Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Enzymatic Synthesis of Resveratrol α-Glucoside by Amylosucrase of Deinococcus geothermalis

  • Moon, Keumok (Microbiological Resource Research Institute, Pusan National University) ;
  • Lee, Seola (Department of Microbiology, Pusan National University) ;
  • Park, Hyunsu (Department of Microbiology, Pusan National University) ;
  • Cha, Jaeho (Microbiological Resource Research Institute, Pusan National University)
  • Received : 2021.08.27
  • Accepted : 2021.09.24
  • Published : 2021.12.28
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Abstract

Glycosylation of resveratrol was carried out by using the amylosucrase of Deinococcus geothermalis, and the glycosylated products were tested for their solubility, chemical stability, and biological activities. We synthesized and identified these two major glycosylated products as resveratrol-4'-O-α-glucoside and resveratrol-3-O-α-glucoside by nuclear magnetic resonance analysis with a ratio of 5:1. The water solubilities of the two resveratrol-α-glucoside isomers (α-piceid isomers) were approximately 3.6 and 13.5 times higher than that of β-piceid and resveratrol, respectively, and they were also highly stable in buffered solutions. The antioxidant activity of the α-piceid isomers, examined by radical scavenging capability, showed it to be initially lower than that of resveratrol, but as time passed, the α-piceid isomers' activity reached a level similar to that of resveratrol. The α-piceid isomers also showed better inhibitory activity against tyrosinase and melanin synthesis in B16F10 melanoma cells than β-piceid. The cellular uptake of the α-piceid isomers, which was assessed by ultra-performance liquid chromatography (UPLC) analysis of the cell-free extracts of B16F10 melanoma cells, demonstrated that the glycosylated form of resveratrol was gradually converted to resveratrol inside the cells. These results indicate that the enzymatic glycosylation of resveratrol could be a useful method for enhancing the bioavailability of resveratrol.

Keywords

Acknowledgement

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2020R1I1A1A01073109) to K.M.

References

  1. Constant J. 1997. Alcohol, ischemic heart disease, and the French paradox. Clin. Cardiol. 20: 420-424. https://doi.org/10.1002/clc.4960200504
  2. Fan E, Zhang L, Jiang S, Bai Y. 2008. Beneficial effects of resveratrol on atherosclerosis. J. Med. Food. 11: 610-614. https://doi.org/10.1089/jmf.2007.0091
  3. Su D, Cheng Y, Liu M, Liu D, Cui H, Zhang B, et al. 2013. Comparision of piceid and resveratrol in antioxidation and antiproliferation activities in vitro. PLoS One 8: e54505. https://doi.org/10.1371/journal.pone.0054505
  4. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CWW, et al. 1997. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275: 218-220. https://doi.org/10.1126/science.275.5297.218
  5. Mizutani K, Ikeda K, Kawai Y, Yamori Y. 1998. Resveratrol stimulates the proliferation and differentiation of osteoblastic MC3T3-E1 cells. Biochem. Biophys. Res. Commun. 253: 859-863. https://doi.org/10.1006/bbrc.1998.9870
  6. Newton RA, Cook AL, Roberts DW, Leonard JH, Sturm RA. 2007. Post-transcriptional regulation of melanin biosynthetic enzymes by cAMP and resveratrol in human melanocytes. J. Invest. Dermatol. 127: 2216-2227. https://doi.org/10.1038/sj.jid.5700840
  7. Fremont L. 2000. Biological effects of resveratrol. Life Sci. 66: 663-673. https://doi.org/10.1016/S0024-3205(99)00410-5
  8. Baxter RA. 2008. Anti-aging properties of resveratrol: review and report of a potent new antioxidant skin care formulation. J. Cosmet. Dermatol. 7: 2-7. https://doi.org/10.1111/j.1473-2165.2008.00354.x
  9. Chimento A, De Amicis F, Sirianni R, Sinicropi MS, Puoci F, Casaburi I, et al. 2019. Progress to improve oral bioavailability and beneficial effects of resveratrol. Int. J. Mol. Sci. 20: 1381. https://doi.org/10.3390/ijms20061381
  10. Walle T. 2011. Bioavailability of resveratrol. Ann. NY Acad. Sci. 1215: 9-15. https://doi.org/10.1111/j.1749-6632.2010.05842.x
  11. Walle T, Hsieh F, DeLegge MH, Oatis JE, Walle UK. 2004. High absorption but very low bioavailability of oral resveratrol in humans. Drug Metab. Dispos. 32: 1377-1382. https://doi.org/10.1124/dmd.104.000885
  12. Yu C, Shin YG, Chow A, Li Y, Kosmeder JW, Lee YS, et al. 2002. Human, rat, and mouse metabolism of resveratrol. Pharm. Res. 19: 1907-1914. https://doi.org/10.1023/A:1021414129280
  13. Wenzel E, Somoza V. 2005. Metabolism and bioavailability of trans-resveratrol. Mol. Nutr. Food Res. 49: 472-481. https://doi.org/10.1002/mnfr.200500010
  14. Orsini F, Verotta L, Klimo K, Gerhauser C. 2016. Synthesis of resveratrol derivatives and in vitro screening for potential cancer chemopreventive activities. Arch. Pharm. Chem. Life Sci. 349: 414-427. https://doi.org/10.1002/ardp.201600022
  15. Liu Q, Kim C, Jo YH, Kim SB, Hwang BY, Lee MK. 2015. Synthesis and biological evaluation of resveratrol derivatives as melanogenesis inhibitors. Molecules 20: 16933-16945. https://doi.org/10.3390/molecules200916933
  16. Cho HK, Kim HH, Seo DH, Jung JH, Park JH, Baek NI, et al. 2011. Biosynthesis of (+)- catechin glycosides using recombinant amylosucrase from Deinococcus geothermalis DSM 11300. Enzyme Microb. Technol. 49: 246-253. https://doi.org/10.1016/j.enzmictec.2011.05.007
  17. Moon KO, Park H, Joo M, Ha KT, Baek NI, Park CS, et al. 2017. Glycosylation enhances the physicochemical properties of caffeic acid phenethyl ester. J. Microbiol. Biotechnol. 27: 1916-1924. https://doi.org/10.4014/jmb.1706.06017
  18. Park S, Moon K, Park CS, Jung DH, Cha J. 2018. Synthesis of aesculetin and aesculin glycosides using engineered Escherichia coli expressing Neisseria polysaccharea amylosucrase. J. Microbiol. Biotechnol. 28: 566-570. https://doi.org/10.4014/jmb.1711.11055
  19. Kim KH, Park YD, Park H, Moon KO, Ha KT, Baek NI, et al. 2014. Synthesis and biological evaluation of a novel baicalein glycoside as an anti-inflammatory agent. Eur. J. Pharmacol. 744: 147-156. https://doi.org/10.1016/j.ejphar.2014.10.013
  20. Kometani T, Nishimura T, Nakae T, Takii H, Okada S. 1996. Synthesis of neohesperidin glycosides and naringin glycosides by cyclodextrin glucano-transferase from an Alkalophilic Bacillus species. Biosci. Biotechnol. Biochem. 60: 645-649. https://doi.org/10.1271/bbb.60.645
  21. Jung JH, Seo DH, Ha SJ, Song MC, Cha J, Yoo SH, et al. 2009. Enzymatic synthesis of salicin glycosides through transglycosylation catalyzed by amylosucrases from Deinococcus geothermalis and Neisseria polysaccharea. Carbohydr. Res. 344: 1612-1619. https://doi.org/10.1016/j.carres.2009.04.019
  22. Park H, Kim J, Choi KH, Hwang S, Yang SJ, Baek NI, et al. 2012. Enzymatic synthesis of piceid glucosides using maltosyltransferase from Caldicellulosiruptor bescii DSM 6725. J. Agric. Food Chem. 60: 8183-8189. https://doi.org/10.1021/jf302127a
  23. Regev-Shoshani G, Shoseyov O, Bilkis I, Kerem Z. 2003. Glycosylation of resveratrol protects it from enzymic oxidation. Biochem. J. 374: 157-163. https://doi.org/10.1042/BJ20030141
  24. Moon K, Cha J. 2020. Enhancement of antioxidant and antibacterial activities of Salvia miltiorrhiza roots fermented with Aspergillus oryzae. Foods 9: 34. https://doi.org/10.3390/foods9010034
  25. Park HJ, Lee EH, Jung HY, Kang IK, Cho YJ. 2020. Effects of phenolics from Oplismenus undulatifolius in α-MSH-stimulated B16F10 melanoma cells. J. Appl. Biol. Chem. 63: 89-93. https://doi.org/10.3839/jabc.2020.012
  26. Marier JF, Vachon P, Gritsas A, Zhang J, Moreau JP, Ducharme MP. 2002. Metabolism and disposition of resveratrol in rats: extent of absorption, glucuronidation, and enterohepatic recirculation evidenced by a linked-rat model. J. Pharmacol. Exp. Ther. 302: 369-373. https://doi.org/10.1124/jpet.102.033340
  27. Remsberg CM, Yanez JA, Ohgami Y, Vega-Villa KR, Rimando AM, Davies NM. 2008. Pharmacometrics of pterostilbene: preclinical pharmacokinetics and metabolism, anticancer, antiinflammatory, antioxidant and analgesic activity. Phytother. Res. 22: 169-179. https://doi.org/10.1002/ptr.2277
  28. Thaipong K, Boonprakob U, Crosby K, Cisneros-Zevallos L, Byrne DH. 2006. Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J. Food Compos. Anal. 19: 669-675. https://doi.org/10.1016/j.jfca.2006.01.003
  29. Jun SY, Park KM, Choi KW, Jang MK, Kang HY, Lee SH, et al. 2008. Inhibitory effects of arbutin-β-glycosides synthesized from enzymatic transglycosylation for melanogenesis. Biotechnol. Lett. 30: 743-748. https://doi.org/10.1007/s10529-007-9605-1
  30. Lee TH, Seo JO, Baek SH, Kim SY. 2014. Inhibitory effects of resveratrol on melanin synthesis in ultraviolet B-induced pigmentation in Guinea pig skin. Biomol. Ther. 22: 35-40. https://doi.org/10.4062/biomolther.2013.081
  31. Yoon HS, Hyun CG, Lee NH, Park SS, Shin DB. 2016. Comparative depigmentation effects of resveratrol and its two methyl analogues in α-melanocyte stimulating hormone-triggered B16/F10 murine melanoma cells. Prev. Nutr. Food Sci. 21: 155. https://doi.org/10.3746/PNF.2016.21.2.155
  32. Kim JK, Park KT, Lee HS, Kim M, Lim YH. 2012. Evaluation of the inhibition of mushroom tyrosinase and cellular tyrosinase activities of oxyresveratrol: comparison with mulberroside A. J. Enzyme Inhib. Med. Chem. 27: 495-503. https://doi.org/10.3109/14756366.2011.598866
  33. Satooka H, Kubo I. 2012. Resveratrol as a kcat type inhibitor for tyrosinase: potentiated melanogenesis inhibitor. Bioorg. Med. Chem. 20: 1090-1099. https://doi.org/10.1016/j.bmc.2011.11.030
  34. Jeong ET, Jin MH, Kim MS, Chang YH, Park SG. 2010. Inhibition of melanogenesis by piceid isolated from Polygonum cuspidatum. Arch. Pharm. Res. 33: 1331-1338. https://doi.org/10.1007/s12272-010-0906-x
  35. Ozaki S, Imai H, Iwakiri T, Sato T, Shimoda K, Nakayama T, et al. 2012. Regioselective glucosidation of trans-resveratrol in Escherichia coli expressing glucosyltransferase from Phytolacca americana. Biotechnol. Lett. 34: 475-481. https://doi.org/10.1007/s10529-011-0784-4
  36. Stivala LA, Savio M, Carafoli F, Perucca P, Bianchi L, Maga G, et al. 2001. Specific structural determinants are responsible for the antioxidant activity and the cell cycle effects of resveratrol. J. Biol. Chem. 276: 22586-22594. https://doi.org/10.1074/jbc.M101846200
  37. Waffo Teguo P, Fauconneau B, Deffieux G, Huguet F, Vercauteren J, Merillon J-M. 1998. Isolation, identification, and antioxidant activity of three stilbene glucosides newly extracted from Vitis vinifera cell cultures. J. Nat. Prod. 61: 655-657. https://doi.org/10.1021/np9704819
  38. Fang JG, Lu M, Chen ZH, Zhu HH, Li Y, Yang L, et al. 2002. Antioxidant effects of resveratrol and its analogues against the free-radical-induced peroxidation of linoleic acid in micelles. Chem. Eur. J. 8: 4191-4198. https://doi.org/10.1002/1521-3765(20020916)8:18<4191::AID-CHEM4191>3.0.CO;2-S
  39. Henriquez C, Lopez-Alarcon C, Lutz MGM, Speisky H. 2011. Time-dependence of ferric reducing antioxidant power (FRAP) index in Chilean apples and berries. Arch. Latinoam. Nutr. 61: 323-332.
  40. Ohguchi K, Tanaka T, Kido T, Baba K, Iinuma M, Matsumoto K, et al. 2003. Effects of hydroxystilbene derivatives on tyrosinase activity. Biochem. Biophys. Res. Commun. 307: 861-863. https://doi.org/10.1016/S0006-291X(03)01284-1
  41. Lee HS, Lee BW, Kim MR, Jun JG. 2010. Syntheses of resveratrol and its hydroxylated derivatives as radical scavenger and tyrosinase inhibitor. Bull. Korean Chem. Soc. 31: 971-975. https://doi.org/10.5012/bkcs.2010.31.04.971
  42. Funayama M, Arakawa H, Yamamoto R, Nishino T, Shin T, Murao S. 1995. Effects of α-and β-arbutin on activity of tyrosinases from mushroom and mouse melanoma. Biosci. Biotechnol. Biochem. 59: 143-144. https://doi.org/10.1271/bbb.59.143
  43. Yamada M, Tanabe F, Arai N, Mitsuzumi H, Miwa Y, Kubota M, et al. 2006. Bioavailability of glucosyl hesperidin in rats. Biosci. Biotechnol. Biochem. 70: 1386-1394. https://doi.org/10.1271/bbb.50657
  44. Jiang JR, Yuan S, Ding JF, Zhu SC, Xu HD, Chen T, et al. 2008. Conversion of puerarin into its 7-O-glycoside derivatives by Microbacterium oxydans (CGMCC 1788) to improve its water solubility and pharmacokinetic properties. Appl. Microbiol. Biotechnol. 81: 647-657. https://doi.org/10.1007/s00253-008-1683-z