Broadening the synthetic potential of disaccharide phosphorylases through enzyme engineering

Process Biochemistry

Volumn 47, Issue 1, 2012, Pages 11-17

  Desmet, Tom ^a   Soetaert, Wim ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Biocatalysis; Disaccharide phosphorylases; Enzyme engineering; Glycosyl phosphate; Glycosylation; High throughput screening

Indexed keywords

BIOCATALYSIS; DISACCHARIDE PHOSPHORYLASES; ENZYME ENGINEERING; GLYCOSYL; HIGH-THROUGHPUT SCREENING;

BIOCATALYSTS; CARBOHYDRATES; GLYCOSYLATION; PHOSPHORYLATION; SUBSTRATES;

ENZYMES;

EID: 83655201119     PISSN: 13595113     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.procbio.2011.10.039     Document Type: Review

References (86)

1. T. Desmet, and W. Soetaert Enzymatic glycosyl transfer: mechanisms and applications Biocatal Biotransform 29 2011 1 18
2. M. Kitaoka, and K. Hayashi Carbohydrate-processing phosphorolytic enzymes Trends Glycosci Glycotechnol 14 2002 35 50
3. S. de Kok, D. Yilmaz, E. Suir, J.T. Pronk, J.M. Daran, and A.J. van Maris Increasing free-energy (ATP) conservation in maltose-grown Saccharomyces cerevisiae by expression of a heterologous maltose phosphorylase Metab Eng 2011 10.1016/j.ymben.2011.06.001
4. C. Luley-Goedl, and B. Nidetzky Carbohydrate synthesis by disaccharide phosphorylases: reactions, catalytic mechanisms and application in the glycosciences Biotechnol J 5 2010 1324 1338
5. J. Seibel, H.J. Jordening, and K. Buchholz Glycosylation with activated sugars using glycosyltransferases and transglycosidases Biocatal Biotransform 24 2006 311 342 (Pubitemid 44615045)
6. M.M. Palcic Glycosyltransferases as biocatalysts Curr Opin Chem Biol 15 2011 226 233
7. K. De Winter, A. Cerdobbel, W. Soetaert, and T. Desmet Operational stability of immobilized sucrose phosphorylase: continuous production of α-glucose-1-phosphate at elevated temperatures Process Biochem 46 2011 2074 2078
8. B. Nidetzky, R. Griessler, A. Weinhausel, D. Haltrich, and K.D. Kulbe Reaction engineering aspects of alpha-1,4-d-glucan phosphorylase catalysis: comparison of plant and bacterial enzymes for the continuous synthesis of d-glucose-1-phosphate Appl Biochem Biotechnol 1997 63 65
9. K. Aisaka, T. Masuda-Kato, T. Chikamune, K. Kamitori, Y. Uosaki, and Y. Saito Enzymatic synthesis of novel disaccharides using disaccharide phosphorylases J Biosci Bioeng 90 2000 208 213
10. J. Van der Borght, T. Desmet, and W. Soetaert Enzymatic production of β-d-glucose-1-phosphate Biotechnol J 5 2010 986 993
11. M.R. De Groeve, V. Depreitere, T. Desmet, and W. Soetaert Enzymatic production of alpha-d-galactose 1-phosphate by lactose phosphorolysis Biotechnol Lett 31 2009 1873 1877
12. C. Eis, and B. Nidetzky Characterization of trehalose phosphorylase from Schizophyllum commune Biochem J 341 1999 385 393 (Pubitemid 29373664)
13. B. Nidetzky, C. Eis, and M. Albert Role of non-covalent enzyme-substrate interactions in the reaction catalysed by cellobiose phosphorylase from Cellulomonas uda Biochem J 351 2000 649 659
14. Y.B. Tewari, and R.N. Goldberg Thermodynamics of hydrolysis of disaccharides J Biol Chem 264 1999 3966 3971
15. C. Goedl, A. Schwarz, A. Minani, and B. Nidetzky Recombinant sucrose phosphorylase from Leuconostoc mesenteroides: characterization, kinetic studies of transglucosylation, and application of immobilised enzyme for production of alpha-d-glucose 1-phosphate J Biotechnol 129 2007 77 86 (Pubitemid 46400019)
16. A. Cerdobbel, K. De Winter, T. Desmet, and W. Soetaert Sucrose phosphorylase as cross-linked enzyme aggregate: improved thermal stability for industrial applications Biotechnol J 5 2010 1192 1197
17. P. Wildberger, C. Luley-Goedl, and B. Nidetzky Aromatic interactions at the catalytic subsite of sucrose phosphorylase: their roles in enzymatic glucosyl transfer probed with Phe52 → Ala and Phe52 → Asn mutants FEBS Lett 585 2011 499 504
18. C. Goedl, T. Sawangwan, M. Mueller, A. Schwarz, and B. Nidetzky A high-yielding biocatalytic process for the production of 2-O-(alpha-d- glucopyranosyl)-sn-glycerol, a natural osmolyte and useful moisturizing ingredient Angew Chem Int Ed Engl 47 2008 10086 10089
19. G.H. Tran, T. Desmet, M. De Groeve, and W. Soetaert Probing the active site of cellodextrin phosphorylase from Clostridium stercorarium: kinetic characterization, ligand docking and site-directed mutagenesis Biotechnol Progr 27 2011 326 332
20. E.D. Chrysina The prototype of glycogen phosphorylase Mini-Rev Med Chem 10 2010 1093 1101
21. R.S. Rathore, N. Garg, S. Garg, and A. Kumar Starch phosphorylase: role in starch metabolism and biotechnological applications Crit Rev Biotechnol 29 2009 214 224
22. O. Mirza, L.K. Skov, D. Sprogoe, L.A. van den Broek, G. Beldman, and J.S. Kastrup Structural rearrangements of sucrose phosphorylase from Bifidobacterium adolescentis during sucrose conversion J Biol Chem 281 2006 35576 35584 (Pubitemid 46036591)
23. A. Schwarz, L. Brecker, and B. Nidetzky Acid-base catalysis in Leuconostoc mesenteroides sucrose phosphorylase probed by site-directed mutagenesis and detailed kinetic comparison of wild-type and Glu237 → Gln mutant enzymes Biochem J 403 2007 441 449 (Pubitemid 46706972)
24. J. Wiesbauer, C. Goedl, A. Schwarz, L. Brecker, and B. Nidetzky Substitution of the catalytic acid-base Glu237 by Gln suppresses hydrolysis during glucosylation of phenolic acceptors catalyzed by Leuconostoc mesenteroides sucrose phosphorylase J Mol Catal B: Enzym 65 2009 24 29
25. C. Goedl, A. Schwarz, M. Mueller, L. Brecker, and B. Nidetzky Mechanistic differences among retaining disaccharide phosphorylases: insights from kinetic analysis of active site mutants of sucrose phosphorylase and alpha,alpha-trehalose phosphorylase Carbohydr Res 343 2008 2032 2040
26. C. Goedl, and B. Nidetzky Sucrose phosphorylase harbouring a redesigned, glycosyltransferase-like active site exhibits retaining glucosyl transfer in the absence of a covalent intermediate Chembiochem 10 2009 2333 2337
27. N.J. Turner Directed evolution drives the next generation of biocatalysts Nat Chem Biol 5 2009 567 573
28. A.S. Bommarius, J.K. Blum, and M.J. Abrahamson Status of protein engineering for biocatalysts: how to design an industrially useful biocatalyst Curr Opin Chem Biol 15 2011 194 200
29. C.H. Fiske, and Y. Subbarow The colorimetric determination of phosphorus J Biol Chem 66 1925 375 400
30. E.B. Cogan, G.B. Birrell, and O.H. Griffith A robotics-based automated assay for inorganic and organic phosphates Anal Biochem 271 1999 29 35 (Pubitemid 29287847)
31. P. Drueckes, R. Schinzel, and D. Palm Photometric microtiter assay of inorganic phosphate in the presence of acid-labile organic phosphates Anal Biochem 230 1995 173 177
32. J.D. Gawronski, and D.R. Benson Microtiter assay for glutamine synthetase biosynthetic activity using inorganic phosphate detection Anal Biochem 327 2004 114 118 (Pubitemid 38367990)
33. M.R. De Groeve, G.H. Tran, A. Van Hoorebeke, J. Stout, T. Desmet, and S.N. Savvides Development and application of a screening assay for glycoside phosphorylases Anal Biochem 401 2010 162 167
34. S.O. Engblom The phosphate sensor Biosens Bioelectron 13 1998 981 994 (Pubitemid 28506009)
35. L. Hoflack, M. De Groeve, T. Desmet, P. Van Gerwen, and W. Soetaert High throughput calorimetry for evaluating enzymatic reactions generating phosphate Comb Chem High Throughput Screen 13 2010 331 336
36. A. Cerdobbel, T. Desmet, K. De Winter, J. Maertens, and W. Soetaert Increasing the thermostability of sucrose phosphorylase by multipoint covalent immobilization J Biotechnol 150 2010 125 130
37. H.-C. Choi, D.-H. Seo, J.-H. Jung, S.-J. Ha, M.-J. Kim, and J.-H. Lee Development of new assay for sucrose phosphorylase and its application to the characterization of Bifidobacterium longum SJ32 sucrose phosphorylase Food Sci Biotechnol 20 2011 513 518
38. D. Aerts, T.F. Verhaeghe, B.I. Roman, C.V. Stevens, T. Desmet, and W. Soetaert Transglucosylation potential of six sucrose phosphorylases toward different classes of acceptors Carbohydr Res 346 2011 1860 1868
39. L.A. van den Broek, E.L. van Boxtel, R.P. Kievit, R. Verhoef, G. Beldman, and A.G. Voragen Physico-chemical and transglucosylation properties of recombinant sucrose phosphorylase from Bifidobacterium adolescentis DSM20083 Appl Microbiol Biotechnol 65 2004 219 227 (Pubitemid 39062485)
40. B. Vilozny, A. Schiller, R.A. Wessling, and B. Singaram Enzyme assays with boronic acid appended bipyridinium salts Anal Chim Acta 649 2009 246 251
41. D. Aerts, T. Verhaeghe, M. De Mey, T. Desmet, and W. Soetaert A constitutive expression system for high-throughput screening Eng Life Sci 11 2011 10 19
42. K. Shintate, M. Kitaoka, Y.K. Kim, and K. Hayashi Enzymatic synthesis of a library of beta-(1,4) hetero-d-glucose and d-xylose-based oligosaccharides employing cellodextrin phosphorylase Carbohydr Res 338 2003 1981 1990 (Pubitemid 37272064)
43. M. Mueller, and B. Nidetzky The role of Asp-295 in the catalytic mechanism of Leuconostoc mesenteroides sucrose phosphorylase probed with site-directed mutagenesis FEBS Lett 581 2007 1403 1408 (Pubitemid 46452614)
44. V. Kren, and T. Rezanka Sweet antibiotics - the role of glycosidic residues in antibiotic and antitumor activity and their randomization FEMS Microbiol Rev 32 2008 858 889
45. M.R. De Groeve, M. De Baere, L. Hoflack, T. Desmet, E.J. Vandamme, and W. Soetaert Creating lactose phosphorylase enzymes by directed evolution of cellobiose phosphorylase Protein Eng Des Sel 22 2009 393 399
46. M.R.M. De Groeve, T. Desmet, and W. Soetaert Engineering of cellobiose phosphorylase for glycoside synthesis J Biotechnol 2011 10.1016/j.jbiotec.2011. 07.006
47. Van Hoorebeke A. Structure-functional studies of bacterial glycoside phosphorylases. PhD Thesis. Belgium: Ghent University; 2010.
48. De Groeve M. Engineering of cellobiose phosphorylase for glycoside synthesis. PhD Thesis. Belgium: Ghent University; 2009.
49. H. Chaen, T. Nakada, T. Nishimoto, N. Kuroda, S. Fukuda, and T. Sugimoto Purification and characterization of thermostable trehalose phosphorylase from Thermoanaerobacter brockii J Appl Glycosci 46 1999 399 405
50. K. Aisaka, T. Masuda, and T. Chikamune Properties of maltose phosphorylase from Propionibacterium freudenreichii J Ferment Bioeng 82 1996 171 173 (Pubitemid 26327264)
51. H. Okada, E. Fukushi, S. Onodera, T. Nishimoto, J. Kawabata, and M. Kikuchi Synthesis and structural analysis of five novel oligosaccharides prepared by glucosyltransfer from beta-d-glucose 1-phosphate to isokestose and nystose using Thermoanaerobacter brockii kojibiose phosphorylase Carbohydr Res 338 2003 879 885 (Pubitemid 36398007)
52. A. Percy, H. Ono, and K. Hayashi Acceptor specificity of cellobiose phosphorylase from Cellvibrio gilvus: synthesis of three branched trisaccharides Carbohydr Res 308 1998 423 429 (Pubitemid 28349986)
53. H. Watanabe, T. Higashiyama, H. Aga, T. Nishimoto, M. Kubota, and S. Fukuda Enzymatic synthesis of a 2-O-alpha-d-glucopyranosyl cyclic tetrasaccharide by kojibiose phosphorylase Carbohydr Res 340 2005 449 454 (Pubitemid 40186772)
54. H. Nakai, M.J. Baumann, B.O. Petersen, Y. Westphal, H. Schols, and A. Dilokpimol The maltodextrin transport system and metabolism in Lactobacillus acidophilus NCFM and production of novel alpha-glucosides through reverse phosphorolysis by maltose phosphorylase FEBS J 276 2009 7353 7365
55. H. Nakai, A. Dilokpimol, M. Abou Hachem, and B. Svensson Efficient one-pot enzymatic synthesis of alpha-(1 → 4)-glucosidic disaccharides through a coupled reaction catalysed by Lactobacillus acidophilus NCFM maltose phosphorylase Carbohydr Res 345 2010 1061 1064
56. T. Yamamoto, H. Yamashita, K. Mukai, H. Watanabe, M. Kubota, and H. Chaen Construction and characterization of chimeric enzymes of kojibiose phosphorylase and trehalose phosphorylase from Thermoanaerobacter brockii Carbohydr Res 341 2006 2350 2359 (Pubitemid 44279607)
57. M.P. Egloff, J. Uppenberg, L. Haalck, and H. van Tilbeurgh Crystal structure of maltose phosphorylase from Lactobacillus brevis: unexpected evolutionary relationship with glucoamylases Structure 9 2001 689 697 (Pubitemid 32772891)
58. H. Nakai, B.O. Petersen, Y. Westphal, A. Dilokpimol, M. Abou Hachem, and J.O. Duus Rational engineering of Lactobacillus acidophilus NCFM maltose phosphorylase into either trehalose or kojibiose dual specificity phosphorylase Protein Eng Des Sel 23 2010 781 787
59. M. Hidaka, M. Kitaoka, K. Hayashi, T. Wakagi, H. Shoun, and S. Fushinobu Structural dissection of the reaction mechanism of cellobiose phosphorylase Biochem J 398 2006 37 43 (Pubitemid 44231299)
60. M.R. De Groeve, L. Remmery, A. Van Hoorebeke, J. Stout, T. Desmet, and S.N. Savvides Construction of cellobiose phosphorylase variants with broadened acceptor specificity towards anomerically substituted glucosides Biotechnol Bioeng 107 2010 413 420
61. T. Yamamoto, H. Watanabe, T. Nishimoto, H. Aga, M. Kubota, and H. Chaen Acceptor recognition of kojibiose phosphorylase from Thermoanaerobacter brockii: syntheses of glycosyl glycerol and myo-inositol J Biosci Bioeng 101 2006 427 433 (Pubitemid 44354423)
62. K. Kino, R. Satake, T. Morimatsu, S. Kuratsu, Y. Shimizu, and M. Sato A new method of synthesis of alkyl beta-glycosides using sucrose as sugar donor Biosci Biotechnol Biochem 72 2008 2415 2417
63. K. Kino, Y. Shimizu, S. Kuratsu, and K. Kirimura Enzymatic synthesis of alpha-anomer-selective d-glucosides using maltose phosphorylase Biosci Biotechnol Biochem 71 2007 1598 1600 (Pubitemid 47012029)
64. C. Goedl, T. Sawangwan, P. Wildberger, and B. Nidetzky Sucrose phosphorylase: a powerful transglucosylation catalyst for the synthesis of alpha-d-glucosides as industrial fine chemicals Biocatal Biotransform 28 2010 10 21
65. J.J. Mieyal, M. Simon, and R.H. Abeles Mechanism of action of sucrose phosphorylase. 3. The reaction with water and other alcohols J Biol Chem 247 1972 532 542
66. T. Kwon, C.T. Kim, and J.H. Lee Transglucosylation of ascorbic acid to ascorbic acid 2-glucoside by a recombinant sucrose phosphorylase from Bifidobacterium longum Biotechnol Lett 29 2007 611 615 (Pubitemid 46384905)
67. S. Kitao, T. Ariga, T. Matsuda, and H. Sekine The syntheses of catechin glucosides by transglycosylation with Leuconostoc mesenteroides sucrose phosphorylase Biosci Biotechnol Biochem 57 1993 2010 2015
68. S. Kitao, T. Matsudo, T. Sasaki, T. Koga, and M. Kawamura Enzymatic synthesis of stable, odorless, and powdered furanone glucosides by sucrose phosphorylase Biosci Biotechnol Biochem 64 2000 134 141
69. S. Kitao, T. Matsudo, and H. Sekine Enzymatic syntheses of two stable (-)-epigallocatechin gallate-glucosides by sucrose phosphorylase Biosci Biotechnol Biochem 59 1995 2167 2169
70. S. Kitao, and H. Sekine Syntheses of two kojic acid glucosides with sucrose phosphorylase from Leuconostoc mesenteroides Biosci Biotechnol Biochem 58 1994 419 420
71. S. Kitao, and H. Sekine Alpha-d-glucosyl transfer to phenolic compounds by sucrose phosphorylase from Leuconostoc mesenteroides and production of alpha-arbutin Biosci Biotechnol Biochem 58 1994 38 42 (Pubitemid 2050079)
72. R. Renirie, A. Pukin, B. van Lagen, and M.C.R. Franssen Regio- and stereoselective glucosylation of diols by sucrose phosphorylase using sucrose or glucose 1-phosphate as glucosyl donor J Mol Catal B: Enzym 67 2010 219 224
73. K. Sugimoto, K. Nomura, H. Nishiura, K. Ohdan, K. Ohdan, and H. Hayashi Novel transglucosylating reaction of sucrose phosphorylase to carboxylic compounds such as benzoic acid J Biosci Bioeng 104 2007 22 29 (Pubitemid 47223814)
74. K. Nomura, K. Sugimoto, H. Nishiura, K. Ohdan, T. Nishimura, and H. Hayashi Glucosylation of acetic acid by sucrose phosphorylase Biosci Biotechnol Biochem 72 2008 82 87 (Pubitemid 351158953)
75. 2 media Food Chem 115 2009 1028 1033
76. H. Chaen, K. Yamamoto, M. Nishimoto, T. Nakada, S. Fukuda, and H. Sugimoto Purification of a novel phosphorylase, kojibiose phosphorylase, from Thermoanaerobium brockii J Appl Glycosci 46 1999 423 429
77. E. Vazquez-Figueroa, V. Yeh, J.M. Broering, J.F. Chaparro-Riggers, and A.S. Bommarius Thermostable variants constructed via the structure-guided consensus method also show increased stability in salt solutions and homogeneous aqueous-organic media Protein Eng Des Sel 21 2008 673 680
78. T. Yamamoto, K. Mukai, H. Yamashita, M. Kubota, S. Fukuda, and M. Kurimoto Enhancement of thermostability of kojibiose phosphorylase from Thermoanaerobacter brockii ATCC35047 by random mutagenesis J Biosci Bioeng 100 2005 212 215 (Pubitemid 41558138)
79. K. Fujii, M. Liboshi, M. Yanase, T. Takaha, and T. Kuriki Enhancing the thermal stability of sucrose phosphorylase from Streptococcus mutans by random mutagenesis J Appl Glycosci 53 2006 91 97
80. A. Cerdobbel, K. De Winter, D. Aerts, R. Kuipers, H.J. Joosten, and W. Soetaert Increasing the thermostability of sucrose phosphorylase by a combination of sequence- and structure-based mutagenesis Protein Eng Des Sel 2011 10.1093/protein/gzr042
81. D. Sprogoe, L.A. van den Broek, O. Mirza, J.S. Kastrup, A.G. Voragen, and M. Gajhede Crystal structure of sucrose phosphorylase from Bifidobacterium adolescentis Biochemistry 43 2004 1156 1162 (Pubitemid 38176513)
82. L. Cao Immobilised enzymes: science or art? Curr Opin Chem Biol 9 2005 217 226 (Pubitemid 40462493)
83. M. Nishimoto, and M. Kitaoka Practical preparation of lacto-N-biose I, a candidate for the bifidus factor in human milk Biosci Biotechnol Biochem 71 2007 2101 2104 (Pubitemid 350113147)
84. T. Nihira, H. Nakai, K. Chiku, and M. Kitaoka Discovery of nigerose phosphorylase from Clostridium phytofermentans Appl Microbiol Biotechnol 2011 10.1007/s00253-011-3515-9
85. T. Senoura, S. Ito, H. Taguchi, M. Higa, S. Hamada, and H. Matsui New microbial mannan catabolic pathway that involves a novel mannosylglucose phosphorylase Biochem Biophys Res Commun 408 2011 701 706
86. Cerdobbel A. Engineering the thermostability of sucrose phosphorylase for industrial applications. PhD Thesis. Belgium: Ghent University; 2011.