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Evaluation of glucosidases of Aspergillus niger strain comparing with other glucosidases in transformation of ginsenoside Rb1 to ginsenosides Rg3

  • Chang, Kyung Hoon (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Jo, Mi Na (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Kim, Kee-Tae (Bio/Molecular Informatics Center, Konkuk University) ;
  • Paik, Hyun-Dong (Department of Food Science and Biotechnology of Animal Resources, Konkuk University)
  • Received : 2013.07.23
  • Accepted : 2013.09.10
  • Published : 2014.01.15

Abstract

The transformation of ginsenoside Rb1 into a specific minor ginsenoside using Aspergillus niger KCCM 11239, as well as the identification of the transformed products and the pathway via thin layer chromatography and high performance liquid chromatography were evaluated to develop a new biologically active material. The conversion of ginsenoside Rb1 generated Rd, Rg3, Rh2, and compound K although the reaction rates were low due to the low concentration. In enzymatic conversion, all of the ginsenoside Rb1 was converted to ginsenoside Rd and ginsenoside Rg3 after 24 h of incubation. The crude enzyme (b-glucosidase) from A. niger KCCM 11239 hydrolyzed the ${\beta}$-($1{\rightarrow}6$)-glucosidic linkage at the C-20 of ginsenoside Rb1 to generate ginsenoside Rd and ginsenoside Rg3. Our experimental demonstration showing that A. niger KCCM 11239 produces the ginsenoside-hydrolyzing b-glucosidase reflects the feasibility of developing a specific bioconversion process to obtain active minor ginsenosides.

Keywords

References

  1. Baque MA, Moh SH, Lee EJ, Zhong JJ, Paek KY. Production of biomass and useful compounds from adventitious roots of high-value added medicinal plants using bioreactor. Biotechnol Adv 2012;30:1255-67. https://doi.org/10.1016/j.biotechadv.2011.11.004
  2. Han S, Kim JS, Jung BK, Han SE, Nam JH, Kwon YK, Nah SY, Kim BJ. Effects of ginsenoside on pacemaker potentials of cultured interstitial cells of Cajal clusters from the small intestine of mice. Mol Cells 2012;33:243-9. https://doi.org/10.1007/s10059-012-2204-6
  3. Shibata S, Ando T, Tanaka O. Chemical Studies on the Oriental Plant Drugs. XVII. The prosapogenin of the ginseng saponins: ginsenosides-Rb1,-Rb2, and -Rc. Chem Pharm Bull (Tokyo) 1966;14:1157-61. https://doi.org/10.1248/cpb.14.1157
  4. Cheng LQ, Na JR, Bang MH, Kim MK, Yang DC. Conversion of major ginsenoside Rb1 to 20(S)-ginsenoside Rg3 by Microbacterium sp. GS514. Phytochemistry 2008;69:218-24. https://doi.org/10.1016/j.phytochem.2007.06.035
  5. Li WK, Gu CG, Zhang HJ, Awang DVC, Fitzloff JF, Fong HHS, Van Breeman RB. Use of high performance liquid chromatography tandem mass spectrometry to distinguish Panax ginseng C.A. Meyer (Asian ginseng) and Panax quinquefolius. L. (American ginseng). Anal Chem 2000;72:5417-22. https://doi.org/10.1021/ac000650l
  6. Ji QC, Harkey MR, Henderson GL, Gershwin ME, Stem JS, Hackman RM. Quantitative determination of ginsenosides by high-performance liquid chromatography-tandem mass spectrometry. Phytochem Anal 2001;12: 320-6. https://doi.org/10.1002/pca.593
  7. Akao T, Kanaoka M, Kobashi K. Appearance of compound K, a major metabolite of ginsenoside Rb1 by intestinal bacterial in rat plasma after oral administration-measurement of compound K by enzyme immunoassay. Biol Pharm Bull 1998;21:245-9. https://doi.org/10.1248/bpb.21.245
  8. Paek IB, Moon Y, Kim J, Ji HY, Kim SA, Sohn DH, Kim JB, Lee HS. Pharmacokinetics of a ginseng saponin metabolite compound K in rats. Biopharm Drug Dispos 2006;27:39-45. https://doi.org/10.1002/bdd.481
  9. Liu WK, Xu SX, Che CT. Anti-proliferative effect of ginseng saponins on human prostate cancer cell line. Life Sci 2000;67:1297-306. https://doi.org/10.1016/S0024-3205(00)00720-7
  10. Min JK, Kim JH, Cho YL, Maeng YS, Lee SJ, Pyun BJ, Kim YM, Park JH, Kwon YG. 20(S)-Ginsenoside Rg3 prevents endothelial cell apoptosis via inhibition of a mitochondrial caspase pathway. Biochem Biophys Res Commun 2006;349: 987-94. https://doi.org/10.1016/j.bbrc.2006.08.129
  11. Poon PY, Kwok HH, Yue PY, Yang MS, Mak NK, Wong CK, Wong RN. Cytoprotective effect of 20(S)-Rg3 on benzo[a]pyrene-induced DNA damage. Drug Metab Dispos 2012;40:120-9. https://doi.org/10.1124/dmd.111.039503
  12. Kim WY, Kim JM, Han SB, Lee SK, Kim ND, Park MK, Kim CK, Park JH. Steaming of ginseng at high temperature enhances biological activity. J Nat Prod 2000;63:1702-4. https://doi.org/10.1021/np990152b
  13. Han BH, Park MH, Han YN, Woo WS, Sankawa U, Yahara S, Tanaka O. Degradation of ginseng saponins under mild acidic condition. Planta Med 1982;44:146-9. https://doi.org/10.1055/s-2007-971425
  14. Yang L, He KJ, Yang Y. A preparation method of less polar individual ginsenosides and saponins by base hydrolysis; 2003. China Patent CN03134090.3.
  15. Luan H, Liu X, Qi X, Hu Y, Hao D, Cui Y, Yang L. Purification and characterization of a novel stable ginsenoside Rb1-hydrolyzing b-D-glucosidase from China white jade snail. Process Biochem 2006;41:1974-80. https://doi.org/10.1016/j.procbio.2006.04.011
  16. Qin Y, Zhou X, Zhou W, Li X, Feng M, Zhou P. Purification and properties of a novel beta-glucosidase, hydrolyzing ginsenoside Rb1 to CK, from Paecilomyces bainier. J Microbiol Biotechn 2008;18:1081-9.
  17. Zhao X, Wang J, Li J, Fu L, Gao J, Du X, Bi H, Zhou Y, Tai G. Highly selective biotransformation of ginsenoside Rb1 to Rd by the phytopathogenic fungus Cladosporium fulvum (syn. Fulvia fulva). Microbiol Biotechnol 2009;36:721-6. https://doi.org/10.1007/s10295-009-0542-y
  18. Gao J, Zhao X, Liu H, Fan Y, Cheng H, Liang F, Chen X, Wang N, Zhou Y, Tai G. A highly selective ginsenoside Rb1-hydrolyzing b-d-glucosidase from Cladosporium fulvum. Process Biochem 2010;45:897-903. https://doi.org/10.1016/j.procbio.2010.02.016
  19. Kim MY, Lee JW, Lee KY, Yang DC. Microbial conversion of major ginsenoside Rb1 to pharmaceutically active minor ginsenoside Rd. J Microbiol 2005;43: 456-62.
  20. Noh KH, Son JW, Kim HJ, Oh DK. Ginsenoside compound K production from ginseng root extract by a thermostable b-glycosidase from Sulfolobus solfataricus. Biosci Biotechnol Biochem 2009;73:316-21. https://doi.org/10.1271/bbb.80525
  21. Lv XC, Huang ZQ, Zhang W, Rao PF, Ni L. Identification and characterization of filamentous fungi isolated from fermentation starters for Hong Qu glutinous rice wine brewing. J Gen Appl Microbiol 2012;58:33-42. https://doi.org/10.2323/jgam.58.33
  22. Pederson L, Hansen K, Nielsen J, Lantz AE, Thykaer J. Industrial glucoamylase fed-batch benefits from oxygen limitation and high osmolarity. Biotechnol Bioeng 2012;109:116-24. https://doi.org/10.1002/bit.23287
  23. Kohchi C, Toh-e A. Cloning of Candida pelliculosa b-glucosidase gene and its expression in Saccharomyces cerevisiae. Mol Gen Genet 1986;203:89-94. https://doi.org/10.1007/BF00330388
  24. Cheng LQ, Kim M, Lee JW, Lee YJ, Yang DC. Conversion of major ginsenoside Rb1 to ginsenoside F2 by Caulobacter leidyia. Biotechnol Lett 2006;28: 1121-7. https://doi.org/10.1007/s10529-006-9059-x
  25. Yu H, Liu Q, Zhang C, Lu M, Fu Y, Im YT, Lee ST, Jin F. A new ginsenosidase from Aspergillus strain hydrolyzing 20-O-multi-glycoside of PPD ginsenoside. Process Biochem 2009;44:772-5. https://doi.org/10.1016/j.procbio.2009.02.005
  26. Quan LH, Min JW, Yang DU, Kim YJ, Yang DC. Enzymatic biotransformation of ginsenoside Rb1 to 20(S)-Rg3 by recombinant beta-glucosidase from Microbacterium esteraromaticum. Appl Microbiol Biot 2012;94:377-84. https://doi.org/10.1007/s00253-011-3861-7
  27. Lee JK, Choi SS, Lee HK, Han KJ, Han EJ, Suh HW. Effects of ginsenoside Rd and decursinol on the neurotoxic responses induced by kainic acid in mice. Planta Med 2003;69:230-4. https://doi.org/10.1055/s-2003-38475
  28. Zeng S, Guan YY, Liu DY, He H, Wang W, Qiu QY, Wang XR, Wang YD. Synthesis of 12-epi-ginsenoside Rd and its effects on contractions of rat aortic rings. Chin Pharmacol Bull 2003;19:282-6.
  29. Shi Q, Hao Q, Bouissac J, Lu Y, Tian S, Luu B. Ginsenoside-Rd from Panax notoginseng enhances astrocyte differentiation from neural stem cells. Life Sci 2005;76:983-5. https://doi.org/10.1016/j.lfs.2004.07.026
  30. Jeong SM, Lee JH, Kim JH, Lee BH, Yoon IS, Lee JH, Kim DH, Rhim H, Kim Y, Nah SY. Stereospecificity of ginsenoside Rg3 action on ion channels. Mol Cells 2004;18:383-9.
  31. Chang KH, Jo MN, Kim KT, Paik HD. Purification and characterization of a ginsenoside Rb1-hydrolyzing b-glucosidase from Aspergillus niger KCCM 11239. Int J Mol Sci 2012;13:12140-52. https://doi.org/10.3390/ijms130912140

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