellulomonas fimi, Biochemistry 36, 1381-1388.
46. Tomme, P., Creagh, A. L., Kilburn, D. G., and Haynes, C. A. (1996) Interaction of polysaccharides with the N-terminal cellulose-binding domain of Cellulomonas fimi CenC. 1. Binding specificity and calorimetric analysis, Biochemistry 35, 13885-13894.
47. Zolotnitsky, G., Cogan, U., Adir, N., Solomon, V., Shoham, G., and Shoham, Y. (2004) Mapping glycoside hydrolase substrate subsites by isothermal titration calorimetry, Proc. Natl. Acad. Sci. U.S.A. 101, 11275-11280.
48. Williams, D. H., Stephens, E., O'Brien, D. P., and Zhou, M. (2004) Understanding noncovalent interactions: Ligand binding energy and catalytic efficiency from ligand-induced reductions in motion within receptors and enzymes, Angew. Chem., Int. Ed. 43, 6596-6616.
49. 15N heteronuclear correlation spectroscopy, J. Am. Chem. Soc. 128, 15388-15389.
50. 13C-NMR study of Bacillus circulans xylanase, Biochemistry 35, 9958-9966.
51. Bai, Y. W. (2006) Protein folding pathways studied by pulsed- and native-state hydrogen exchange, Chem. Rev. 106, 1757-1768.
52. Savard, P. Y., and Gagné, S. M. (2006) Backbone dynamics of TEM-1 determined by NMR: Evidence for a highly ordered protein, Biochemistry 45, 11414-11424.
53. Kern, D., and Zuiderweg, E. R. P. (2003) The role of dynamics in allosteric regulation, Curr. Opin. Struct. Biol. 13, 748-757.
54. Notenboom, V., Birsan, C., Nitz, M., Rose, D. R., Warren, R. A. J., and Withers, S. G. (1998) Insights into transition state stabilization of the β-1,4-glycosidase Cex by covalent intermediate accumulation in active site mutants, Nat. Struct. Biol. 5, 812-818.
55. Notenboom, V., Williams, S. J., Hoos, R., Withers, S. G., and Rose, D. R. (2000) Detailed structural analysis of glycosidase/inhibitor interactions: Complexes of Cex from Cellulomonas fimi with xylobiose-derived aza-sugars. Biochemistry 39, 11553-11563.
56. Davies, G. J., Mackenzie, L., Varrot, A., Dauter, M., Brzozowski, A. M., Schulein, M., and Withers, S. G. (1998) Snapshots along an enzymatic reaction coordinate: Analysis of a retaining β-glycoside hydrolase, Biochemistry 37, 11707-11713.