Rational engineering of mannosyl binding in the distal glycone subsites of cellulomonas fimi endo-β-1,4-mannanase: Mannosyl binding promoted at subsite -2 and demoted at subsite -3

Biochemistry

Volumn 49, Issue 23, 2010, Pages 4884-4896

  Hekmat, Omid ^a   Lo Leggio, Leila ^b   Rosengren, Anna ^a   Kamarauskaite, Jurate ^b   Kolenova, Katarina ^a   Stålbrand, Henrik ^a  

^a LUND UNIVERSITY   (Sweden)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RESIDUES; ANION EXCHANGE CHROMATOGRAPHY; CATALYTIC EFFICIENCIES; CELLULOMONAS; GLYCOSIDASES; GLYCOSIDE HYDROLASES; HYDROGEN BONDINGS; MANNANASE; MASS SPECTROMETRIC PROFILING; ORDER OF MAGNITUDE; POLYMERIC SUBSTRATE; PRODUCT ANALYSIS; RATIONAL REDESIGN; SOIL BACTERIUM; SPATIAL REPOSITIONING; SUBSITES; SUBSTRATE BINDING; WILD TYPES; X RAY CRYSTAL STRUCTURES;

AMINO ACIDS; CERIUM; CERIUM COMPOUNDS; CRYSTAL STRUCTURE; ENZYME KINETICS; ENZYMES; HYDROGEN BONDS; ORGANIC ACIDS; SUGARS;

SUBSTRATES;

CELLULASE; ENDO BETA 1,4 MANNANASE; MANNOSE OLIGOSACCHARIDE; UNCLASSIFIED DRUG;

ANION EXCHANGE CHROMATOGRAPHY; ARTICLE; CATALYSIS; CELL ENCAPSULATION; CELLULOMONAS; CHEMICAL MUTAGENESIS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME ENGINEERING; ENZYME KINETICS; ENZYME STRUCTURE; GENE EXPRESSION; HYDROLYSIS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SUBSTITUTION; BINDING SITES; CARBOHYDRATE SEQUENCE; CELLULOMONAS; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HYDROLYSIS; MANNOSE; MANNOSIDASES; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN ENGINEERING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); CELLULOMONAS FIMI; CELLVIBRIO JAPONICUS;

EID: 77953243269     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100097f     Document Type: Article

References (59)

1. Lundqvist, J., Teleman, A., Junel, L., Zaachi, G., Dahlman, O., Tjerneld, F., and Stålbrand, H. (2002) Isolation and characterization of galactoglucomannan from Spruce (Picea abies) Carbohydr. Polym. 48, 29-39
2. Gilbert, H. J., Stålbrand, H., and Brumer, H. (2008) How the walls come crumbling down: Recent structural biochemistry of plant polysaccharide degradation Curr. Opin. Plant Biol. 11, 338-348
3. 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-D238
4. Jenkins, J., Lo Leggio, L., Harris, G., and Pickersgill, R. (1995) β-Glucosidase, β-galactosidase, family A cellulases, family F xylanases and two barley glucanases form a superfamily of enzymes with 8-fold β/α architecture and with two conserved glutamates near the carboxy-terminal ends of β-strands four and seven FEBS Lett. 362, 281-285
5. Henrissat, B., Callebaut, I., Fabrega, S., Lehn, P., Mornon, J.-P., and Davies, G. (1995) Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases Proc. Natl. Acad. Sci. U.S.A. 92, 7090-7094
6. Zechel, D. L. and Withers, S. G. (2000) Glycosidase mechanisms: Anatomy of a finely tuned catalyst Acc. Chem. Res. 33, 11-18
7. Hägglund, P., Eriksson, T., Collen, A., Nerinckx, W., Claeyssen, M., and Stålbrand, H. (2003) A cellulose binding module of a Trichoderma reesei β-1,4-mannanase increases the mannan-hydrolysis of complex J. Biotechnol. 101, 37-48
8. Boraston, A. B., Bolam, D. N., Gilbert, H. J., and Davies, G. J. (2004) Carbohydrate-binding modules: Fine-tuning polysaccharide recognition Biochem. J. 382, 769-781
9. Hilge, M., Gloor, S. M., Rypniewski, W., Sauer, O., Heightman, T. D., Zimmermann, W., Winterhalter, K., and Piontek, K. (1998) High-resolution native and complex structures of thermostable β-mannanase from Thermomonospora fusca -substrate specificity in glycosyl hydrolase family 5 Structure 6, 1433-1444
10. Sabini, E., Schubert, H., Murshudov, G., Wilson, K. S., Siika-Aho, M., and Penttilä, M. (2000) The three-dimensional structure of a Trichoderma reesei β-mannanase from glycoside hydrolase family 5 Acta Crystallogr. D56, 3-13
11. Bourgault, R., Oakley, A. J., Bewley, J. D., and Wilce, M. C. (2005) Three-dimensional structure of (1,4)-β- d -mannan mannanohydrolase from tomato fruit Protein Sci. 14, 1233-1241
12. Larsson, A. M., Anderson, L., Xu, B., Muñoz, I. G., Usón, I., Janson, J. C., Stålbrand, H., and Ståhlberg, J. (2006) Three-dimensional crystal structure and enzymic characterization of β-mannanase Man5A from blue mussel Mytilus edulis J. Mol. Biol. 357, 1500-1510
13. Hogg, D., Woo, E. J., Bolam, D. N., McKie, V. A., Gilbert, H. J., and Pickersgill, R. W. (2001) Crystal structure of mannanase 26A from Pseudomonas cellulosa and analysis of residues involved in substrate binding J. Biol. Chem. 276, 31186-31192
14. (2,5) conformation for the transition state Angew. Chem., Int. Ed. 41, 2824-2827
15. Jahn, M., Stoll, D., Warren, R. A., Szabó, L., Singh, P., Gilbert, H. J., Ducros, V. M., Davies, G. J., and Withers, S. G. (2003) Expansion of the glycosynthase repertoire to produce defined manno-oligosaccharides Chem. Commun. 12, 1327-1329
16. Le Nours, J., Anderson, L., Stoll, D., Stålbrand, H., and Lo Leggio, L. (2005) The structure and characterization of a modular endo-β-1,4-mannanase from Cellulomonas fimi Biochemistry 44, 12700-12708
17. Cartmell, A., Topakas, E., Ducros, V. M., Suits, M. D., Davies, G. J., and Gilbert, H. J. (2008) The Cellvibrio japonicus mannanase CjMan26C displays a unique exo-mode of action that is conferred by subtle changes to the distal region of the active site J. Biol. Chem. 283, 34403-34413
18. Yan, X. X., An, X. M., Gui, L. L., and Liang, D. C. (2008) From structure to function: Insights into the catalytic substrate specificity and thermostability displayed by Bacillus subtilis mannanase BCman J. Mol. Biol. 379, 535-544
19. Tailford, L. E., Ducros, V. M., Flint, J. E., Roberts, S. M., Morland, C., Zechel, D. L., Smith, N., Bjornvad, M. E., Borchert, T. V., Wilson, K. S., Davies, G. J., and Gilbert, H. J. (2009) Understanding how diverse β-mannanases recognize heterogeneous substrates Biochemistry 48, 7009-7018
20. Davies, G. J., Wilson, K. S., and Henrissat, B. (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases Biochem. J. 321, 557-559
21. Tailford, L. E., Offen, W. A., Smith, N. L., Dumon, C., Morland, C., Gratien, J., Heck, M. P., Stick, R. V., Bleriot, Y., Vasella, A., Gilbert, H. J., and Davies, G. J. (2008) Structural and biochemical evidence for a boat-like transition state in β-mannosidases Nat. Chem. Biol. 4, 306-312
22. Stoll, D., Stålbrand, H., and Warren, R. A. J. (1999) Mannan-degrading enzymes from Cellulomonas fimi Appl. Environ. Microbiol. 65, 2598-2605
23. Stoll, D., Boraston, A., Stålbrand, H., McLean, B. W., Kilburn, D. G., and Warren, R. A. J. (2000) Mannanase Man26A from Cellulomonas fimi has a mannan-binding module FEMS Microbiol. Lett. 183, 265-269
24. 1H-NMR Biocatal. Biotransform. 26, 86-95
25. Bolam, D. N., Hughes, N., Virden, R., Lakey, J. H., Hazlewood, G. P., Henrissat, B., Braithwaite, K. L., and Gilbert, H. J. (1996) Mannanase A from Pseudomonas fluorescens ssp. cellulosa is a retaining glycosyl hydrolase in which E212 and E320 are the putative catalytic residues Biochemistry 35, 16195-16204
26. Horton, R. M., Hunt, H. D., Ho, S. N., Pullen, J. K., and Pease, L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77, 61-68
27. Stålbrand, H., Siika-aho, M., Tenkanen, M., and Viikari, L. (1993) Purification and characterization of two β-mannanases from Trichoderma reesei J. Biotechnol. 29, 229-242
28. Leslie, A. G. (1999) Integration of macromolecular diffraction data Acta Crystallogr. D55, 1696-1702
29. Evans, P. R. (1997) Scaling of MAD data Joint CCP4 and ESF-EACBM Newsletter 33, 22-24
30. Weiss, M. S. (2001) Global indicators of X-ray data quality J. Appl. Crystallogr. 34, 130-135
31. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
32. Vagin, A. and Teplyakov, A. (1997) MOLREP: An automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025
33. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
34. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
35. Perrakis, A., Morris, R. M., and Lamzin, V. S. (1999) Automated protein model building combined with iterative structure refinement Nat. Struct. Biol. 6, 458-463
36. Bounias, M. (1980) N-(1-naphthyl)ethylenediamine dihydrochloride as a new reagent for nanomole quantification of sugars on thin-layer plates by a mathematical calibration process Anal. Biochem. 106, 291-295
37. 18O water and ESI-MS detection in subsite characterisation and investigation of the hydrolytic action of an endoglucanase Anal. Bioanal. Chem. 394, 1977-1984
38. Antonov, V. K., Ginodman, L. M., Rumsh, L. D., Kapitannikov, Y. V., Barshevskaya, T. N., Yavashev, L. P., Gurova, A. G., and Volkova, L. I. (1981) Studies on the mechanisms of action of proteolytic enzymes using heavy oxygen exchange Eur. J. Biochem. 117, 195-200
39. Angeles, T. S., Roberts, G. A., Carr, S. A., and Meek, T. D. (1992) Solvent isotope partitioning: A new kinetic tool for the determination of desorption rates of reactant water from enzyme-substrate complexes in proteases Biochemistry 31, 11778-11784
40. Julka, S. and Regnier, F. (2004) Quantification in proteomics through stable isotope coding: A review J. Proteome Res. 3, 350-363
41. Leitner, A. and Lindner, W. (2004) Current chemical tagging strategies for proteome analysis by mass spectrometry J. Chromatogr., B 813, 1-26
42. 18O-labeling strategies for quantitative proteomics Mass Spectrom. Rev. 26, 121-136
43. Tüting, W., Wegemann, K., and Mischnick, P. (2004) Enzymatic degradation and electrospray tandem mass spectrometry as tools for determining the structure of cationic starches prepared by wet and dry methods Carbohydr. Res. 339, 637-648
44. Varki, A., Sherman, W., and Kornfeld, S. (1983) Demonstration of the enzymatic mechanisms of α-N-acetyl- d -glucosamine-1-phosphodiester N-acetylglucosaminidase (formerly called α-N- acetylglucosaminylphosphodiesterase) and lysosomal α-N- acetylglucosaminidase Arch. Biochem. Biophys. 222, 145-149
45. Kiso, T., Nakano, H., Nakajima, H., Terai, T., Okamoto, K., and Kitahata, S. (2000) Hydrolysis of β-galactosyl ester linkage by β- galactosidases Biosci., Biotechnol., Biochem. 64, 1702-1706
46. Kato, M., Takehara, K., Kettoku, M., Kobayashi, K., and Shimizu, T. (2000) Subsite structure and catalytic mechanism of a new glycosyltrehalose- producing enzyme isolated from the hyperthermophilic archaeum, Sulfolobus solfataricus KM1 Biosci., Biotechnol., Biochem. 64, 319-326
47. Haga, K., Kanai, R., Sakamoto, O., Aoyagi, M., Harata, K., and Yamane, K. (2003) Effects of essential carbohydrate/aromatic stacking interaction with Tyr100 and Phe259 on substrate binding of cyclodextrin glycosyltransferase from alkalophilic Bacillus sp. 1011 J. Biochem. 134, 881-891
48. Albenne, C., Skov, L. K., Mirza, O., Gajhede, M., Feller, G., D(Amico, S., André, G., Potocki-Véronse, G., van der Veen, B. A., Monsan, P., and Remaud-Simeon, M. (2004) Molecular basis of the amylose-like polymer formation catalyzed by Neisseria polysaccharea amylosucrase J. Biol. Chem. 279, 726-734
49. Ademark, P., Varga, A., Medve, J., Harjunpää, V., Drakenberg, T., Tjerneld, F., and Stålbrand, H. (1998) Softwood hemicellulose- degrading enzymes from Aspergillus niger: Purification and properties of a β-mannanase J. Biotechnol. 63, 199-210
50. Braithwaite, K. L., Black, G. W., Hazlewood, G. P., Ali, B. R., and Gilbert, H. J. (1995) A non-modular endo-β-1,4-mannanase from Pseudomonas fluorescens subspecies cellulosa Biochem. J. 305, 1005-1010
51. Fersht, A. (1999) Structure and Mechanism in Protein Science, W. H. Freeman and Co., New York.
52. Hekmat, O., Tokuyasu, K., and Withers, S. G. (2003) Subsite structure of the endo-type chitin deacetylase from a deuteromycete, Colletotrichum lindemuthianum: An investigation using steady-state kinetic analysis and MS Biochem. J. 374, 369-380
53. Thoma, J. A., Rao, G. V., Brothers, C., Spradlin, J., and Li, L. H. (1971) Subsite mapping of enzymes. Correlation of product patterns with Michaelis parameters and substrate-induced strain J. Biol. Chem. 246, 5621-5635
54. Allen, J. D. (1980) Subsite mapping on enzymes: Application to polysaccharide depolymerases Methods Enzymol. 64, 248-277
55. Charnock, S. J., Spurway, T. D., Xie, H., Beylot, M. H., Virden, R., Warren, R. A., Hazlewood, G. P., and Gilbert, H. J. (1998) The topology of the substrate binding clefts of glycosyl hydrolase family 10 xylanases are not conserved J. Biol. Chem. 273, 32187-32199
56. Ly, H. D. and Withers, S. G. (1999) Mutagenesis of glycosidases Annu. Rev. Biochem. 68, 487-522
57. Charnock, S. J., Lakey, J. H., Virden, R., Hughes, N., Sinnott, M. L., Hazlewood, G. P., Pickersgill, R., and Gilbert, H. J. (1997) Key residues in subsite F play a critical role in the activity of Pseudomonas fluorescens subspecies cellulosa xylanase A against xylooligosaccharides but not against highly polymeric substrates such as xylan J. Biol. Chem. 272, 2942-2951
58. Armand, S., Andrews, S. R., Charnock, S. J., and Gilbert, H. J. (2001) Influence of the aglycone region of the substrate binding cleft of Pseudomonas xylanase 10A on catalysis Biochemistry 40, 7404-7409
59. Bak-Jensen, K. S., Andre, G., Gottschalk, T. E., Paes, G., Tran, V., and Svensson, B. (2004) Tyrosine 105 and threonine 212 at outermost substrate binding subsites -6 and +4 control substrate specificity, oligosaccharide cleavage patterns, and multiple binding modes of barley α-amylase 1 J. Biol. Chem. 279, 10093-10102