Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Fermentation of red ginseng extract by the probiotic Lactobacillus plantarum KCCM 11613P: ginsenoside conversion and antioxidant effects

  • Jung, Jieun (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Jang, Hye Ji (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Eom, Su Jin (Department of Food Science and Biotechnology of Animal Resources, Konkuk University) ;
  • Choi, Nam Soon (Department of Food and Nutrition, Baewha Women's University) ;
  • Lee, Na-Kyoung (Bio/Molecular Informatics Center, Konkuk University) ;
  • Paik, Hyun-Dong (Department of Food Science and Biotechnology of Animal Resources, Konkuk University)
  • Received : 2017.02.21
  • Accepted : 2017.07.20
  • Published : 2019.01.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Ginsenosides, which are bioactive components in ginseng, can be converted to smaller compounds for improvement of their pharmacological activities. The conversion methods include heating; acid, alkali, and enzymatic treatment; and microbial conversion. The aim of this study was to determine the bioconversion of ginsenosides in fermented red ginseng extract (FRGE). Methods: Red ginseng extract (RGE) was fermented using Lactobacillus plantarum KCCM 11613P. This study investigated the ginsenosides and their antioxidant capacity in FRGE using diverse methods. Results: Properties of RGE were changed upon fermentation. Fermentation reduced the pH value, but increased the titratable acidity and viable cell counts of lactic acid bacteria. L. plantarum KCCM 11613P converted ginsenosides $Rb_2$ and $Rb_3$ to ginsenoside Rd in RGE. Fermentation also enhanced the antioxidant effects of RGE. FRGE reduced 2,2-diphenyl-1-picrylhydrazyl radical scavenging activity and reducing power; however, it improved the inhibition of ${\beta}$-carotene and linoleic acid oxidation and the lipid peroxidation. This suggested that the fermentation of RGE is effective for producing ginsenoside Rd as precursor of ginsenoside compound K and inhibition of lipid oxidation. Conclusion: This study showed that RGE fermented by L. plantarum KCCM 11613P may contribute to the development of functional food materials.

Keywords

References

  1. Im K, Kim J, Min H. Ginseng, the natural effectual antiviral: protective effects of Korean red ginseng against viral infection. J Ginseng Res 2016;40:309-14. https://doi.org/10.1016/j.jgr.2015.09.002
  2. Kopalli SR, Won YJ, Hwang SY, Cha KM, Kim SY, Han CK, Lee SH, Hong JY, Kim SK. Korean red ginseng protects against doxorubicin-induced testicular damage: an experimental study in rats. J Funct Foods 2016;20:96-107. https://doi.org/10.1016/j.jff.2015.10.020
  3. Yun TK. Brief introduction of Panax ginseng C.A. Meyer. J Korean Med Sci 2001;16:S3-5. https://doi.org/10.3346/jkms.2001.16.S.S3
  4. Lee D, Kang KS, Yu JS, Woo JY, Hwang GS, Eom DW, Baek SH, Lee HL, Kim KH, Yamabe N. Protective effect of Korean red ginseng against FK-506-induced damage in LLC-PK1 cells. J Ginseng Res 2017;41:284-9. https://doi.org/10.1016/j.jgr.2016.05.002
  5. Kim JK, Cui CH, Yoon MH, Kim SC, Im WT. Bioconversion of major ginsenosides Rg1 to minor ginsenoside F1 using novel recombinant ginsenoside hydrolyzing glycosidase cloned from Sanguibacter keddieii and enzyme characterization. J Biotechnol 2012;161:294-301. https://doi.org/10.1016/j.jbiotec.2012.06.021
  6. Song H, Lee YJ. Inhibition of hypoxia-induced cyclooxygenase-2 by Korean red ginseng is dependent on peroxisome proliferator-activated receptor gamma. J Ginseng Res 2017;41:240-6. https://doi.org/10.1016/j.jgr.2016.04.001
  7. Lee YM, Yoon H, Park HM, Song BC, Yeum KJ. Implications of red Panax ginseng in oxidative stress associated chronic diseases. J Ginseng Res 2017;41:113-9. https://doi.org/10.1016/j.jgr.2016.03.003
  8. Kim BG, Choi SY, Kim MR, Suh HJ, Park HJ. Changes of ginsenosides in Korean red ginseng (Panax ginseng) fermented by Lactobacillus plantarum M1. Process Biochem 2010;45:1319-24. https://doi.org/10.1016/j.procbio.2010.04.026
  9. Park SE, Na CS, Yoo SA, Seo SH, Son HS. Biotransformation of major ginsenosides in ginsenoside model culture by lactic acid bacteria. J Ginseng Res 2017;41:36-42. https://doi.org/10.1016/j.jgr.2015.12.008
  10. Liu C, Zuo K, Yu H, Sun C, Zhang T, Xu L, Jin Y, Im WT, Jin F. Preparation of minor ginsenosides C-Mx and C-K from notoginseng leaf ginsenosides by a special ginsenoside type-I. Process Biochem 2015;50:2158-67. https://doi.org/10.1016/j.procbio.2015.10.011
  11. Yang XD, Yang YY, Ouyang DS, Yang GP. A review of biotransformation and pharmacology of ginsenoside compound K. Fitoterapia 2015;100:208-20. https://doi.org/10.1016/j.fitote.2014.11.019
  12. Lee SJ, Kim Y, Kim MG. Changes in the ginsenoside content during the fermentation process using microbial strains. J Ginseng Res 2015;39:392-7. https://doi.org/10.1016/j.jgr.2015.05.005
  13. Chang KH, Jo MN, Kim KT, Paik HD. Purification and characterization of a ginsenoside $Rb_{1}$-hydrolyzing ${\beta}$-glucosidase from Aspergillus niger KCCM 11239. Int J Mol Sci 2012;13:12140-52. https://doi.org/10.3390/ijms130912140
  14. Bai Y, Ganzle MG. Conversion of ginsenosides by Lactobacillus plantarum studied by liquid chromatography coupled to quadrupole trap mass spectrometry. Food Res Int 2015;76:709-18. https://doi.org/10.1016/j.foodres.2015.07.040
  15. Jo MN, Jung JE, Yoon HJ, Chang KH, Jee HS, Kim KT, Paik HD. Bioconversion of ginsenoside Rb1 to the pharmaceutical ginsenoside compound K using Aspergillus usamii KCTC 6954. Korean J Microbiol Biotechnol 2014;42:347-53. https://doi.org/10.4014/kjmb.1407.07010
  16. Nout MJR, Motarjemi Y. Assessment of fermentation as a household technology for improving food safety: a joint FAO/WHO workshop. Food Control 1997;8:221-6. https://doi.org/10.1016/S0956-7135(97)00021-2
  17. Li P, Gu Q. Complete genome sequence of Lactobacillus plantarum LZ95, a potential probiotic strain producing bacteriocins and B-group vitamin riboflavin. J Biotechnol 2016;229:1-2. https://doi.org/10.1016/j.jbiotec.2016.04.048
  18. Zhang Z, Tao X, Shah NP, Wei H. Antagonistics against pathogenic Bacillus cereus in milk fermentation by Lactobacillus plantarum ZDY2013 and its anti-adhesion effect on Caco-2 cells against pathogens. J Dairy Sci 2016;99:2666-74. https://doi.org/10.3168/jds.2015-10587
  19. Lee NK, Kim SY, Han KJ, Eom SJ, Paik HD. Probiotic potential of Lactobacillus strains with anti-allergic effects from kimchi for yogurt starters. LWT-Food Sci Technol 2014;58:130-4. https://doi.org/10.1016/j.lwt.2014.02.028
  20. Hugo AA, Bruno F, Golowczyc MA. Whey permeate containing galactooligosaccharides as a medium for biomass production and spray drying of Lactobacillus plantarum CIDCA 83114. LWT-Food Sci Technol 2016;69:185-90. https://doi.org/10.1016/j.lwt.2016.01.031
  21. Collins JL, Ebah CB, Mount JR, Demott BJ, Draughon FA. Production and evaluation of milk-sweet potato mixtures fermented with yogurt bacteria. J Food Sci 1991;56:685-8. https://doi.org/10.1111/j.1365-2621.1991.tb05356.x
  22. Chang KH, Jee HS, Lee NK, Park SH, Lee NW, Paik HD. Optimization of the enzymatic production of 20(S)-ginsenoside Rg3 from white ginseng extract using response surface methodology. New Biotechnol 2009;26:181-6. https://doi.org/10.1016/j.nbt.2009.08.011
  23. Lee KA, Kim KT, Kim HJ, Chung MS, Chang PS, Park H, Paik HD. Antioxidant activities of onion (Allium cepa L.) peel extracts produced by ethanol, hot water, and subcritical water extraction. Food Sci Biotechnol 2014;23:615-21. https://doi.org/10.1007/s10068-014-0084-6
  24. Xiao Y, Wang L, Rui X, Li W, Chen X, Jiang M, Dong M. Enhancement of the antioxidant capacity of soy whey by fermentation with Lactobacillus plantarum B1-6. J Funct Foods 2015;12:33-44. https://doi.org/10.1016/j.jff.2014.10.033
  25. Park EH, Kim HS, Eom SJ, Kim KT, Paik HD. Antioxidative and anticanceric activities of Magnolia (Magnolia denudate) flower petal extract fermented by Pediococcus acidilactici KCCM 11614. Molecules 2015;20:12154-65. https://doi.org/10.3390/molecules200712154
  26. Jung JE, Yoon HJ, Yu HS, Lee NK, Jee HS, Paik HD. Physicochemical and antioxidant properties of milk supplemented with red ginseng extract. J Dairy Sci 2015;98:95-9. https://doi.org/10.3168/jds.2014-8476
  27. Sung SK, Rhee YK, Cho CW, Kim YC, Lee OH, Hong HD. Physicochemical properties and antioxidative activity of fermented Rhodiola sachalinensis and Korean red ginseng mixture by Lactobacillus acidophilus. Korean J Food Nutr 2013;26:358-65. https://doi.org/10.9799/ksfan.2013.26.3.358
  28. Park JH, Moon HJ, Oh JH, Lee JH, Jung HK, Choi KM, Cha JD, Lim JY, Han SB. B Tae. Changes in the functional components of Lactobacillus acidophilus-fermented red ginseng extract and its application to fresh cheese production. Korean J Dairy Sci Technol 2014;32:47-53.
  29. Hasegawa H. Proof of the mysterious efficacy of ginseng: basic and clinical trials: metabolic activation of ginsenoside: deglycosylation by intestinal bacteria and esterification with fatty acid. J Pharmacol Sci 2004;95:153-7. https://doi.org/10.1254/jphs.FMJ04001X4
  30. Feng L, Xu C, Li Z, Li J, Dai Y, Han H, Yu S, Liu S. Microbial conversion of ginsenoside Rd from Rb1 by the fungus mutant Aspergillus niger strain TH-10a. Prep Biochem Biotechnol 2016;46:336-41. https://doi.org/10.1080/10826068.2015.1031391
  31. Jhan JK, Chang WF, Wang PM, Chou ST, Chung YC. Production of fermented red beans with multiple bioactivities using co-cultures of Bacillus subtilis and Lactobacillus delbrueckii subsp. bulgaricus. LWT-Food Sci Technol 2015;63:1281-7. https://doi.org/10.1016/j.lwt.2015.03.107
  32. Jung K, An JM, Eom DW, Kang KS, Kim SN. Preventive effect of fermented black ginseng against cisplatin-induced nephrotoxicity in rats. J Ginseng Res 2017;41:188-94. https://doi.org/10.1016/j.jgr.2016.03.001
  33. Liyana-Pathirana CM, Shahidi F. Antioxidant activity of commercial soft and hard wheat (Triticum aestivum L.) as affected by gastric pH conditions. J Agric Food Chem 2005;53:2433-40. https://doi.org/10.1021/jf049320i
  34. Boligon AA, Machado MM, Athayde ML. Technical evaluation of antioxidant activity. Med Chem 2014;4:517-22.
  35. Elfahri KR, Vasiljevic T, Yeager T, Donkor ON. Anti-colon cancer and antioxidant activities of bovine skim milk fermented by selected Lactobacillus helveticus strains. J Dairy Sci 2016;99:31-40. https://doi.org/10.3168/jds.2015-10160
  36. Sah BNP, Vasiljevic T, Mckechnie S, Conkor ON. Effect of probiotics on antioxidant and antimutagenic activities of crude peptide extract from yogurt. Food Chem 2014;156:264-70. https://doi.org/10.1016/j.foodchem.2014.01.105
  37. Jayanthi P, Lalitha P. Reducing power of the solvent extracts of Eichhornia crassipes (Mart.) solms. Int J Pharm Pharm Sci 2011;3:126-8.
  38. Lee YL, Yang JH, Mau JL. Antioxidant properties of water extracts from Monascus fermented soybeans. Food Chem 2008;106:1128-37. https://doi.org/10.1016/j.foodchem.2007.07.047
  39. Kato S, Aoshima H, Saitoh Y, Miwa N. Highly hydroxylated or ${\gamma}$-cyclodextrinbicapped water-soluble derivative of fullerene: the antioxidant ability assessed by electron spin resonance method and ${\beta}$-carotene bleaching assay. Bioorg Med Chem Lett 2009;19:5293-6. https://doi.org/10.1016/j.bmcl.2009.07.149
  40. Ibrahim NA, Mustafa S, Ismail A. Effect of lactic fermentation on the antioxidant capacity of Malaysian herbal teas. Int Food Res J 2014;21:1483-8.
  41. Zhang YX, Wang L, Xiao EL, Li SJ, Chen JJ, Gao B, Min GN, Wang ZP, Wu YJ. Ginsenoside-Rd exhibits anti-inflammatory activities through elevation of antioxidant enzyme activities and inhibition of JNK and ERK activation in vivo. Int Immunopharmacol 2013;17:1094-100. https://doi.org/10.1016/j.intimp.2013.10.013
  42. Ye R, Kong X, Yang Q, Zhang Y, Han J, Zhao G. Ginsenoside Rd attenuates redox imbalance and improves stroke outcome after focal cerebral ischemia in aged mice. Neuropharmacology 2011;61:815-24. https://doi.org/10.1016/j.neuropharm.2011.05.029
  43. Zamora R, Hidalgo FJ. The triple defensive barrier of phenolic compounds against the lipid oxidation-induced damage in food products. Trends Food Sci Technol 2016;54:165-74. https://doi.org/10.1016/j.tifs.2016.06.006

Cited by

  1. Lactobacillus plantarum with Functional Properties: An Approach to Increase Safety and Shelf-Life of Fermented Foods vol.2018, 2018, https://doi.org/10.1155/2018/9361614
  2. Protective effects of enhanced minor ginsenosides in Lactobacillus fermentum KP-3-fermented ginseng in mice fed a high fat diet vol.9, pp.11, 2018, https://doi.org/10.1039/c8fo01056k
  3. Functional Regulation of Ginsenosides on Myeloid Immunosuppressive Cells in the Tumor Microenvironment vol.18, 2019, https://doi.org/10.1177/1534735419886655
  4. Improved Antioxidant, Anti-inflammatory, and Anti-adipogenic Properties of Hydroponic Ginseng Fermented by Leuconostoc mesenteroides KCCM 12010P vol.24, pp.18, 2019, https://doi.org/10.3390/molecules24183359
  5. Combination therapy of ginsenoside compound K and methotrexate was efficient in elimination of anaemia and reduction of disease activity in adjuvant-induced arthritis rats vol.58, pp.1, 2019, https://doi.org/10.1080/13880209.2020.1844761
  6. Cooperated biotransformation of ginsenoside extracts into ginsenoside 20(S)‐Rg3 by three thermostable glycosidases vol.128, pp.3, 2020, https://doi.org/10.1111/jam.14513
  7. Preventive Effect of Fermented Chestnut Inner Shell Extract on Obesity-Induced Hepatic Steatosis vol.25, pp.1, 2020, https://doi.org/10.3746/pnf.2020.25.1.32
  8. Endophytes, biotransforming microorganisms, and engineering microbial factories for triterpenoid saponins production vol.41, pp.2, 2019, https://doi.org/10.1080/07388551.2020.1869691
  9. Fermented Red Ginseng Alleviates Ovalbumin-Induced Inflammation in Mice by Suppressing Interleukin-4 and Immunoglobulin E Expression vol.24, pp.6, 2021, https://doi.org/10.1089/jmf.2020.4854
  10. Production of minor ginsenosides by combining Stereum hirsutum and cellulase vol.16, pp.8, 2019, https://doi.org/10.1371/journal.pone.0255899
  11. Pharmacological properties of ginsenosides in inflammation-derived cancers vol.476, pp.9, 2021, https://doi.org/10.1007/s11010-021-04162-w
  12. Antioxidant Activity and Inhibitory Effect on Nitric Oxide Production of Hydroponic Ginseng Fermented with Lactococcus lactis KC24 vol.10, pp.10, 2019, https://doi.org/10.3390/antiox10101614
  13. Probiotics-Mediated Bioconversion and Periodontitis vol.41, pp.6, 2021, https://doi.org/10.5851/kosfa.2021.e57