Toward efficient enzymatic glycan synthesis: Directed evolution and enzyme engineering

Journal of Carbohydrate Chemistry

Volumn 30, Issue 4-6, 2011, Pages 181-205

  Kwan, David H ^a   Withers, Stephen G ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Directed evolution; Enzymatic synthesis; Enzyme engineering; Glycosidase; Glycosphingolipid; Glycosynthase; Glycosytransferase

Indexed keywords

EID: 84855778433     PISSN: 07328303     EISSN: 15322327     Source Type: Journal    
DOI: 10.1080/07328303.2011.604457     Document Type: Article

References (66)

1. Crocker, P. R.; Feizi, T. Carbohydrate recognition systems: functional triads in cell-cell interactions. Curr. Opin. Struct. Biol. 1996, 6, 679-691. (Pubitemid 26372346)
2. Hakomori, S. Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu. Rev. Biochem. 1981, 50, 733-764.
3. Weymouth-Wilson, A. C. The role of carbohydrates in biologically active natural products. Nat. Prod. Rep. 1997, 14, 99-110. (Pubitemid 27191082)
4. Paulsen, H. Progress in the selective chemical synthesis of complex oligosaccharides. Angew. Chem. 1982, 94, 184-201.
5. Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.; Bernard, T.; Lombard, V.; Henrissat, B. The Carbohydrate-Active EnZymes database (CAZy) : an expert resource for glycogenomics. Nucleic Acids Res. 2009, 37, D233-D238.
6. Luley-Goedl, C.; Nidetzky, B. Carbohydrate synthesis by disaccharide phosphorylases: reactions, catalytic mechanisms and application in the glycosciences. Biotechnol. J. 2010, 5, 1324-1338.
7. Nidetzky, B.; Griessler, R.; Schwarz, A.; Splechtna, B. Cellobiose phosphorylase from Cellulomonas uda: gene cloning and expression in Escherichia coli, and application of the recombinant enzyme in a 'glycosynthase-type' reaction. J. Mol. Catal. B Enzym. 2004, 29, 241-248. (Pubitemid 38624096)
8. Suzuki, M.; Kaneda, K.; Nakai, Y.; Kitaoka, M.; Taniguchi, H. Synthesis of cellobiose from starch by the successive actions of two phosphorylases. New Biotechnol. 2009, 26, 137-142.
9. Hiraishi, M.; Igarashi, K.; Kimura, S.; Wada, M.; Kitaoka, M.; Samejima, M. Synthesis of highly ordered cellulose II in vitro using cellodextrin phosphorylase. Carbohydr. Res. 2009, 344, 2468-2473.
10. Nishimoto, M.; Kitaoka, M. One-pot enzymatic production of β-D-galactopyranosyl-(1,3)-2-acetamido-2-deoxy-D-galactose (galacto-N-biose) from sucrose and 2-acetamido-2-deoxy-D-galactose (N-acetylgalactosamine). Carb. Res. 2009, 344, 2573-2576.
11. McCarter, J. D.; Withers, S. G. Mechanisms of enzymatic glycoside hydrolysis. Curr. Opin. Struct. Biol. 1994, 4, 885-892.
12. Zechel, D. L.; Withers, S. G. Dissection of nucleophilic and acid-base catalysis in glycosidases. Curr. Opin. Chem. Biol. 2001, 5, 643-649. (Pubitemid 33153160)
13. Lang, M.; Kamrat, T.; Nidetzky, B. Influence of ionic liquid cosolvent on transgalactosylation reactions catalyzed by thermostable β- glycosylhydrolase CelB from Pyrococcus furiosus. Biotechnol. Bioeng. 2006, 95, 1093-1100. (Pubitemid 44901324)
14. Yoon, J. H.; McKenzie, D. A comparison of the activities of three β-galactosidases in aqueous-organic solvent mixtures. Enzyme Microb. Technol. 2005, 36, 439-446. (Pubitemid 40186838)
15. Rakić, B.; Withers, S. G. Recent developments in glycoside synthesis with glycosynthases and thioglycoligases. Aust. J. Chem. 2009, 62, 510-520.
16. Shaikh, F. A.; Withers, S. G. Teaching old enzymes new tricks: engineering and evolution of glycosidases and glycosyl transferases for improved glycoside synthesis. Cell Biol. 2008, 86, 169-177. (Pubitemid 351536497)
17. Mackenzie, L. F.; Wang, Q.; Warren, R. A. J.; Withers, S. G. Glycosynthases: mutant glycosidases for oligosaccharide synthesis. J. Am. Chem. Soc. 1998, 120, 5583-5584.
18. Mayer, C.; Zechel, D. L.; Reid, S. P.; Warren, R. A.; Withers, S. G. The E358S mutant of Agrobacterium sp. β-glucosidase is a greatly improved glycosynthase. FEBS Lett. 2000, 466, 40-44. (Pubitemid 30050679)
19. Hancock, S. M.; Vaughan, M. D.; Withers, S. G. Engineering of glycosidases and glycosyltransferases. Curr. Opin. Chem. Biol. 2006, 10, 509-519. (Pubitemid 44375059)
20. Honda, Y.; Kitaoka, M. The first glycosynthase derived from an inverting glycoside hydrolase. J. Biol. Chem. 2006, 281, 1426-1431.
21. Honda, Y.; Fushinobu, S.; Hidaka, M.; Wakagi, T.; Shoun, H.; Taniguchi, H.; Kitaoka, M. Alternative strategy for converting an inverting glycoside hydrolase into a glycosynthase. Glycobiology 2008, 18, 325-330. (Pubitemid 351461065)
22. Wada, J.; Honda, Y.; Nagae, M.; Kato, R.; Wakatsuki, S.; Katayama, T.; Taniguchi, H.; Kumagai, H.; Kitaoka, M.; Yamamoto, K. 1, 2-α-L- fucosynthase: a glycosynthase derived from an inverting α-glycosidase with an unusual reaction mechanism. FEBS Lett. 2008, 582, 3739-3743.
23. Hidaka, M.; Fushinobu, S.; Honda, Y.; Wakagi, T.; Shoun, H.; Kitaoka, M. Structural explanation for the acquisition of glycosynthase activity. J. Biochem. 2010, 147, 237-244.
24. Hehre, E. J.; Brewer, C. F.; Genghof, D. S. Scope and mechanism of carbohydrase action. Hydrolytic and nonhydrolytic actions of β-amylase on α-and β-maltosyl fluoride. J. Biol. Chem. 1979, 254, 5942-5960.
25. Jahn, M.; Marles, J.; Warren, R. A.; Withers, S. G. Thioglycoligases: mutant glycosidases for thioglycoside synthesis. Angew. Chem. Int. Ed. Engl. 2003, 42, 352-354. (Pubitemid 36176322)
26. Müllegger, J.; Jahn, M.; Chen, H.-M.; Warren, R. A.; Withers, S. G. Engineering of a thioglycoligase: randomized mutagenesis of the acid-base residue leads to the identification of improved catalysts. Protein Eng. Des. Sel. 2005, 18, 33-40. (Pubitemid 40516989)
27. Kim, Y. W.; Lovering, A. L.; Chen, H.; Kantner, T.; McIntosh, L. P.; Strynadka, N. C.; Withers, S. G. Expanding the thioglycoligase strategy to the synthesis of α-linked thioglycosides allows structural investigation of the parent enzyme/substrate complex. J. Am. Chem. Soc. 2006, 128, 2202-2203.
28. Kim, Y. W.; Chen, H.; Kim, J. H.; Withers, S. G. Catalytic properties of a mutant β-galactosidase from Xanthomonas manihotis engineered to synthesize galactosyl-thio-β-1, 3 and-β-1, 4-glycosides. FEBS Lett. 2006, 580, 4377-4381. (Pubitemid 44118252)
29. Müllegger, J.; Chen, H.-M.; Warren, R. A.; Withers, S. G. Glycosylation of a neoglycoprotein by using glycosynthase and thioglycoligase approaches: the generation of a thioglycoprotein. Angew. Chem. Int. Ed. Engl. 2006, 45, 2585-2588. (Pubitemid 44105766)
30. Kim, Y. W.; Chen, H.-M.; Kim, J. H.; Müllegger, J.; Mahuran, D.; Withers, S. G. Thioglycoligase-based assembly of thiodisaccharides: Screening as β-galactosidase inhibitors. ChemBioChem 2007, 8, 1495-1499. (Pubitemid 47436904)
31. Armstrong, Z.; Reitinger, S.; Kantner, T.; Withers, S. G. Enzymatic thioxyloside synthesis: characterization of thioglycoligase variants identified from a site-saturation mutagenesis library of Bacillus circulans xylanase. ChemBioChem 2010, 11, 533-538.
32. Jahn, M.; Chen, H.; Müllegger, J.; Marles, J.; Warren, R. A.; Withers, S. G. Thioglycosynthases: double mutant glycosidases that serve as scaffolds for thioglycoside synthesis. Chem. Commun. 2004, 274-275. (Pubitemid 38249185)
33. Kim, Y. W.; Zhang, R.; Chen, H.; Withers, S. G. O-glycoligases, a new category of glycoside bond-forming mutant glycosidases, catalyse facile syntheses of isoprimeverosides. Chem. Commun. 2010, 8725-8727.
34. Arnold, F. H.; Volkov, A. A. Directed evolution of biocatalysts. Curr. Opin. Chem. Biol. 1999, 3, 54-59. (Pubitemid 29118980)
35. Arnold, F. H. Combinatorial and computational challenges for biocatalyst design. Nature 2001, 409, 253-257. (Pubitemid 32144295)
36. Kittl, R.; Withers, S. G. New approaches to enzymatic glycoside synthesis through directed evolution. Carb. Res. 2010, 345, 1272-1279.
37. Koné, F. M.; Le Béchec, M.; Sine, J. P.; Dion, M.; Tellier, C. Digital screening methodology for the directed evolution of transglycosidases. Protein Eng. Des. Sel. 2009, 22, 37-44.
38. Mayer, C.; Jakeman, D. L.; Mah, M.; Karjala, G.; Gal, L.; Warren, R. A. J.; Withers, S. G. Directed evolution of new glycosynthases from Agrobacterium β-glucosidase: a general screen to detect enzymes for oligosaccharide synthesis. Chem. Biol. 2001, 8, 437-443. (Pubitemid 32455898)
39. Kim, Y.-W.; Lee, S. S.; Warren, R. A. J.; Withers, S. G. Directed evolution of a glycosynthase from Agrobacterium sp. increases its catalytic activity dramatically and expands its substrate repertoire. J. Biol. Chem. 2004, 279(41), 42787-42793. (Pubitemid 39372166)
40. Kempton, J. B.; Withers, S. G. Mechanism of Agrobacterium β-glucosidase: kinetic studies. Biochemistry 1992, 31, 9961-9969.
41. Kwan, D. H.; Chen, H.-M.; Ratananikom, H.; Hancock, S. M.; Watanabe, Y.; Kongsaeree, P. T.; Samuels, A. L.; Withers, S. G. Self-immobilizing fluorogenic imaging agents of enzyme activity. Angew. Chem. Int. Ed. Engl. 2011, 50, 300-303.
42. Yang, G.; Withers, S. G. Ultrahigh-throughput FACS-based screening for directed enzyme evolution. ChemBioChem 2009, 10, 2704-2715.
43. Hancock, S. M.; Tarling, C. A.; Withers, S. G. High-throughput screening of cell lysates for ganglioside synthesis. Anal. Biochem. 2008, 382, 48-54.
44. Hoetzl, S.; Sprong, H.; van Meer, G. The way we view cellular (glyco) sphingolipids. J. Neurochem. 2007, 103, 3-13.
45. Mishra, S.; Joshi, P. G. Lipid raft heterogeneity: an enigma. J. Neurochem. 2007, 103, 135-142.
46. Wyman, M. P.; Schneiter, R. Lipid signalling in disease. Nat. Rev. Mol. Cell Biol. 2008, 9, 162-176. (Pubitemid 351158917)
47. De Rosa, M.; Park, H.-J.; Myvaganum, M.; Binnington, B.; Lund, N.; Branch, D. R.; Lingwood, C. A. The medium is the message: glycosphingolipids and their soluble analogues. Biochim. Biophys. Acta. 2008, 1780, 347-352.
48. Ito, M.; Yamagata, T. A novel glycosphingolipid-degrading enzyme cleaves the linkage between the oligosaccharide and ceramide of neutral and acidic glycosphingolipids. J. Biol. Chem. 1986, 261, 14278-14282. (Pubitemid 17196338)
49. Hancock, S. M.; Rich, J. R.; Caines, M. E.; Strynadka, N. C.; Withers, S. G. Designer enzymes for glycosphingolipid synthesis by directed evolution. Nat. Chem. Biol. 2009, 5, 508-514.
50. Baker, K.; Bleczinski, C.; Lin, H.; Salazar-Jimenez, G.; Sengupta, D.; Krane, S.; Cornish, V. W. Chemical complementation: a reaction-independent genetic assay for enzyme catalysis. Proc. Natl. Acad. Sci. USA 2002, 99, 16537-16542. (Pubitemid 36034008)
51. Lin, H.; Tao, H.; Cornish, V. W. Directed evolution of a glycosynthase via chemical complementation. J. Am. Chem. Soc. 2004, 126, 15051-15059. (Pubitemid 39557264)
52. Lin, H.; Abida, W. M.; Sauer, R. T.; Cornish, V. W. Dexamethasone- methotrexate: an efficient chemical inducer of protein dimerization in vivo. J. Am. Chem. Soc. 2000, 122, 4247-4248. (Pubitemid 30304874)
53. Ben-David, A.; Shoham, G.; Shoham, Y. A universal screening assay for glycosynthases: directed evolution of glycosynthase XynB2 (E335G) suggests a general path to enhance activity. Chem. Biol. 2008, 15, 546-551. (Pubitemid 351815055)
54. Ben-David, A.; Bravman, T.; Balazs, Y. S.; Czjzek, M.; Schomburg, D.; Shoham, G.; Shoham, Y. Glycosynthase activity of Geobacillus stearothermophilus GH52 β-xylosidase: efficient synthesis of xylooligosaccharides from α-D-xylopyranosyl fluoride through a conjugated reaction. ChemBioChem 2007, 8, 2145-2151. (Pubitemid 350220766)
55. Williams, G. J.; Zhang, C.; Thorson, J. S. Expanding the promiscuity of a naturalproduct glycosyltransferase by directed evolution. Nat. Chem. Biol. 2007, 3, 657-662. (Pubitemid 47417707)
56. Salas, M.; Méndez, C. Engineering the glycosylation of natural products in actinomycetes. Trends Microbiol. 2007, 15, 219-232. (Pubitemid 46660603)
57. Griffith, B. R.; Langenhan, J. M.; Thorson, J. S. 'Sweetening' natural products via glycorandomization. Curr. Opin. Biotechnol. 2005, 16, 622-630. (Pubitemid 41654640)
58. Yang, M.; Proctor, M. R.; Bolam, D. N.; Errey, J. C.; Field, R. A.; Gilbert, H. J.; Davis, B. G. Probing the breadth of macrolide glycosyltransferases: in vitro remodeling of a polyketide antibiotic creates active bacterial uptake and enhances potency. J. Am. Chem. Soc. 2005, 127, 9336-9337. (Pubitemid 40934725)
59. Collier, A. C.; Tingle, M. D.; Keelan, J. A.; Paxton, J. W.; Mitchell, M. D. A highly sensitive fluorescent microplate method for the determination of UDP-glucuronosyl transferase activity in tissues and placental cell lines. Drug Metab. Dispos. 2000, 28, 1184-1186.
60. Aharoni, A.; Thieme, K.; Chiu, C. P. C.; Buchini, S.; Lairson, L. L.; Chen, H.; Strynadka, N. C. J.; Wakarchuk, W. W.; Withers, S. G. High-throughput screening methodology for the directed evolution of glycosyltransferases. Nat. Methods 2006, 3, 609-614. (Pubitemid 44123427)
61. Harduin-Lepers, A.; Vallejo-Ruiz, V.; Krzewinski-Recchi, M. A.; Samyn-Petit, B.; Julien, S.; Delannoy, P. The human sialyltransferase family. Biochimie 2001, 83, 727-737. (Pubitemid 32821237)
62. Chiu, C. P.; Watts, A. G.; Lairson, L. L.; Gilbert, M.; Lim, D.; Wakarchuk, W. W.; Withers, S. G.; Strynadka, N. C. Structural analysis of the sialyltransferase CstII from Campylobacter jejuni in complex with a substrate analog. Nat. Struct. Mol. Biol. 2004, 11, 163-170. (Pubitemid 38146520)
63. Audry, M.; Jeanneau, C.; Imberty, A.; Harduin-Lepers, A.; Delannoy, P.; Breton, C. Current trends in the structure-activity relationships of sialyltransferases. Glycobiology 2011, 21, 716-726.
64. Schmidt-Dannert, C.; Arnold, F. H. Directed evolution of industrial enzymes. Trends Biotechnol. 1999, 17, 135-136. (Pubitemid 29273942)
65. Yang, G.; Rich, J. R.; Gilbert, M.; Wakarchuk, W. W.; Feng, Y.; Withers, S. G. Fluorescence activated cell sorting as a general ultra-high-throughput screening method for directed evolution of glycosyltransferases. J. Am. Chem. Soc. 2010, 132, 10570-10577.
66. 13C NMR analysis. J. Biol. Chem. 2000, 27, 3896-3906. (Pubitemid 30094614)