Semi-rational approach for converting a GH36 α-glycosidase into an α-transglycosidase

Glycobiology

Volumn 25, Issue 4, 2015, Pages 420-427

  Teze, David ^a   Daligault, Franck ^a   Ferrières, Vincent ^b,c   Sanejouand, Yves Henri ^a   Tellier, Charles ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b UNIV RENNES   (France)

^c UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

Author keywords

evolution; glycosidase; mutagenesis; oligosaccharide; transglycosylation

Indexed keywords

ALPHA GALACTOSIDASE; ALPHA GLYCOSIDASE; ALPHA TRANSGLYCOSIDASE; AMINO ACID; GLYCOSIDASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; DISACCHARIDE;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; GEOBACILLUS STEAROTHERMOPHILUS; GLYCOSYLATION; HYDROLYSIS; KINETIC PARAMETERS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; RATE CONSTANT; SITE DIRECTED MUTAGENESIS; SUBSTRATE CONCENTRATION; SYNTHESIS; AMINO ACID SUBSTITUTION; BIOCATALYSIS; CHEMISTRY; CONFORMATION; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; KINETICS;

ALPHA-GALACTOSIDASE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BIOCATALYSIS; CARBOHYDRATE CONFORMATION; CATALYTIC DOMAIN; DISACCHARIDES; GEOBACILLUS STEAROTHERMOPHILUS; GLYCOSYLATION; KINETICS; MUTAGENESIS, SITE-DIRECTED;

EID: 84941133159     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwu124     Document Type: Article

References (52)

1. Andersen JM, Barrangou R, Abou HachemM, Lahtinen SJ, Goh YJ, Svensson B, Klaenhammer TR. 2013. Transcriptional analysis of oligosaccharide utilization by Bifidobacterium lactis Bl-04. BMC Genomics. 14:312.
2. Andre C, Spangenberg P, Rabiller C. 2001. In Situ 19 F NMR spectroscopy study of enzymatic transglycosylation reactions using-D-aldohexopyranosyl fluorides as donors and acceptors. Tetrahedron Asymmetry. 12:779-783.
3. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro F, Gasteiger E, Huang H, Lopez R, Magrane M, et al. 2004. UniProt: The universal protein knowledgebase. Nucleic Acids Res. 32(Database issue): D115-D119.
4. Astronomo RD, Burton DR. 2010. Carbohydrate vaccines: Developing sweet solutions to sticky situations? Nat Rev Drug Discov. 9:308-324.
5. Bobrov KS, Borisova AS, Eneyskaya EV, Ivanen DR, Shabalin KA, Kulminskaya AA, Rychkov GN. 2013. Improvement of the efficiency of transglycosylation catalyzed by ? galactosidase from Thermotoga maritima by protein engineering. Biochemistry (Moscow). 78:1112-1123.
6. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 2009. The Carbohydrate-Active EnZymes Database (CAZy): An expert resource for glycogenomics. Nucleic Acids Res. 37(Database issue): D233-D238.
7. Cervera-Tison M, Tailford LE, Fuell C, Bruel L, Sulzenbacher G, Henrissat B, Berrin JG, Fons M, Giardina T, Juge N. 2012. Functional analysis of family GH36-galactosidases from Ruminococcus gnavus E1: Insights into the metabolism of a plant oligosaccharide by a human gut symbiont. Appl Environ Microbiol. 78:7720-7732.
8. Champion E, Andre I, Moulis C, Boutet J, Descroix K, Morel S, Monsan P, Mulard LA, Remaud-Simeon M. 2009. Design of-transglucosidases of controlled specificity for programmed chemoenzymatic synthesis of antigenic oligosaccharides. J Am Chem Soc. 131:7379-7389.
9. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. 2003. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31:3497-3500.
10. Cobucci-Ponzano B, Perugino G, Strazzulli A, Moracci M. 2012. Thermophilic glycosynthases for oligosaccharides synthesis. In: Cellulases. 1st ed. Vol. 510. Elsevier Inc.
11. Cobucci-Ponzano B, Zorzetti AC, Strazzulli SC, Bedini E, Corsaro MM, Comfort DA, Kelly RM, Rossi M, Moracci M. 2010. A Novel a-Dgalactosynthase from Thermotoga Maritima converts-D-galactopyranosyl azide to-galacto-oligosaccharides. Glycobiology. 21:448-456.
12. D'Almeida A, Ionata M, Tran V, Tellier C, Dion M, Rabiller C. 2009. An expeditious and efficient synthesis of-D-galactopyranosyl-(1-3)-D-Nacetylglucosamine (lacto-N-biose) using a glycosynthase from Thermus Thermophilus as a catalyst. Tetrahedron Asymmetry. 20:1243-1246.
13. Dion M, Nisole A, Spangenberg P, Andre C, Glottin-fleury A, Mattes R, Tellier C, Rabiller C. 2001. Modulation of the regioselectivity of a Bacillus alpha-galactosidase by directed evolution. Glycoconjugate J. 18:215-223.
14. Dion M, Osanjo G, Andre C, Spangenberg P, Rabiller C, Tellier C. 2001. Identification by saturation mutagenesis of a single residue involved in the-galactosidase AgaB regioselectivity. Glycoconjugate J. 18:457-464.
15. Feng HY, Drone J, Hoffmann L, Tran V, Tellier C, Rabiller C, Dion M. 2005. Converting a-glycosidase into a-transglycosidase by directed evolution. J Biol Chem. 280:37088-37097.
16. Fredslund F, Hachem MA, Larsen RJ, Sørensen PG, Coutinho PM, Leggio LL, Svensson B. 2011. Crystal structure of-galactosidase from Lactobacillus acidophilus NCFM insight into tetramer formation and substrate binding. J Mol Biol. 412:466-480.
17. Gantt RW, Peltier-Pain P, Singh S, Zhou M, Thorson JS. 2013. Broadening the scope of glycosyltransferase-catalyzed sugar nucleotide synthesis. Proc Natl Acad Sci USA. 110:7648-7653.
18. Ghazarian H, Idoni B, Oppenheimer SB. 2011. A glycobiology review: Carbohydrates, lectins and implications in cancer therapeutics. Acta Histochem. 113:236-247.
19. Hachem MA, Fredslund F, Andersen JM, Larsen RJ, Majumder A, Ejby M, Van Zanten G, Lahtinen SJ, Barrangou R, Klaenhammer TR, et al. 2012. Raffinose family oligosaccharide utilisation by probiotic bacteria: Insight into substrate recognition, molecular architecture and diversity of GH36-galactosidases. Biocatal Biotransform. 30:316-325.
20. Hart GW, Copeland RJ. 2010. Essay glycomics hits the big time. Cell. 143: 672-676.
21. Hehre EJ, Brewer CF, Genghof DS. 1979. Scope and mechanism of carbohydrase action. Hydrolytic and nonhydrolytic actions of beta-amylase on alpha-and beta-maltosyl fluoride. J Biol Chem. 254:5942-5950.
22. Honda Y, Fushinobu S, Hidaka M, Wakagi T, Shoun H, Taniguchi H, Kitaoka M. 2008. Alternative strategy for converting an inverting glycoside hydrolase into a glycosynthase. Glycobiology. 18:325-330.
23. Honda Y, Kitaoka M. 2006. The first glycosynthase derived from an inverting glycoside hydrolase. J Biol Chem. 281:1426-1431.
24. Irague R, Massou S, Moulis C, Saurel O, Milon A, Monsan P, Remaud-Simeon M, Portais JC, Potocki-Veronese G. 2011. NMR-based structural glycomics for high-throughput screening of carbohydrate-active enzyme specificity. Anal Chem. 83:1202-1206.
25. Kelly RM, Leemhuis H, Rozeboom HJ, van Oosterwijk N, Dijkstra BW, Dijkhuizen L. 2008. Elimination of competing hydrolysis and coupling side reactions of a cyclodextrin glucanotransferase by directed evolution. Biochem J. 413:517-525.
26. Koné FMT, Le Béchec M, Sine JP, Dion M, Tellier C. 2009. Digital screening methodology for the directed evolution of transglycosidases. Protein Eng Des Sel. 22:37-44.
27. Lairson LL, Henrissat B, Davies GJ, Withers SG. 2008. Glycosyltransferases: Structures, functions, and mechanisms. Annu Rev Biochem. 77:521-555.
28. Leemhuis H, Dijkstra BW, Dijkhuizen L. 2002. Mutations converting cyclodextrin glycosyltransferase from a transglycosylase into a starch hydrolase. FEBS Lett. 514:189-192.
29. Lichtenstein RG, Rabinovich GA. 2013. Glycobiology of cell death: When glycans and lectins govern cell fate. Cell Death Differ. 2869:1-11.
30. Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42:D490-D495.
31. Macher BA, Galili U. 2008. The Gal1, 3Gal1, 4GlcNAc-R (-Gal) epitope: A carbohydrate of unique evolution and clinical relevance. Biochim Biophys Acta. 1780:75-88.
32. Mackenzie LF, Wang Q, Warren RAJ, Withers SG. 1998. Glycosynthases: Mutant glycosidases for oligosaccharide synthesis. J Am Chem Soc. 120: 5583-5584.
33. Malet C, Planas A. 1998. From-glucanase to-glucansynthae: Glycosyl transfer to-glycosyl fluorides catalyzed by a mutant endoglucanase lacking its catalytic nucleophile. FEBS Lett. 440:208-212.
34. Marton Z, Tran V, Tellier C, Dion M, Drone J, Rabiller C. 2008. Engineering of glucoside acceptors for the regioselective synthesis of-(1->3)-disaccharides with glycosynthases. Carbohydr Res. 343:2939-2946.
35. Merceron R, Foucault M, Haser R, Mattes R, Watzlawick H, Gouet P. 2012. The molecular mechanism of thermostable-galactosidases AgaA and AgaB explained by X-ray crystallography and mutational studies. J Biol Chem. 287:39642-39652.
36. Nakai H, Baumann M, Petersen B, Westpha Y, Hachem M, Dilokpimol A, Duus JØ, Schols HA, Svensson B. 2010. Aspergillus nidulans-galactosidase of glycoside hydrolase family 36 catalyses the formation of galactooligosaccharides by transglycosylation. FEBS J. 277:3538-3551.
37. Osanjo G, Dion M, Drone J, Solleux C, Tran V, Rabiller C, Tellier C. 2007. Directed evolution of the alpha-L-fucosidase from Thermotoga maritima into an-L-transfucosidase. Biochemistry. 46:1022-1033.
38. Peterbauer T, Karner U, Mucha J, Mach L, Jones DA, Hedley CL, Richter A. 2003. Enzymatic control of the accumulation of verbascose in pea seeds. Plant Cell Environ. 26:1385-1391.
39. Peterbauer T, Mach L, Mucha J, Richter A. 2002. Functional expression of a cDNA encoding pea (Pisum Sativum L.) Raffinose synthase, partial purification of the enzyme from maturing seeds, and steady-state kinetic analysis of raffinose synthesis. Planta. 215:839-846.
40. Peterbauer T, Mucha J, Mach L, Richter A. 2002. Chain elongation of raffinose in pea seeds. Isolation, characterization, and molecular cloning of mutifunctional enzyme catalyzing the synthesis of stachyose and verbascose. J Biol Chem. 277:194-200.
41. Pizzut-Serin S, Potocki-Veronese G, Van Der Veen BA, Albenne C, Monsan P, Remaud-Simeon M. 2005. Characterisation of a novel amylosucrase from Deinococcus radiodurans. FEBS Lett. 579:1405-1410.
42. Plou FJ, Segura AG, Ballesteros A. 2007. Application of glycosidases and transglycosidases in the synthesis of oligosaccharides. In Polaina J, MacCabe AP, editors. Industrial enzymes: structure, function and application. New York (NY): Springer
43. Spangenberg P, Andre C, Dion M, Rabiller C, Mattes R. 2000. Comparative study of new a-galactosidases in transglycosylation reactions. Carbohydr Res. 329:65-73.
44. Teze D, Dion M, Daligault F, Tran V, André-Miral C, Tellier C. 2013. Alkoxyamino glycoside acceptors for the regioselective synthesis of oligosaccharides using glycosynthases and transglycosidases. Bioorg Med Chem Lett. 23:448-451.
45. Teze D, Hendrickx J, Czjzek M, Ropartz D, Sanejouand YH, Tran V, Tellier C, Dion M. 2014. Semi-rational approach for converting a GH1-glycosidase into a-transglycosidase. Protein Eng Des Sel. 27:13-19.
46. Teze D, Hendrickx J, Dion M, Tellier C, Woods VL, Tran V, Sanejouand YH. 2013. Conserved water molecules in family 1 glycosidases: A DXMS and molecular dynamics study. Biochemistry. 52:5900-5910.
47. Wada J, Honda Y, Nagae M, Kato R, Wakatsuki S, Katayama T, Taniguchi H, Kumagai H, Kitaoka M, Yamamoto K. 2008. 1, 2-alpha-L-fucosynthase: A glycosynthase derived from an inverting alpha-glycosidase with an unusual reaction mechanism. FEBS Lett. 582(27):3739-3743.
48. Wang Q, Graham RW, Trimbur D, Warren RAJ, Withers SG. 1994. Changing enzymatic reaction mechanisms by mutagenesis: Converting a retaining glucosidase to an inverting enzyme. J Am Chem Soc. 116:11594-11595.
49. Wang CC, Lee JC, Luo SY, Kulkarni SS, Huang YW, Lee CC. 2007. Regioselective one-pot protection of carbohydrates. Nature. 446: 896-899.
50. Wang H, Ma R, Shi P, Xue X, Luo H, Huang H, Bai Y, Yang P, Yao B. 2014. A New-galactosidase from Thermoacidophilic alicyclobacillus sp. A4 with wide acceptor specificity for transglycosylation. Appl Biochem Biotechnol 174:328-338.
51. Zhang C, Griffith BR, Fu Q, Albermann C, Fu X, Lee IK, Li L, Thorson JS. 2006. Exploiting the reversibility of natural product glycosyltransferasecatalysed reactions. Science. 313:1291-1294.
52. Zhu X, Schmidt RR. 2009. New principles for glycoside-bond formation. Angew Chem Int Ed. 48:1900-1934.