Strategies for modulating the pH-dependent activity of a family 11 glycoside hydrolase

Biochemistry

Volumn 52, Issue 18, 2013, Pages 3138-3156

  Ludwiczek, Martin L ^a,b   D'Angelo, Igor ^a   Yalloway, Gary N ^a   Brockerman, Jacob A ^a,b   Okon, Mark ^a,b   Nielsen, Jens E ^c   Strynadka, Natalie C J ^a   Withers, Stephen G ^a   McIntosh, Lawrence P ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS CIRCULANS XYLANASE; GLYCOSIDE HYDROLASES; IONIZATION STATE; NATURALLY OCCURRING; OPPOSITE CHARGE; PH-DEPENDENT ACTIVITY; REVERSE PROTONATION; SMALL POPULATION;

BACTERIOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

NUCLEOPHILES;

CARBOXYL GROUP; GLUTAMIC ACID; GLYCOSIDASE; GLYCOSIDE HYDROLASE 11; HISTIDINE; NUCLEOPHILE; UNCLASSIFIED DRUG; XYLAN ENDO 1,3 BETA XYLOSIDASE; XYLOBIOSIDE; XYLOSE;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS CIRCULANS; CARBON NUCLEAR MAGNETIC RESONANCE; CHEMICAL REACTION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME SUBSTRATE; HYDROLYSIS; MUTATION; NONHUMAN; PH; PKA; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; STATIC ELECTRICITY; SUCCINYLATION; WILD TYPE; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; GLYCOSIDE HYDROLASES; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MUTAGENESIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84877356787     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400034m     Document Type: Article

References (60)

1. Zechel, D. L. and Withers, S. G. (2000) Glycosidase mechanisms: anatomy of a finely tuned catalyst Acc. Chem. Res. 33, 11-18
2. Rye, C. S. and Withers, S. G. (2000) Glycosidase mechanisms Curr. Opin. Chem. Biol. 4, 573-580
3. Vocadlo, D. J. and Davies, G. J. (2008) Mechanistic insights into glycosidase chemistry Curr. Opin. Chem. Biol. 12, 539-555
4. Davies, G. J., Planas, A., and Rovira, C. (2012) Conformational analyses of the reaction coordinate of glycosidases Acc. Chem. Res. 45, 308-316
5. Sapag, A., Wouters, J., Lambert, C., de Ioannes, P., Eyzaguirre, J., and Depiereux, E. (2002) The endoxylanases from family 11: computer analysis of protein sequences reveals important structural and phylogenetic relationships J. Biotechnol. 95, 109-131
6. Collins, T., Gerday, C., and Feller, G. (2005) Xylanases, xylanase families and extremophilic xylanases FEMS Micro. Rev. 29, 3-23
7. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Nucleic Acids Res. 37, D233-238
8. Pollet, A., Delcour, J. A., and Courtin, C. M. (2010) Structural determinants of the substrate specificities of xylanases from different glycoside hydrolase families Crit. Rev. Biotechnol. 30, 176-191
9. Paes, G., Berrin, J. G., and Beaugrand, J. (2012) GH11 xylanases: Structure/function/properties relationships and applications Biotech. Adv. 30, 564-592
10. 13C-NMR study of Bacillus circulans xylanase Biochemistry 35, 9958-9966
11. Joshi, M. D., Sidhu, G., Nielsen, J. E., Brayer, G. D., Withers, S. G., and McIntosh, L. P. (2001) Dissecting the electrostatic interactions and pH-dependent activity of a family 11 glycosidase Biochemistry 40, 10115-10139
12. Joshi, M. D., Sidhu, G., Pot, I., Brayer, G. D., Withers, S. G., and McIntosh, L. P. (2000) Hydrogen bonding and catalysis: A novel explanation for how a single amino acid substitution can change the pH optimum of a glycosidase J. Mol. Biol. 299, 255-279
13. Mock, W. L. (1992) Theory of enzymatic reverse-protonation catalysis Bioorg. Chem. 20, 377-381
14. Sung, W. L., Luk, C. K., Zahab, D. M., and Wakarchuk, W. (1993) Overexpression and purification of the Bacillus subtilis and Bacillus circulans xylanases in Escherichia coli Prot. Express. Purif. 4, 200-216
15. Kunkel, T. A., Roberts, J. D., and Zakour, R. A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection Meth. Enzymol. 154, 367-382
16. Wakarchuk, W. W., Campbell, R. L., Sung, W. L., Davoodi, J., and Yaguchi, M. (1994) Mutational and crystallographic analyses of the active site residues of the Bacillus circulans xylanase Protein Sci. 3, 467-475
17. LeMaster, D. M. and Richards, F. M. (1988) NMR sequential assignment of Escherichia coli thioredoxin utilizing random fractional deuteriation Biochemistry 27, 142-150
18. 15N-amino acids. J Biomol. NMR 8, 184-192
19. Muchmore, D. C., McIntosh, L. P., Russell, C. B., Anderson, D. E., and Dahlquist, F. W. (1989) Expression and nitrogen-15 labeling of proteins for proton and nitrogen-15 nuclear magnetic resonance Methods Enzymol. 177, 44-73
20. Sidhu, G., Withers, S. G., Nguyen, N. T., McIntosh, L. P., Ziser, L., and Brayer, G. D. (1999) Sugar ring distortion in the glycosyl-enzyme intermediate of a family G/11 xylanase Biochemistry 38, 5346-5354
21. 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
22. Goddard, T. D. and Kneeler, D. G. (1999) Sparky 3, University of California, San Francisco.
23. Pelton, J. G., Torchia, D. A., Meadow, N. D., and Roseman, S. (1993) Tautomeric states of the active-site histidines of phosphorylated and unphosphorylated III(Glc), a signal-transducing protein from Escherichia coli, using 2-dimensional heteronuclear NMR techniques Protein Sci. 2, 543-558
24. Mulder, F. A. A., Spronk, C. A. E. M., Slijper, M., Kaptein, R., and Boelens, R. (1996) Improved HSQC experiments for the observation of exchange broadened signals J. Biomol. NMR 8, 223-228
25. Schubert, M., Poon, D. K. Y., Wicki, J., Tarling, C. A., Kwan, E. M., Nielsen, J. E., Withers, S. G., and McIntosh, L. P. (2007) Probing electrostatic interactions along the reaction pathway of a glycoside hydrolase: Histidine characterization by NMR spectroscopy Biochemistry 46, 7383-7395
26. 13C-labeled proteins J. Magn. Reson. Ser. B 112, 259-268
27. 20 J. Am. Chem. Soc. 115, 2055-2057
28. Oda, Y., Yamazaki, T., Nagayama, K., Kanaya, S., Kuroda, Y., and Nakamura, H. (1994) Individual ionization constants of all the carboxyl groups in Ribonuclease HI from Escherichia coli determined by NMR Biochemistry 33, 5275-5284
29. Plesniak, L. A., Connelly, G. P., Wakarchuk, W. W., and McIntosh, L. P. (1996) Characterization of a buried neutral histidine residue in Bacillus circulans xylanase: NMR assignments, pH titration, and hydrogen exchange Protein Sci. 5, 2319-2328
30. Connelly, G. P. and McIntosh, L. P. (1998) Characterization of a buried neutral histidine in Bacillus circulans xylanase: internal dynamics and interaction with a bound water molecule Biochemistry 37, 1810-1818
31. Sattler, M., Schleucher, J., and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients Prog. Nucl. Magn. Reson. Spectrosc. 34, 93-158
32. McIntosh, L. P., Naito, D., Baturin, S. J., Okon, M., Joshi, M. D., and Nielsen, J. E. (2011) Dissecting electrostatic interactions in Bacillus circulans xylanase through NMR-monitored pH titrations J. Biomol. NMR 51, 5-19
33. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Macromol. Cryst. Part A 276, 307-326
34. Mccoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
35. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921
36. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53, 240-255
37. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 486-501
38. Baturin, S. J., Okon, M., and McIntosh, L. P. (2011) Structure, dynamics, and ionization equilibria of the tyrosine residues in Bacillus circulans xylanase J. Biomol. NMR 51, 379-394
39. Means, G. E. and Feeney, R. E. (1971) Chemical Modification of Proteins, Holden-Day, San Francisco, CA.
40. Haynes, W. M. (2011) CRC Handbook of Chemistry and Physics (Haynes, W. M., Ed.), Chapman and Hall, Boca Raton, FL.
41. a values of the carboxyl and imidazole groups in Bacillus circulans xylanase Protein Sci. 6, 2667-2670
42. Grimsley, G. R., Scholtz, J. M., and Pace, C. N. (2009) A summary of the measured pK values of the ionizable groups in folded proteins Protein Sci. 18, 247-251
43. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., and Wishart, D. S. (2003) VADAR: a web server for quantitative evaluation of protein structure quality Nucleic Acids Res. 31, 3316-3319
44. Miao, S., Ziser, L., Aebersold, R., and Withers, S. G. (1994) Identification of glutamic acid 78 as the active site nucleophile in Bacillus subtilis xylanase using electrospray tandem mass spectrometry Biochemistry 33, 7027-7032
45. 2,5B conformations at the active centre Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 1344-1347
46. a, calculations Proteins 79, 685-702
47. Knowles, J. R. (1976) Intrinsic pKa values of functional groups in enzymes-Improper deductions from pH-dependence of steady-state parameters CRC Crit. Rev. Biochem. 4, 165-173
48. Michaux, C., Pouyez, J., Mayard, A., Vandurm, P., Housen, I., and Wouters, J. (2010) Structural insights into the acidophilic pH adaptation of a novel endo-1,4-beta-xylanase from Scytalidium acidophilum Biochimie 92, 1407-1415
49. Mamo, G., Thunnissen, M., Hatti-Kaul, R., and Mattiasson, B. (2009) An alkaline active xylanase: insights into mechanisms of high pH catalytic adaptation Biochimie 91, 1187-1196
50. Poon, D. K. Y., Ludwiczek, M. L., Schubert, M., Kwan, E. M., Withers, S. G., and McIntosh, L. P. (2007) NMR spectroscopic characterization of a beta-(1,4)-glycosidase along its reaction pathway: Stabilization upon formation of the glycosyl-enzyme intermediate Biochemistry 46, 1759-1770
51. Valenzuela, P. and Bender, M. L. (1971) Kinetic properties of succinylated and ethylenediamine-amidated -chymotrypsins Biochem. Biophys. Acta 250, 538-548
52. Russell, A. J. and Fersht, A. R. (1987) Rational modification of enzyme catalysis by engineering surface charge Nature 328, 496-500
53. Pey, A. L., Rodriguez-Larrea, D., Gavira, J. A., Garcia-Moreno, B., and Sanchez-Ruiz, J. M. (2010) Modulation of buried ionizable groups in proteins with engineered surface charge J. Am. Chem. Soc. 132, 1218-1219
54. Cockburn, D. W. and Clarke, A. J. (2011) Modulating the pH-activity profile of cellulase A from Cellulomonas fimi by replacement of surface residues Protein Eng. Des. Select. 24, 429-437
55. Tynan-Connolly, B. M. and Nielsen, J. E. (2007) Redesigning protein pKa values Protein Sci. 16, 239-249
56. Lawson, S. L., Wakarchuk, W. W., and Withers, S. G. (1996) Effects of both shortening and lengthening the active site nucleophile of Bacillus circulans xylanase on catalytic activity Biochemistry 35, 10110-10118
57. Lawson, S. L., Wakarchuk, W. W., and Withers, S. G. (1997) Positioning the acid/base catalyst in a glycosidase: Studies with Bacillus circulans xylanase Biochemistry 36, 2257-2265
58. Litzinger, S., Fischer, S., Polzer, P., Diederichs, K., Welte, W., and Mayer, C. (2010) Structural and kinetic analysis of Bacillus subtilis N-acetylglucosaminidase reveals a unique Asp-His dyad mechanism J. Biol. Chem. 285, 35675-35684
59. Chan, P. H., Lairson, L. L., Lee, H. J., Wakarchuk, W. W., Strynadka, N. C., Withers, S. G., and McIntosh, L. P. (2009) NMR spectroscopic characterization of the sialyltransferase CstII from Campylobacter jejuni: histidine 188 is the general base Biochemistry 48, 11220-11230
60. DeLano, W. L. and Lam, J. W. (2005) PyMOL: A communications tool for computational models Abs. Paper Am. Chem. Soc. 230, U1371-U1372