Oligosaccharide and substrate binding in the starch debranching enzyme barley limit dextrinase

Journal of Molecular Biology

Volumn 427, Issue 6, 2015, Pages 1263-1277

  Møller, Marie S ^a,b,c   Windahl, Michael S ^a   Sim, Lyann ^a,d   Bøjstrup, Marie ^a,e   Abou Hachem, Maher ^b   Hindsgaul, Ole ^a   Palcic, Monica ^a   Svensson, Birte ^b   Henriksen, Anette ^a,f  

^a CARLSBERG LABORATORY   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c ROSKILDE UNIVERSITY   (Denmark)

^d RYERSON UNIVERSITY   (Canada)

^e PFIZER INC   (United States)

^f NOVO NORDISK A S   (Denmark)

Author keywords

pullulanase; substrate specificity; thio oligosaccharide; transglycosylase; 1,6 glucosidase

Indexed keywords

CARBOXYLIC ACID; GLUTAMIC ACID; OLIGO 1,6 GLUCOSIDASE; OLIGOSACCHARIDE; STARCH; GLYCOSIDASE; MALTOOLIGOSACCHARIDES; MALTOSE; PULLULANASE;

ARTICLE; AUREOBASIDIUM PULLULANS; BINDING SITE; CHEMICAL BINDING; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GERMINATION; HYDROLYSIS; KLEBSIELLA PNEUMONIAE; MAIZE; NUCLEOPHILICITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DATA BANK; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; HORDEUM; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

HORDEUM;

BINDING SITES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLYCOSIDE HYDROLASES; HORDEUM; HYDROLYSIS; MALTOSE; MODELS, MOLECULAR; OLIGOSACCHARIDES; PROTEIN CONFORMATION; STARCH; SUBSTRATE SPECIFICITY;

EID: 84924120262     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.12.019     Document Type: Article

References (51)

1. A. Buleon, P. Colonna, V. Planchot, and S. Ball Starch granules: structure and biosynthesis Int J Biol Macromol 23 1998 85 112
2. S.J. Kays Secondary metabolic processes and products Secondary metabolic processes and products 1991 Van Nostrand Reinhold New York 143 256
3. M. Kristensen, F. Lok, V. Planchot, I. Svendsen, R. Leah, and B. Svensson Isolation and characterization of the gene encoding the starch debranching enzyme limit dextrinase from germinating barley Biochim Biophys Acta 1431 1999 538 546
4. M. Kristensen, V. Planchot, J. Abe, and B. Svensson Large-scale purification and characterization of barley limit dextrinase, a member of the α-amylase structural family Cereal Chem 75 1998 473 479
5. M.J. Sissons, M. Taylor, and M. Proudlove Barley malt limit dextrinase: its extraction, heat stability and activity during malting and mashing J Am Soc Brew Chem 53 1995 105 110
6. D.E. Evans, R. Damsberg, D. Ratkowsky, C. Li, S. Harasymow, and S. Roumeliotis Refining the prediction of potential malt fermentability by including an assessment of limit dextrinase thermostability and additional measures of malt modification, using two different methods for multivariate model development J Inst Brew 116 2010 86 96
7. C.A. McCafferty, H.R. Jenkinson, J.M. Brosnan, and J.H. Bryce Does its malt activity relate to its activity during brewing? J Inst Brew 110 2004 284 296
8. X.D. Wang, J. Yang, and G.P. Zhang Genotypic and environmental variation in barley limit dextrinase activity and its relation to malt quality J Zhejiang Univ Sci B 7 2006 386 392
9. K. Stenholm, and S. Home A new approach to limit dextrinase and its role in mashing J Inst Brew 105 1999 205 210
10. J.R. Dinges, C. Colleoni, M.G. James, and A.M. Myers Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism Plant Cell 15 2003 666 680
11. B.L. Cantarel, P.M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics Nucleic Acids Res 37 2009 D233 D238
12. M.R. Stam, E.G. Danchin, C. Rancurel, P.M. Coutinho, and B. Henrissat Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of α-amylase-related proteins Protein Eng Des Sel 19 2006 555 562
13. R.S. Singh, G.K. Saini, and J.F. Kennedy Pullulan: microbial sources, production and applications Carbohydr Polym 73 2008 515 531
14. J.C. Uitdehaag, R. Mosi, K.H. Kalk, B.A. van der Veen, L. Dijkhuizen, and S.G. Withers X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the α-amylase family Nat Struct Biol 6 1999 432 436
15. G. Davies, and B. Henrissat Structures and mechanisms of glycosyl hydrolases Structure 3 1995 853 859
16. E.A. MacGregor, S. Janecek, and B. Svensson Relationship of sequence and structure to specificity in the α-amylase family of enzymes Biochim Biophys Acta 1546 2001 1 20
17. E.A. MacGregor An overview of clan GH-H and distantly-related families Biologia 60 2005 5 12
18. M.S. Møller, M. Abou Hachem, B. Svensson, and A. Henriksen Structure of the starch-debranching enzyme barley limit dextrinase reveals homology of the N-terminal domain to CBM21 Acta Crystallogr Sect F Struct Biol Cryst Commun 68 2012 1008 1012
19. M.B. Vester-Christensen, M. Abou Hachem, B. Svensson, and A. Henriksen Crystal structure of an essential enzyme in seed starch degradation: barley limit dextrinase in complex with cyclodextrins J Mol Biol 403 2010 739 750
20. B. Mikami, H. Iwamoto, D. Malle, H.J. Yoon, E. Demirkan-Sarikaya, and Y. Mezaki Crystal structure of pullulanase: evidence for parallel binding of oligosaccharides in the active site J Mol Biol 359 2006 690 707
21. L.J. Gourlay, I. Santi, A. Pezzicoli, G. Grandi, M. Soriani, and M. Bolognesi Group B Streptococcus pullulanase crystal structures in the context of a novel strategy for vaccine development J Bacteriol 191 2009 3544 3552
22. A. Lammerts van Bueren, E. Ficko-Blean, B. Pluvinage, J.H. Hehemann, M.A. Higgins, and L. Deng The conformation and function of a multimodular glycogen-degrading pneumococcal virulence factor Structure 19 2011 640 651
23. D. Malle, T. Itoh, W. Hashimoto, K. Murata, S. Utsumi, and B. Mikami Overexpression, purification and preliminary X-ray analysis of pullulanase from Bacillus subtilis strain 168 Acta Crystallogr Sect F Struct Biol Cryst Commun 62 2006 381 384
24. J.P. Turkenburg, A.M. Brzozowski, A. Svendsen, T.V. Borchert, G.J. Davies, and K.S. Wilson Structure of a pullulanase from Bacillus acidopullulyticus Proteins 76 2009 516 519
25. J. Xu, F. Ren, C.H. Huang, Y. Zheng, J. Zhen, and H. Sun Functional and structural studies of pullulanase from Anoxybacillus sp. LM18-11 Proteins 82 2013 1685 1693
26. G.J. Davies, K.S. Wilson, and B. Henrissat Nomenclature for sugar-binding subsites in glycosyl hydrolases Biochem J 321 1997 557 559
27. F.W. Studier, A.H. Rosenberg, J.J. Dunn, and J.W. Dubendorff Use of T7 RNA polymerase to direct expression of cloned genes Methods Enzymol 185 1990 60 89
28. M.T. Jensen Structure and function of barley limit dextrinase and mutational analysis of barley α-amylase isozyme differences and interaction with branched oligosaccharides Ph.D. Thesis 2002 University of Southern Denmark Odense
29. V. Kumar Analysis of the key active subsites of glycoside hydrolase 13 family members Carbohydr Res 345 2010 893 898
30. L. Greffe, M.T. Jensen, C. Bosso, B. Svensson, and H. Driguez Chemoenzymatic synthesis of branched oligo- and polysaccharides as potential substrates for starch active enzymes Chembiochem 4 2003 1307 1311
31. M.B. Vester-Christensen, M. Abou Hachem, H. Naested, and B. Svensson Secretory expression of functional barley limit dextrinase by Pichia pastoris using high cell-density fermentation Protein Expr Purif 69 2010 112 119
32. X. Robert, R. Haser, H. Mori, B. Svensson, and N. Aghajari Oligosaccharide binding to barley α-amylase 1 J Biol Chem 280 2005 32968 32978
33. K. Hasegawa, M. Kubota, and Y. Matsuura Roles of catalytic residues in α-amylases as evidenced by the structures of the product-complexed mutants of a maltotetraose-forming amylase Protein Eng 12 1999 819 824
34. M. Yamashita, D. Matsumoto, and Y. Murooka Amino acid residues specific for the catalytic action towards α-1,6-glucosidic linkages in Klebsiella pullulanase J Ferment Bioeng 84 1997 283 290
35. X. Robert, R. Haser, T.E. Gottschalk, F. Ratajczak, H. Driguez, and B. Svensson The structure of barley α-amylase isozyme 1 reveals a novel role of domain C in substrate recognition and binding: a pair of sugar tongs Structure 11 2003 973 984
36. A. Kadziola, M. Sogaard, B. Svensson, and R. Haser Molecular structure of a barley alpha-amylase-inhibitor complex: implications for starch binding and catalysis J Mol Biol 278 1998 205 217
37. D.J. Manners, and D. Yellowlees Studies on carbohydrate metabolising enzymes. Part XXVI. Limit dextrinase from germinated barley Starch/Staerke 23 1971 228 234
38. D.G. Hardie, D.J. Manners, and D. Yellowlees The limit dextrinase from malted sorghum (Sorghum vulgare) Carbohydr Res 50 1976 75 85
39. D. Yellowlees Purification and characterisation of limit dextrinase from Pisum sativum L Carbohydr Res 83 1980 109 118
40. S.L. Hii, J.S. Tan, T.C. Ling, and A.B. Ariff Pullulanase: role in starch hydrolysis and potential industrial applications Enzyme Res 921362 2012 1 14
41. L. Greffe, M.T. Jensen, F. Chang-Pi-Hin, S. Fruchard, M.J. O'Donohue, and B. Svensson Chemoenzymatic syntheses of linear and branched hemithiomaltodextrins as potential inhibitors for starch-debranching enzymes Chem Eur J 8 2002 5447 5455
42. C.T. Jørgensen, A. Svendsen, and J. Brask Enzymatic synthesis of oligosaccharides from branched cyclodextrins Carbohydr Res 340 2005 1233 1237
43. W. Kabsch XDS Acta Crystallogr D Biol Crystallogr 66 2010 125 132
44. T.G. Battye, L. Kontogiannis, O. Johnson, H.R. Powell, and A.G. Leslie iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM Acta Crystallogr D Biol Crystallogr 67 2011 271 281
45. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, and P.R. Evans Overview of the CCP4 suite and current developments Acta Crystallogr D Biol Crystallogr 67 2011 235 242
46. E. Potterton, P. Briggs, M. Turkenburg, and E. Dodson A graphical user interface to the CCP4 program suite Acta Crystallogr D Biol Crystallogr 59 2003 1131 1137
47. A. Vagin, and A. Teplyakov Molecular replacement with MOLREP Acta Crystallogr D Biol Crystallogr 66 2010 22 25
48. G.N. Murshudov, P. Skubak, A.A. Lebedev, N.S. Pannu, R.A. Steiner, and R.A. Nicholls REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr D Biol Crystallogr 67 2011 355 367
49. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr D Biol Crystallogr 66 2010 486 501
50. R.A. Laskowski, M.W. MacArthur, D.S. Moss, and J.M. Thornton Procheck: a program to check the stereochemical quality of protein structures J Appl Crystallogr 26 1993 283 291
51. V.B. Chen, W.B. Arendall, J.J. Headd, D.A. Keedy, R.M. Immormino, and G.J. Kapral MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr D Biol Crystallogr 66 2010 12 21