Crystal structure ofβ-1,4-glucan lyase, a unique glycoside hydrolase family member with a novel catalytic mechanism

Journal of Biological Chemistry

Volumn 288, Issue 37, 2013, Pages 26764-26774

  Rozeboom, Henriëtte J ^a   Yu, Shukun ^b   Madrid, Susan ^b,d   Kalk, Kor H ^a   Zhang, Ran ^c   Dijkstra, Bauke W ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b DANISCO A S   (Denmark)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d GENENCOR INTERNATIONAL INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC MECHANISMS; CATALYTIC NUCLEOPHILES; COVALENTLY BOUND; DUAL FUNCTION; ELIMINATION REACTION; GLYCOSIDE HYDROLASES;

BIOCHEMISTRY; BIOLOGY;

NUCLEOPHILES;

1 DEXOYNOJIRIMYCIN; ACARBOSE; ALPHA 1,4 GLUCAN LYASE; ASPARTIC ACID; CARBOHYDRATE DERIVATIVE; GLYCOSIDASE; NUCLEOPHILE; UNCLASSIFIED DRUG; 1 DEOXYNOJIRIMYCIN; ALPHA GLUCOSIDASE; ALPHA-1,4-GLUCAN LYASE; GLUCAN; GLUTAMIC ACID; POLYSACCHARIDE LYASE; PROTON; TRISACCHARIDE; VALINE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; GRACILARIOPSIS LEMANEIFORMIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; SEAWEED; STRUCTURE ACTIVITY RELATION; SULFOLOBUS SOLFATARICUS; ANHYDROFRUCTOSE PATHWAY; CARBOHYDRATE BINDING SITE; CHEMISTRY; ENZYME MECHANISMS; ENZYMOLOGY; GLYCOSYLATION INHIBITORS; GLYCOSYLENZYME INTERMEDIATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MUTATION; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY; X-RAY CRYSTALLOGRAPHY;

1-DEOXYNOJIRIMYCIN; ACARBOSE; ANHYDROFRUCTOSE PATHWAY; CARBOHYDRATE BINDING SITE; CRYSTAL STRUCTURE; ENZYME MECHANISMS; GLYCOSIDE HYDROLASES; GLYCOSYLATION INHIBITORS; GLYCOSYLENZYME INTERMEDIATE; X-RAY CRYSTALLOGRAPHY;

ACARBOSE; ALPHA-GLUCOSIDASES; CATALYSIS; CATALYTIC DOMAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRYSTALLOGRAPHY, X-RAY; GLUCANS; GLUTAMIC ACID; GLYCOSIDE HYDROLASES; MUTAGENESIS, SITE-DIRECTED; MUTATION; POLYSACCHARIDE-LYASES; PROTEIN STRUCTURE, TERTIARY; PROTONS; SEAWEED; SULFOLOBUS SOLFATARICUS; TRISACCHARIDES; VALINE;

EID: 84884169627     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.485896     Document Type: Article

References (50)

1. Henrissat, B., Sulzenbacher, G., and Bourne, Y. (2008) Glycosyltransferases, glycoside hydrolases: surprise, surprise! Curr. Opin. Struct. Biol. 18, 527-533
2. 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
3. Lombard, V., Bernard, T., Rancurel, C., Brumer, H., Coutinho, P. M., and Henrissat, B. (2010) A hierarchical classification of polysaccharide lyases for glycogenomics. Biochem. J. 432, 437-444
4. Yu, S., and Marcussen, J. (1999) in Recent Advances in Carbohydrate Bioengineering (Gilbert, H. J., Davies, G., Henrissat, B., and Svensson, B., eds) pp. 243-250, Royal Society of Chemistry Press, London, UK
5. Yu, S., Bojsen, K., Svensson, B., and Marcussen, J. (1999) α-1,4-Glucan lyases producing 1,5-anhydro-D-fructose from starch and glycogen have sequence similarity toα-glucosidases. Biochim. Biophys. Acta 1433, 1-15
6. Ernst, H. A., Lo Leggio, L., Willemoës, M., Leonard, G., Blum, P., and Larsen, S. (2006) Structure of the Sulfolobus solfataricusβ- glucosidase: implications for domain conservation and substrate recognition in GH31. J. Mol. Biol. 358, 1106-1124
7. Lee, S. S., Yu, S., and Withers, S. G. (2002)α-1,4-Glucan lyase performs a trans-elimination via a nucleophilic displacement followed by a syn-elimination. J. Am. Chem. Soc. 124, 4948-4949
8. Lovering, A. L., Lee, S. S., Kim, Y. W., Withers, S. G., and Strynadka, N. C. (2005) Mechanistic and structural analysis of a family 31β-glycosidase and its glycosyl-enzyme intermediate. J. Biol. Chem. 280, 2105-2115
9. Lee, S. S., Yu, S., and Withers, S. G. (2003) Detailed dissection of a new mechanism for glycoside cleavage:α-1,4-glucan lyase. Biochemistry 42, 13081-13090
10. Lee, S. S., Yu, S., and Withers, S. G. (2005) Mechanism of action of exoactingα-1,4-glucan lyase: a glycoside hydrolase family 31 enzyme. Biologia Bratislava 60, 137-148
11. Yoshinaga, K., Fujisue, M., Abe, J., Hanashiro, I., Takeda, Y., Muroya, K., and Hizukuri, S. (1999) Characterization of exo-(1,4)-βglucan lyase from red alga Gracilaria chorda: activation, inactivation and the kinetic properties of the enzyme. Biochim. Biophys. Acta 1472, 447-454
12. McCarter, J. D., and Withers, S. G. (1996) Unequivocal identification of Asp-214 as the catalytic nucleophile of Saccharomyces cerevisiaeβ- glucosidase using 5-fluoro glycosyl fluorides. J. Biol. Chem. 271, 6889-6894
13. Numao, S., Kuntz, D. A., Withers, S. G., and Rose, D. R. (2003) Insights into the mechanism of Drosophila melanogaster Golgiβ-mannosidase II through the structural analysis of covalent reaction intermediates. J. Biol. Chem. 278, 48074-48083
14. Larsbrink, J., Izumi, A., Ibatullin, F. M., Nakhai, A., Gilbert, H. J., Davies, G. J., and Brumer, H. (2011) Structural and enzymatic characterization of a glycoside hydrolase family 31β-xylosidase from Cellvibrio japonicus involved in xyloglucan saccharification. Biochem. J. 436, 567-580
15. Bojsen, K., Yu, S., Kragh, K. M., and Marcussen, J. (1999) A group ofα-1,4-glucan lyases and their genes from the red alga Gracilariopsis lemaneiformis: purification, cloning, and heterologous expression. Biochim. Biophys. Acta 1430, 396-402
16. Cook, M. W., and Thygesen, H. V. (2003) Safety evaluation of a hexose oxidase expressed in Hansenula polymorpha. Food Chem. Toxicol. 41, 523-529
17. Yu, S., Ahmad, T., Kenne, L., and Pedersén, M. (1995)α-1,4-Glucan lyase, a new class of starch glycogen-degrading enzyme. Substrate specificity, mode of action, and cleavage mechanism. Biochim. Biophys. Acta 1244, 1-9
18. Yu, S., Christensen, T. M., Kragh, K. M., Bojsen, K., and Marcussen, J. (1997) Efficient purification, characterization and partial amino acid sequencing of twoα-1,4-glucan lyases from fungi. Biochim. Biophys. Acta 1339, 311-320
19. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
20. McCarter, J. D., and Withers, S. G. (1996) 5-Fluoro glycosides: a new class of mechanism-based inhibitors of bothβ- andβ-glucosidases. J. Am. Chem. Soc. 118, 241-242
21. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R., and Leslie, A. G. (2011) iMosflm: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D 67, 271-281
22. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235-242
23. Kabsch, W. (2010) XDS. Acta Crystallogr. D 66, 125-132
24. 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
25. Jaroszewski, L., Rychlewski, L., Li, Z. W., Li, W. Z., and Godzik, A. (2005) FFAS03: a server for profile-profile sequence alignments. Res. Nucleic Acids Res. 33, W284-288
26. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D 67, 355-367
27. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for x-ray crystallography using ARP/ wARP version, Nat. Protoc. 3, 1171-1179
28. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of COOT. Acta Crystallogr. D 66, 486-501
29. Painter, J., and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111
30. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21
31. Yu, S., Olsen, C. E., and Marcussen, J. (1998) Methods for the assay of 1,5-anhydro-D-fructose andα-1,4-glucan lyase. Carbohydr. Res. 305, 73-82
32. Hirano, K., Ziak, M., Kamoshita, K., Sukenaga, Y., Kametani, S., Shiga, Y., Roth, J., and Akanuma, H. (2000) N-Linked oligosaccharide-processing enzyme glucosidase II produces 1,5-anhydrofructose as a side product. Glycobiology 10, 1283-1289
33. Yu, S., Kenne, L., and Pedersén, M. (1993)α-1,4-Glucan lyase, a new class of starch glycogen-degrading enzyme. Efficient purification and characterization from red seaweeds. Biochim. Biophys. Acta 1156, 313-320
34. Ernst, H. A., Leggio, L. L., Yu, S., Finnie, C., Svensson, B., and Larsen, L. (2005) Probing the structure of glucan lyases by sequence analysis, circular dichroism and proteolysis. Biologia Bratislava 60, 149-159
35. Sim, L., Quezada-Calvillo, R., Sterchi, E. E., Nichols, B. L., and Rose, D. R. (2008) Human intestinal maltase-glucoamylase: crystal structure of the N-terminal catalytic subunit and basis of inhibition and substrate specificity. J. Mol. Biol. 375, 782-792
36. Ren, L., Qin, X., Cao, X., Wang, L., Bai, F., Bai, G., and Shen, Y. (2011) Structural insight into substrate specificity of human intestinal maltaseglucoamylase. Protein Cell 2, 827-836
37. Sim, L., Willemsma, C., Mohan, S., Naim, H. Y., Pinto, B. M., and Rose, D. R. (2010) Structural basis for substrate selectivity in human maltaseglucoamylase and sucrase-isomaltase N-terminal domains. J. Biol. Chem. 285, 17763-17770
38. Tan, K., Tesar, C., Wilton, R., Keigher, L., Babnigg, G., and Joachimiak, A. (2010) Novelα-glucosidase from human gut microbiome: substrate specificities and their switch. FASEB J. 24, 3939-3949
39. Larsbrink, J., Izumi, A., Hemsworth, G. R., Davies, G. J., and Brumer, H. (2012) Structural enzymology of Cellvibrio japonicus Agd31B protein revealsα-transglucosylase activity in glycoside hydrolase family 31. J. Biol. Chem. 287, 43288-43299
40. Murzin, A. G., Brenner, S. E., Hubbard, T., and Chothia, C. (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247, 536-540
41. Cuyvers, S., Dornez, E., Delcour, J. A., and Courtin, C. M. (2012) Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases. Crit. Rev. Biotechnol. 32, 93-107
42. Nakai, H., Ito, T., Tanizawa, S., Matsubara, K., Yamamoto, T., Okuyama, M., Mori, H., Chiba, S., Sano, Y., and Kimura, A. (2006) Plantβ- glucosidase: molecular analysis of riceα-glucosidase and degradation mechanism of starch granules in germination stage. J. Appl. Glycosci. 53, 137-142
43. McCarter, J. D., and Withers, S. G. (1994) Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 4, 885-892
44. Okuyama, M., Kaneko, A., Mori, H., Chiba, S., and Kimura, A. (2006) Structural elements to convert Escherichia coliα-xylosidase (YicI) intoα-glucosidase. FEBS Lett. 580, 2707-2711
45. Trincone, A., Pagnotta, E., Rossi, M., Mazzone, M., and Moracci, M. (2001) Enzymatic synthesis of 2-deoxy-βglucosides and stereochemistry ofβ-glycosidase from Sulfolobus solfataricus on glucal. Tetrahedron Asym. 12, 2783-2787
46. Yip, V. L., and Withers, S. G. (2006) Breakdown of oligosaccharides by the process of elimination. Curr. Opin. Chem. Biol. 10, 147-155
47. Yu, S. (2008) The anhydrofructose pathway of glycogen catabolism. IUBMB Life 60, 798-809
48. Guillén Schlippe, Y. V., and Hedstrom, L. (2005) A twisted base? The role of arginine in enzyme-catalyzed proton abstractions. Arch. Biochem. Biophys. 433, 266-278
49. Okuyama, M., Okuno, A., Shimizu, N., Mori, H., Kimura, A., and Chiba, S. (2001) Carboxyl group of residue Asp647 as possible proton donor in catalytic reaction ofα-glucosidase from Schizosaccharomyces pombe. Eur. J. Biochem. 268, 2270-2280
50. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc- Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221