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Applied Microbiology and Biotechnology

, Volume 100, Issue 10, pp 4269–4281 | Cite as

Recent developments in the enzymatic O-glycosylation of flavonoids

  • Bernd HoferEmail author
Mini-Review

Abstract

The glycosylation of bioactive compounds, such as flavonoids, is of particular relevance, as it modulates many of their pharmacokinetic parameters. This article reviews the literature between 2010 and the end of 2015 that deals with the enzymatic O-glycosylation of this class of compounds. Enzymes of glycosyltransferase family 1 remain the biocatalysts of choice for glycodiversification of flavonoids, in spite of relatively low yields. Transfers of 14 different sugars, in addition to glucose, were reported. Several Escherichia coli strains were metabolically engineered to enable a (more efficient) synthesis of the required donor during in vivo glycosylations. For the transfer of glucose, enzymes of glycoside hydrolase families 13 and 70 were successfully assayed with several flavonoids. The number of acceptor substrates and of regiospecificities characterized so far is smaller than for glycosyltransferases. However, their glycosyl donors are much cheaper and yields are considerably higher. A few success stories of enzyme engineering were reported. These improved the catalytic efficiency as well as donor, acceptor, or product ranges. Currently, the development of appropriate high-throughput screening systems appears to be the major bottleneck for this powerful technology.

Keywords

Flavonoid Glycosylation Glycosyltransferase Glycoside hydrolase 

Notes

Acknowledgments

The author thanks the Bundesministerium für Forschung und Technologie for repeated funding of the work carried out in his laboratory.

Compliance with ethical standards

Conflict of interest

The author declares that he has no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by the author.

Supplementary material

253_2016_7465_MOESM1_ESM.pdf (143 kb)
ESM 1 (PDF 143 kb)

References

  1. Aramsangtienchai P, Chavasiri W, Ito K, Pongsawasdi P (2011) Synthesis of epicatechin glucosides by a β-cyclodextrin glycosyltransferase. J Mol Catal B-Enzym 73:27–34CrossRefGoogle Scholar
  2. Cao H, Chen X, Jassbi AR, Xiao J (2015) Microbial biotransformation of bioactive flavonoids. Biotechnol Adv 33:214–223CrossRefPubMedGoogle Scholar
  3. Chang A, Singh S, Phillips GN Jr, Thorson JS (2011) Glycosyltransferase structural biology and its role in the design of catalysts for glycosylation. Curr Opin Biotechnol 22:800–808CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cho H-K, Kim H-H, Seo D-H, Jung J-H, Park J-H, Baek N-I, Kim M-J, Yoo S-H, Cha J, Kim Y-R, Park C-S (2011) Biosynthesis of (+)-catechin glycosides using recombinant amylosucrase from Deinococcus geothermalis DSM 11300. Enzyme Microb Technol 49:246–253CrossRefPubMedGoogle Scholar
  5. Choi SH, Ryu M, Yoon YJ, Kim DM, Lee EY (2012) Glycosylation of various flavonoids by recombinant oleandomycin glycosyltransferase from Streptomyces antibioticus in batch and repeated batch modes. Biotechnol Lett 34:499–505CrossRefPubMedGoogle Scholar
  6. Cushnie TP, Lamb AJ (2011) Recent advances in understanding the antibacterial properties of flavonoids. Int J Antimicrob Agent 38:99–107CrossRefGoogle Scholar
  7. Das SS, Gauri SS, Misra BB, Biswas M, Dey S (2013) Purification and characterization of a betanidin glucosyltransferase from Amaranthus tricolor L catalyzing non-specific biotransformation of flavonoids. Plant Sci 211:61–69CrossRefPubMedGoogle Scholar
  8. De Bruyn F, Van Brempt M, Maertens J, Van Bellegem W, Duchi D, De Mey M (2015) Metabolic engineering of Escherichia coli into a versatile glycosylation platform: production of bio-active quercetin glycosides. Microb Cell Factories 14:138CrossRefGoogle Scholar
  9. Durga M, Nathiya S, Devasena T (2014) Immunomodulatory and antioxidant actions of dietary flavonoids. Int J Pharm Pharm Sci 6:50–56Google Scholar
  10. Funaki A, Waki T, Noguchi A, Kawai Y, Yamashita S, Takahashi S, Nakayama T (2015) Identification of a highly specific isoflavone 7-O-glucosyltransferase in the soybean (Glycine max (L.) Merr.). Plant Cell Physiol 56:1512–1520CrossRefPubMedGoogle Scholar
  11. Gantt RW, Peltier-Pain P, Cournoyer WJ, Thorson JS (2011) Using simple donors to drive the equilibria of glycosyltransferase-catalyzed reactions. Nat Chem Biol 7:685–691CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gosch C, Flachowsky H, Halbwirth H, Thill J, Mjka-Wittmann R, Treutter D, Richter K, Hanke M-V, Stich K (2012) Substrate specificity and contribution of the glycosyltransferase UGT71A15 to phloridzin biosynthesis. Trees-Struct Funct 26:259–271CrossRefGoogle Scholar
  13. Gurung RB, Kim EH, Oh TJ, Sohng JK (2013) Enzymatic synthesis of apigenin glucosides by glucosyltransferase (YjiC) from Bacillus licheniformis DSM 13. Mol Cells 36:355–361CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gutmann A, Bungaruang L, Weber H, Leypold M, Breinbauer R, Nidetzky B (2014) Towards the synthesis of glycosylated dihydrochalcone natural products using glycosyltransferase-catalysed cascade reactions. Green Chem 16:4417–4425CrossRefGoogle Scholar
  15. Hall D, Kim KH, De Luca V (2011) Molecular cloning and biochemical characterization of three Concord grape (Vitis labrusca) flavonol 7-O-glucosyltransferases. Planta 234:1201–1214CrossRefPubMedGoogle Scholar
  16. Hall D, Yuan XX, Murata J, De Luca V (2012) Molecular cloning and biochemical characterization of the UDP-glucose: flavonoid 3-O-glucosyltransferase from Concord grape (Vitis labrusca). Phytochemistry 74:90–99CrossRefPubMedGoogle Scholar
  17. Han SH, Kim BG, Yoon JA, Chong Y, Ahn JH (2014) Synthesis of flavonoid O-pentosides by Escherichia coli through engineering of nucleotide sugar pathways and glycosyltransferase. Appl Environ Microbiol 80:2754–2762CrossRefPubMedPubMedCentralGoogle Scholar
  18. He F, Chen WK, Yu KJ, Ji XN, Duan CQ, Reeves MJ, Wang J (2015) Molecular and biochemical characterization of the UDP-glucose: anthocyanin 5-O-glucosyltransferase from Vitis amurensis. Phytochemistry 117:363–372CrossRefPubMedGoogle Scholar
  19. Hellmuth H, Wittrock S, Kralj S, Dijkhuizen L, Hofer B, Seibel J (2008) Engineering the glucansucrase GtfR enzyme reaction and glycosidic bond specificity: toward tailor-made polymer and oligosaccharide products. Biochemistry 47:6678–6684CrossRefPubMedGoogle Scholar
  20. Hiromoto T, Honjo E, Tamada T, Noda N, Kazuma K, Suzuki M, Kuroki R (2013) Crystal structure of UDP-glucose:anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. J Synchrotron Radiat 20:894–898CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hiromoto T, Honjo E, Noda N, Tamada T, Kazuma K, Suzuki M, Blaber M, Kuroki R (2015) Structural basis for acceptor-substrate recognition of UDP-glucose: anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. Protein Sci 24:395–407CrossRefPubMedPubMedCentralGoogle Scholar
  22. Iwakiri T, Mase S, Murakami T, Matsumoto M, Hamada H, Nakayama T, Ozaki S-I (2013) Glucosylation of hydroxyflavones by glucosyltransferases from Phytolacca americana. J Mol Catal B-Enzym 90:61–65CrossRefGoogle Scholar
  23. Jung NR, Joe EJ, Kim B-G, Ahn BC, Park JC, Chong Y, Ahn J-H (2010) Change of Bacillus cereus flavonoid O-triglucosyltransferase into flavonoid O-monoglucosyltransferase by error-prone polymerase chain reaction. J Microbiol Biotechnol 20:1393–1396CrossRefPubMedGoogle Scholar
  24. Kim B-G, Jung NR, Joe EJ, Hur H-G, Lim Y, Chong Y, Ahn J-H (2010a) Bacterial synthesis of a flavonoid deoxyaminosugar conjugate in Escherichia coli expressing a glycosyltransferase of Arabidopsis thaliana. ChemBioChem 11:2389–2392CrossRefPubMedGoogle Scholar
  25. Kim B-G, Kim HJ, Ahn J-H (2012a) Production of bioactive flavonol rhamnosides by expression of plant genes in Escherichia coli. J Agric Food Chem 60:11143–11148CrossRefPubMedGoogle Scholar
  26. Kim B-G, Sung SH, Ahn J-H (2012b) Biological synthesis of quercetin 3-O-N-acetylglucosamine conjugate using engineered Escherichia coli expressing UGT78D2. Appl Microbiol Biotechnol 93:2447–2453CrossRefPubMedGoogle Scholar
  27. Kim B-G, Sung SH, Jung NR, Chong Y, Ahn J-H (2010b) Biological synthesis of isorhamnetin 3-O-glucoside using engineered glucosyltransferase. J Mol Catal B-Enzym 63:194–199CrossRefGoogle Scholar
  28. Kim B-G, Yang SM, Kim SY, Cha MN, Ahn J-H (2015a) Biosynthesis and production of glycosylated flavonoids in Escherichia coli: current state and perspectives. Appl Microbiol Biotechnol 99:2979–2988CrossRefPubMedGoogle Scholar
  29. Kim HJ, Kim B-G, Ahn J-H (2013a) Regioselective synthesis of flavonoid bisglycosides using Escherichia coli harboring two glycosyltransferases. Appl Microbiol Biotechnol 97:5275–5282CrossRefPubMedGoogle Scholar
  30. Kim HS, Kim B-G, Sung S, Kim M, Mok H, Chong Y, Ahn J-H (2013b) Engineering flavonoid glycosyltransferases for enhanced catalytic efficiency and extended sugar-donor selectivity. Planta 238:683–693CrossRefPubMedGoogle Scholar
  31. Kim KH, Park Y-D, Park H, Moon K-O, Ha K-T, Baek N-I, Park C-S, Joo M, Cha J (2014) Synthesis and biological evaluation of a novel baicalein glycoside as an anti-inflammatory agent. Eur J Pharmacol 744:147–156CrossRefPubMedGoogle Scholar
  32. Kim SY, Lee HR, Park K-S, Kim B-G, Ahn J-H (2015b) Metabolic engineering of Escherichia coli for the biosynthesis of flavonoid-O-glucuronides and flavonoid-O-galactoside. Appl Microbiol Biotechnol 99:2233–2242CrossRefPubMedGoogle Scholar
  33. Koirala N, Pandey RP, Parajuli P, Jung HJ, Sohng JK (2014a) Methylation and subsequent glycosylation of 7,8-dihydroxyflavone. J Biotechnol 184:128–137Google Scholar
  34. Koirala N, Pandey RP, Thang DV, Jung HJ, Sohng JK (2014b) Glycosylation and subsequent malonylation of isoflavonoids in E. coli: strain development, production and insights into future metabolic perspectives. J Ind Microbiol Biotechnol 41:1647–1658CrossRefPubMedGoogle Scholar
  35. Kovinich N, Saleem A, Arnason JT, Miki B (2010) Functional characterization of a UDP-glucose: flavonoid 3-O-glucosyltransferase from the seed coat of black soybean (Glycine max (L.) Merr.). Phytochemistry 71:1253–1263Google Scholar
  36. Kumar RJS, Ruby SS, Sonawane PD, Vishwakarma RK, Khan BM (2013) Functional characterization of a glucosyltransferase specific to flavonoid 7-O-glucosides from Withania somnifera. Plant Mol Biol Rep 31:1100–1108CrossRefGoogle Scholar
  37. Lairson LL, Henrissat B, Davies GJ, Withers SG (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77:521–555CrossRefPubMedGoogle Scholar
  38. Leemhuis H, Kelly RM, Dijkhuizen L (2010) Engineering of cyclodextrin glucanotransferases and the impact for biotechnological applications. Appl Microbiol Biotechnol 85:823–835CrossRefPubMedPubMedCentralGoogle Scholar
  39. Li HM, Lee JK, Nie LJ, Huo Q, Ma T, Sohng JK, Hong YS, Wu CZ (2015) Enzymatic synthesis of novel isobavachalcone glucosides via a UDP-glycosyltransferase. Arch Pharm Res 38:2208–2215CrossRefPubMedGoogle Scholar
  40. Li J, Li Z, Li C, Gou J, Zhang Y (2014) Molecular cloning and characterization of an isoflavone 7-O-glucosyltransferase from Pueraria lobata. Plant Cell Rep 33:1173–1185CrossRefPubMedGoogle Scholar
  41. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495CrossRefPubMedPubMedCentralGoogle Scholar
  42. MacKenzie CR, Perry MB, McDonald IJ, Johnson KG (1978) Structure of the D-glucans produced by Neisseria perflava. Can J Microbiol 24:1419–1422CrossRefPubMedGoogle Scholar
  43. Malbert Y, Pizzut-Serin S, Massou S, Cambon E, Laguerre S, Monsan P, Lefoulon F, Morel S, André I, Remaud-Simeon M (2014) Extending the structural diversity of α-flavonoid glycosides with engineered glucansucrases. ChemCatChem 6:2282–2291CrossRefGoogle Scholar
  44. Malik V, Black GW (2012) Structural, functional, and mutagenesis studies of UDP-glycosyltransferases. Adv Protein Chem Struct Biol 87:87–115CrossRefPubMedGoogle Scholar
  45. Malla S, Pandey RP, Kim BG, Sohng JK (2013) Regiospecific modifications of naringenin for astragalin production in Escherichia coli. Biotechnol Bioeng 110:2525–2535CrossRefPubMedGoogle Scholar
  46. Matsuba Y, Sasaki N, Tera M, Okamura M, Abe Y, Okamoto E, Nakamura H, Funabashi H, Takatsu M, Saito M, Matsuoka H, Nagasawa K, Ozeki Y (2010) A novel glucosylation reaction on anthocyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell 22:3374–3389CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mirza O, Skov LK, Remaud-Siméon M, Potocki de Montalk G, Albenne C, Monsan P, Gajhede M (2001) Crystal structures of amylosucrase from Neisseria polysaccharea in complex with D-glucose and the active site mutant Glu328Gln in complex with the natural substrate sucrose. Biochemistry 40:9032–9039CrossRefPubMedGoogle Scholar
  48. Miyahara T, Takahashi M, Ozeki Y, Sasaki N (2012) Isolation of an acyl-glucose-dependent anthocyanin 7-O-glucosyltransferase from the monocot Agapanthus africanus. J Plant Physiol 169:1321–1326CrossRefPubMedGoogle Scholar
  49. Miyahara T, Tani T, Takahashi M, Nishizaki Y, Ozeki Y, Sasaki N (2014) Isolation of anthocyanin 7-O-glucosyltransferase from canterbury bells (Campanula medium). Plant Biotechnol 31:555–559CrossRefGoogle Scholar
  50. Offen W, Martinez-Fleites C, Yang M, Kiat-Lim E, Davis BG, Tarling CA, Ford CM, Bowles DJ, Davies GJ (2006) Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J 25:1396–1405CrossRefPubMedPubMedCentralGoogle Scholar
  51. Ohgami S, Ono E, Toyonaga H, Watanabe N, Ohnishi T (2014) Identification and characterization of Camellia sinensis glucosyltransferase, UGT73A17: a possible role in flavonol glucosylation. Plant Biotechnol 31:573–578CrossRefGoogle Scholar
  52. Olthof MR, Hollman PC, Vree TB, Katan MB (2000) Bioavailabilities of quercetin-3-glucoside and quercetin-4’-glucoside do not differ in humans. J Nutr 130:1200–1203PubMedGoogle Scholar
  53. Overwin H, Wray V, Hofer B (2015a) Biotransformation of phloretin by amylosucrase yields three novel dihydrochalcone glucosides. J Biotechnol 211:103–106CrossRefPubMedGoogle Scholar
  54. Overwin H, Wray V, Hofer B (2015b) Flavonoid glucosylation by non-Leloir glycosyltransferases: formation of multiple derivatives of 3,5,7,3′,4′-pentahydroxyflavane stereoisomers. Appl Microbiol Biotechnol 99:9565–9576CrossRefPubMedGoogle Scholar
  55. Pandey RP, Gurung RB, Parajuli P, Koirala N, Tuoi LT, Sohng JK (2014a) Assessing acceptor substrate promiscuity of YjiC-mediated glycosylation toward flavonoids. Carbohydr Res 393:26–31CrossRefPubMedGoogle Scholar
  56. Pandey RP, Li TF, Kim EH, Yamaguchi T, Park YI, Kim JS, Sohng JK (2013a) Enzymatic synthesis of novel phloretin glucosides. Appl Environ Microbiol 79:3516–3521CrossRefPubMedPubMedCentralGoogle Scholar
  57. Pandey RP, Malla S, Simkhada D, Kim BG, Sohng JK (2013b) Production of 3-O-xylosyl quercetin in Escherichia coli. Appl Microbiol Biotechnol 97:1889–1901CrossRefPubMedGoogle Scholar
  58. Pandey RP, Parajuli P, Chu LL, Darsandhari S, Sohng JK (2015) Biosynthesis of amino deoxy-sugar-conjugated flavonol glycosides by engineered Escherichia coli. Biochem Eng J 101:191–199CrossRefGoogle Scholar
  59. Pandey RP, Parajuli P, Koirala N, Lee JH, Park YI, Sohng JK (2014b) Glucosylation of isoflavonoids in engineered Escherichia coli. Mol Cells 37:172–177CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pandey RP, Parajuli P, Koirala N, Park JW, Sohng JK (2013c) Probing 3-hydroxyflavone for in vitro glycorandomization of flavonols by YjiC. Appl Environ Microbiol 79:6833–6838CrossRefPubMedPubMedCentralGoogle Scholar
  61. Parajuli P, Pandey RP, Trang NT, Chaudhary AK, Sohng JK (2015a) Synthetic sugar cassettes for the efficient production of flavonol glycosides in Escherichia coli. Microb Cell Factories 14:76CrossRefGoogle Scholar
  62. Parajuli P, Pandey RP, Trang NT, Oh TJ, Sohng JK (2015b) Expanded acceptor substrates flexibility study of flavonol 7-O-rhamnosyltransferase, AtUGT89C1 from Arabidopsis thaliana. Carbohydr Res 418:13–19CrossRefPubMedGoogle Scholar
  63. Park S-H, Park H-Y, Sohng JK, Lee HC, Liou K, Yoon YJ, Kim B-G (2009) Expanding substrate specificity of GT-B fold glycosyltransferase via domain swapping and high-throughput screening. Biotechnol Bioeng 102:988–994CrossRefPubMedGoogle Scholar
  64. Piovan A, Cozza G, Caniato R, Moro S, Filippini R (2010) A novel glucosyltransferase from Catharanthus roseus cell suspensions. Process Biochem 45:655–659CrossRefGoogle Scholar
  65. Raab T, Barron D, Arce Vera F, Crespy V, Oliveira M, Williamson G (2010) Catechin glucosides: occurrence, synthesis, and stability. J Agric Food Chem 58:2138–2149CrossRefPubMedGoogle Scholar
  66. Rabausch U, Juergensen J, Ilmberger N, Böhnke S, Fischer S, Schubach B, Schulte M, Streit WR (2013) Functional screening of metagenome and genome libraries for detection of novel flavonoid-modifying enzymes. Appl Environ Microbiol 79:4551–4563CrossRefPubMedPubMedCentralGoogle Scholar
  67. Ren G, Hou J, Fang Q, Sun H, Liu X, Zhang L, Wang PG (2012) Synthesis of flavonol 3-O-glycoside by UGT78D1. Glycoconj J 29:425–432CrossRefPubMedGoogle Scholar
  68. Roepke J, Bozzo GG (2013) Biocatalytic synthesis of quercetin 3-O-glucoside-7-O-rhamnoside by metabolic engineering of Escherichia coli. ChemBioChem 14:2418–2422Google Scholar
  69. Ruby, Kumar RJS, Vishwakarma RK, Singh S, Khan BM (2014) Molecular cloning and characterization of genistein 4′-O-glucoside specific glycosyltransferase from Bacopa monniera. Mol Biol Rep 41:4675–4688Google Scholar
  70. Sak K (2014) Cytotoxicity of dietary flavonoids on different human cancer types. Pharmacogn Rev 8:122–146CrossRefPubMedPubMedCentralGoogle Scholar
  71. Schneider J, Fricke C, Overwin H, Hofmann B, Hofer B (2009) Generation of amylosucrase variants that terminate catalysis of acceptor elongation at the di- or trisaccharide stage. Appl Environ Microbiol 75:7453–7460CrossRefPubMedPubMedCentralGoogle Scholar
  72. Simkhada D, Kurumbang NP, Lee HC, Sohng JK (2010a) Exploration of glycosylated flavonoids from metabolically engineered E. coli. Biotechnol Bioprocess Eng 15:754–760CrossRefGoogle Scholar
  73. Simkhada D, Lee HC, Sohng JK (2010b) Genetic engineering approach for the production of rhamnosyl and allosyl flavonoids from Escherichia coli. Biotechnol Bioeng 107:154–162CrossRefPubMedGoogle Scholar
  74. Singh S, Vishwakarma RK, Kumar RJ, Sonawane PD, Ruby, Khan BM (2013) Functional characterization of a flavonoid glycosyltransferase gene from Withania somnifera (Ashwagandha). Appl Biochem Biotechnol 170:729–741Google Scholar
  75. Song C, Gu L, Liu J, Zhao S, Hong X, Schulenburg K, Schwab W (2015) Functional characterization and substrate promiscuity of UGT71 glycosyltransferases from strawberry (Fragaria x ananassa). Plant Cell Physiol 56:2478–2493CrossRefPubMedGoogle Scholar
  76. Thuan NH, Pandey RP, Thuy TT, Park JW, Sohng JK (2013a) Improvement of regio-specific production of myricetin-3-O-α-L-rhamnoside in engineered Escherichia coli. Appl Biochem Biotechnol 171:1956–1967CrossRefPubMedGoogle Scholar
  77. Thuan NH, Park JW, Sohng JK (2013b) Toward the production of flavone-7-O-β-D-glucopyranosides using Arabidopsis glycosyltransferase in Escherichia coli. Process Biochem 48:1744–1748CrossRefGoogle Scholar
  78. Thuan NH, Sohng JK (2013) Recent biotechnological progress in enzymatic synthesis of glycosides. J Ind Microbiol Biotechnol 40:1329–1356CrossRefPubMedGoogle Scholar
  79. Uitdehaag JC, Mosi R, Kalk KH, van der Veen BA, Dijkhuizen L, Withers SG, Dijkstra BW (1999) X-ray structures along the reaction pathway of cyclodextrin glycosyltransferase elucidate catalysis in the alpha-amylase family. Nat Struct Biol 6:432–436CrossRefPubMedGoogle Scholar
  80. van Hijum SA, Kralj S, Ozimek LK, Dijkhuizen L, van Geel-Schutten IG (2006) Structure–function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev 70:157–176CrossRefPubMedPubMedCentralGoogle Scholar
  81. Veljanovski V, Constabel CP (2013) Molecular cloning and biochemical characterization of two UDP-glycosyltransferases from poplar. Phytochemistry 91:148–157CrossRefPubMedGoogle Scholar
  82. Vujicic-Zagar A, Pijning T, Kralj S, López CA, Eeuwema W, Dijkhuizen L, Dijkstra BW (2010) Crystal structure of a 117 kDa glucansucrase fragment provides insight into evolution and product specificity of GH70 enzymes. Proc Natl Acad Sci U S A 107:21406–21411CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wang L, Han W, Xie C, Hou J, Fang Q, Gu J, Wang PG, Cheng J (2013) Comparing the acceptor promiscuity of a Rosa hybrida glucosyltransferase RhGT1 and an engineered microbial glucosyltransferase OleDPSA toward a small flavonoid library. Carbohydr Res 368:73–77CrossRefPubMedGoogle Scholar
  84. Weymouth-Wilson AC (1997) The role of carbohydrates in biologically active natural products. Nat Prod Rep 14:99–110Google Scholar
  85. Williams GJ, Zhang C, Thorson JS (2007) Expanding the promiscuity of a natural-product glycosyltransferase by directed evolution. Nat Chem Biol 3:657–662CrossRefPubMedGoogle Scholar
  86. Withers S (2012) Glycoside Hydrolase Family 1. CAZypedia, available at URL http://www.cazypedia.org/
  87. Woo HJ, Kang HK, Nguyen TT, Kim GE, Kim YM, Park JS, Kim D, Cha J, Moon YH, Nam SH, Xia YM, Kimura A, Kim D (2012) Synthesis and characterization of ampelopsin glucosides using dextransucrase from Leuconostoc mesenteroides B-1299CB4: glucosylation enhancing physicochemical properties. Enzym Microb Technol 51:311–318CrossRefGoogle Scholar
  88. Xiao J, Muzashvili TS, Georgiev MI (2014) Advances in the biotechnological glycosylation of valuable flavonoids. Biotechnol Adv 32:1145–1156CrossRefPubMedGoogle Scholar
  89. Xie K, Chen R, Li J, Wang R, Chen D, Dou X, Dai J (2014) Exploring the catalytic promiscuity of a new glycosyltransferase from Carthamus tinctorius. Org Lett 16:4874–4877CrossRefPubMedGoogle Scholar
  90. Yang S-M, Han SH, Kim B-G, Ahn J-H (2014) Production of kaempferol 3-O-rhamnoside from glucose using engineered Escherichia coli. J Ind Microbiol Biotechnol 41:1311–1318CrossRefPubMedGoogle Scholar
  91. Yoon J-A, Kim B-G, Lee WJ, Lim Y, Chong Y, Ahn J-H (2012) Production of a novel quercetin glycoside through metabolic engineering of Escherichia coli. Appl Environ Microbiol 78:4256–4262CrossRefPubMedPubMedCentralGoogle Scholar
  92. Zhou M, Hamza A, Zhan CG, Thorson JS (2013) Assessing the regioselectivity of OleD-catalyzed glycosylation with a diverse set of acceptors. J Nat Prod 76:279–286CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Chemical BiologyHelmholtz Centre for Infection ResearchBraunschweigGermany

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