Glycoside Hydrolases for Extraction and Modification of Polyphenolic Antioxidants

  • Kazi Zubaida Gulshan Ara
  • Samiullah Khan
  • Tejas S. Kulkarni
  • Tania Pozzo
  • Eva Nordberg Karlsson
Chapter
First Online:

Abstract

Antioxidants are important molecules that are widely used by humans, both as dietary supplements and as additives to different types of products. In this chapter, we review how flavonoids, a class of polyphenolic antioxidants that are often found in glycosylated forms in many natural resources, can be extracted and modified using glycoside hydrolases (GHs). Glycosylation is a fundamental enzymatic process in nature, affecting function of many types of molecules (glycans, proteins, lipids as well as other organic molecules such as the flavonoids). Possibilities to control glycosylation thus mean possibilities to control or modify the function of the molecule. For the flavonoids, glycosylation affect both the antioxidative power and solubility. In this chapter we overview results on in vitro deglycosylation and glycosylation of flavonoids by selected GHs. For optimal enzymatic performance, desired features include a correct specificity for the target, combined with high stability. Poor specificity towards a specific substituent is thus a major drawback for enzymes in particular applications. Efforts to develop the enzymes as conversion tools are reviewed.

Keywords

Glucosidase Cellulase Amylase Glycosynthase GH Flavonoid Quercetin 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements 

The authors wish to thank Formas 2009-1527 (SuReTech), the European project AMYLOMICS and the Antidiabetic Food Centre, a VINNOVA VINN Excellence Centre at Lund University.

References

  1. Berrin JG, Czjzek M, Kroon PA, McLauchlan WR, Puigserver A, Williamson G, Juge N (2003) Substrate (aglycone) specificity of human cytosolic β-glucosidase. Biochem J 373:41–48PubMedCrossRefGoogle Scholar
  2. Bhatia Y, Mishra S, Bisaria VS (2002) Microbial β-glucosidases: cloning, properties, and applications. Crit Rev Biotechnol 22:375–407PubMedCrossRefGoogle Scholar
  3. Bommarius AS, Broering JM, Chaparro-Riggers JF, Polizzi KM (2006) High-throughput screening for enhanced protein stability. Curr Opin Biotechnol 17:606–610PubMedCrossRefGoogle Scholar
  4. Boudet AM (2007) Evolution and current status of research in phenolic compounds. Phytochemistry 68:2722–2735PubMedCrossRefGoogle Scholar
  5. Chuenchor W, Pengthaisong S, Robinson RC, Yuvaniyama J, Oonanant W, Bevan DR, Esen A, Chen C-J, Opassiri R, Svasti J, Cairns JRK (2008) Structural insights into rice bglu1 β-glucosidase oligosaccharide hydrolysis and transglycosylation. J Mol Biol 377:1200–1215PubMedCrossRefGoogle Scholar
  6. Corradini E, Foglia P, Giansanti P, Gubbiotti R, Samperi R, Lagana A (2011) Flavonoids: chemical properties and analytical methodologies of identification and quantitation in foods and plants. Nat Prod Res 25:469–495PubMedCrossRefGoogle Scholar
  7. Cuyckens F, Shahat AA, Van den Heuvel H, Abdel-Shafeek KA, El-Messiry MM, Seif-El Nasr MM, Pieters L, Vlietinck AJ, Claeys M (2003) The application of liquid chromatography-electrospray ionization mass spectrometry and collision-induced dissociation in the structural characterization of acylated flavonol O-glycosides from the seeds of Carrichtera annua. Eur J Mass Spectrom 9:409–420CrossRefGoogle Scholar
  8. Davis BG (2000) Recent developments in oligosaccharide synthesis. J Chem Soc Perkin Trans 1:2137–2160CrossRefGoogle Scholar
  9. Fu Y-J, Liu W, Zu Y-G, Tong M-H, Li S-M, Yan M-M, Efferth T, Luo H (2008) Enzyme assisted extraction of luteolin and apigenin from pigeonpea [Cajanus cajan (L.) Millsp.] leaves. Food Chem 111:508–512CrossRefGoogle Scholar
  10. Gao C, Mayon P, MacManus DA, Vulfson EN (2000) Novel enzymatic approach to the synthesis of flavonoid glycosides and their esters. Biotechnol Bioeng 71:235–243PubMedCrossRefGoogle Scholar
  11. Griffiths G, Trueman L, Crowther T, Thomas B, Smith B (2002) Onions—a global benefit to health. Phytother Res 16(7):603–615. doi: 10.1002/ptr.1222 PubMedCrossRefGoogle Scholar
  12. Haddad AQ, Venkateswaran V, Viswanathan L, Teahan SJ, Fleshner NE, Klotz LH (2005) Novel antiproliferative flavonoids induce cell cycle arrest in human prostate cancer cell lines. Prostate Cancer Prostatic Dis 9:68–76CrossRefGoogle Scholar
  13. Hancock SM, Vaughan MD, Withers SG (2006) Engineering of glycosidases and glycosyltransferases. Curr Opin Chem Biol 10:509–519PubMedCrossRefGoogle Scholar
  14. Havsteen BH (2002) The biochemistry and medical significance of the flavonoids. Pharmacol Ther 96:67–202PubMedCrossRefGoogle Scholar
  15. Hollman PCH, Arts ICW (2000) Flavonols, flavones and flavanols – nature, occurrence and dietary burden. J Sci Food Agric 80:1081–1093CrossRefGoogle Scholar
  16. Hughes RJ, Croley TR, Metcalfe CD, March RE (2001) A tandem mass spectrometric study of selected characteristic flavonoids. Int J Mass Spec 210/211:371–385CrossRefGoogle Scholar
  17. Ishihara K, Nakajima N (2003) Structural aspects of acylated plant pigments: stabilization of flavonoid glucosides and interpretation of their functions. J Mol Catal B Enzym 23:411–417CrossRefGoogle Scholar
  18. Iwashina T (2000) The structure and distribution of the flavonoids in plants. J Plant Res 113:287–299CrossRefGoogle Scholar
  19. Kapasakalidis PG, Rastall RA, Gordon MH (2009) Effect of a cellulase treatment on extraction of antioxidant phenols from black currant (Ribes nigrum L.) pomace. J Agric Food Chem 57:4342–4351PubMedCrossRefGoogle Scholar
  20. Ketudat Cairns J, Esen A (2010) β-Glucosidases. Cell Mol Life Sci 67:3389–3405PubMedCrossRefGoogle Scholar
  21. Khan S, Pozzo T, Megyeri M, Lindahl S, Sundin A, Turner C, Nordberg Karlsson E (2011) Aglycone specificity of Thermotoga neapolitana β-glucosidase 1A modified by mutagenesis, leading to increased catalytic efficiency in quercetin-3-glucoside hydrolysis. BMC Biochem 12:11PubMedCrossRefGoogle Scholar
  22. Kim Y-S, Yeom S-J, Oh D-K (2011) Characterization of a GH3 family β-glucosidase from Dictyoglomus turgidum and its application to the hydrolysis of isoflavone glycosides in spent coffee grounds. J Agric Food Chem 59:11812–11818PubMedCrossRefGoogle Scholar
  23. Klibanov AM (2001) Improving enzymes by using them in organic solvents. Nature 409:241–246PubMedCrossRefGoogle Scholar
  24. Kong F (2003) Regio- and stereoselective synthesis of oligosaccharides with unprotected or lightly protected sugars as glycosyl acceptors. Curr Org Chem 7:841–865CrossRefGoogle Scholar
  25. Kulkarni TS, Khan S, Mahmood T, Sundin A, Lindahl S, Turner C, Logan DT, Nordberg Karlsson E (unpublished) Structure of Thermotoga neapolitana β-glucosidase 1A and comparison of active site mutants in hydrolysis of pNPGlc and quercetin-3 glucosidesGoogle Scholar
  26. Landbo A-K, Meyer AS (2001) Enzyme-assisted extraction of antioxidative phenols from black currant juice press residues (Ribes nigrum). J Agric Food Chem 49:3169–3177PubMedCrossRefGoogle Scholar
  27. Lee KW, Lee HJ (2006) The roles of polyphenols in cancer chemoprevention. Biofactors 26:105–121PubMedCrossRefGoogle Scholar
  28. Lin JK, Weng MS (2006) Flavonoids as nutraceuticals. In: Grotewold E (ed) The science of flavonoids. Springer, New York, pp 213–238CrossRefGoogle Scholar
  29. Lin S-C, Chang C-MJ, Deng T-S (2009) Enzymatic hot pressurized fluids extraction of polyphenolics from Pinus taiwanensis and Pinus morrisonicola. J Taiwan Inst Chem Eng 40:136–142CrossRefGoogle Scholar
  30. Lindahl S, Ekman A, Khan S, Wennerberg C, Borjesson P, Sjoberg PJR, Nordberg Karlsson E, Turner C (2010) Exploring the possibility of using a thermostable mutant of β-glucosidase for rapid hydrolysis of quercetin glucosides in hot water. Green Chem 12:159–168CrossRefGoogle Scholar
  31. Ljunger G, Adlercreutz P, Mattiasson B (1994) Enzymatic synthesis of octyl-β-glucoside in octanol at controlled water activity. Enzyme Microb Technol 16:751–755CrossRefGoogle Scholar
  32. Ly HD, Withers SG (1999) Mutagenesis of glycosidases. Ann Rev Biochem 68:487–522PubMedCrossRefGoogle Scholar
  33. Maier T, Göppert A, Kammerer D, Schieber A, Carle R (2008) Optimization of a process for enzyme-assisted pigment extraction from grape (Vitis vinifera L.) pomace. Eur Food Res Technol 227:267–275CrossRefGoogle Scholar
  34. Mamma D, Hatzinikolaou DG, Christakopoulos P (2004) Biochemical and catalytic properties of two intracellular β-glucosidases from the fungus Penicillium decumbens active on flavonoid glucosides. J Mol Catal B Enzym 27:183–190CrossRefGoogle Scholar
  35. Nakatani H (2001) Analysis of glycosidase-catalyzed transglycosylation reaction using probabilistic model. Arch Biochem Biophys 385:387–391PubMedCrossRefGoogle Scholar
  36. Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74:418–425PubMedGoogle Scholar
  37. Noguchi A, Inohara-Ochiai M, Ishibashi N, Fukami H, Nakayama T, Nakao M (2008) A novel glucosylation enzyme: molecular cloning, expression, and characterization of Trichoderma viride Jcm22452 α-amylase and enzymatic synthesis of some flavonoid monoglucosides and oligoglucosides. J Agric Food Chem 56:12016–12024PubMedCrossRefGoogle Scholar
  38. Park T-H, Choi K-W, Park C-S, Lee S-B, Kang H-Y, Shon K-J, Park J-S, Cha J (2005) Substrate specificity and transglycosylation catalyzed by a thermostable β-glucosidase from marine hyperthermophile Thermotoga neapolitana. Appl Microbiol Biotechnol 69:411–422PubMedCrossRefGoogle Scholar
  39. Robards K, Li X, Antolovich M, Boyd S (1997) Characterisation of citrus by chromatographic analysis of flavonoids. J Sci Food Agric 75:87–101CrossRefGoogle Scholar
  40. Sansenya S, Maneesan J, Ketudat Cairns JR (2012) Exchanging a single amino acid residue generates or weakens a +2 cellooligosaccharide binding subsite in rice beta-glucosidases. Carbohydr Res 351:130–133PubMedCrossRefGoogle Scholar
  41. Stobiecki M, Malosse C, Kerhoas L, Wojlaszek P, Einhorn J (1999) Detection of isoflavonoids and their glycosides by liquid chromatography/electrospray ionization mass spectrometry in root extracts of lupin (Lupinus albus). Phytochem Anal 10:198–207CrossRefGoogle Scholar
  42. Tribolo S, Berrin JG, Kroon PA, Czjzek M, Juge N (2007) The crystal structure of human cytosolic β-glucosidase unravels the substrate aglycone specificity of a family 1 glycoside hydrolase. J Mol Biol 370:964–975PubMedCrossRefGoogle Scholar
  43. Turner P, Mamo G, Nordberg Karlsson E (2007) Potential and utilization of thermophiles and thermostable enzymes in biorefining. Microb Cell Fact 6:9PubMedCrossRefGoogle Scholar
  44. Turner C, Turner P, Jacobson G, Almgren K, Waldeback M, Sjoberg P, Nordberg Karlsson E, Markides KE (2006) Subcritical water extraction and β-glucosidase-catalyzed hydrolysis of quercetin glycosides in onion waste. Green Chem 8:949–959CrossRefGoogle Scholar
  45. Walle T (2004) Absorption and metabolism of flavonoids. Free Radic Biol Med 36(7):829–837PubMedCrossRefGoogle Scholar
  46. Wang L-X, Huang W (2009) Enzymatic transglycosylation for glycoconjugate synthesis. Curr Opin Chem Biol 13:592–600PubMedCrossRefGoogle Scholar
  47. Yang M, Davies GJ, Davis BG (2007) A glycosynthase catalyst for the synthesis of flavonoid glycosides. Angew Chem 46:3885–3888CrossRefGoogle Scholar
  48. Zheng H-Z, Hwang I-W, Chung S-K (2009) Enhancing polyphenol extraction from unripe apples by carbohydrate-hydrolyzing enzymes. J Zhejiang Univrsity Sci B 10:912–919CrossRefGoogle Scholar

Copyright information

© Springer India 2013

Authors and Affiliations

  • Kazi Zubaida Gulshan Ara
    • 1
  • Samiullah Khan
    • 1
  • Tejas S. Kulkarni
    • 1
  • Tania Pozzo
    • 1
  • Eva Nordberg Karlsson
    • 1
  1. 1.Biotechnology, Department of ChemistryLund UniversityLundSweden

Personalised recommendations