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Published in: BMC Complementary Medicine and Therapies 1/2018

Open Access 01-12-2018 | Research article

Enhancement of neuroprotective activity of Sagunja-tang by fermentation with lactobacillus strains

Authors: Nam-Hui Yim, Min Jung Gu, Hee Ra Park, Youn-Hwan Hwang, Jin Yeul Ma

Published in: BMC Complementary Medicine and Therapies | Issue 1/2018

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Abstract

Background

Sagunja-tang (SGT) is widely used in traditional herbal medicine to treat immune system and gastrointestinal disorders and reportedly has protective effects against inflammation, cancer, and osteoporosis. In this study, we fermented SGT with different Latobacillus strains and investigated the change in phytochemical compositions in SGT and enhancement of it neuroprotective effects in SH-SY5Y human neuroblastoma.

Methods

Marker components, including ginsenoside Rg1, glycyrrhizin, liquiritin, liquiritigenin, atractylenolide I, atractylenolide II, atractylenolide III, and pachymic acid, in SGT, were qualitatively and quantitatively analyzed using high-performance liquid chromatography–diode array detection and liquid chromatography–mass spectrometry. SGT was fermented with eight different Lactobacillus strains to yield eight fermented SGTs (FSGTs). The conversion efficiencies of SGT marker components were determined in each FSGT. To detect the protective effect of SGT and FSGT, reactive oxygen species (ROS) assay and mitochondrial membrane potentials (MMPs) assay were performed in SH-SY5Y cells.

Results

Compared with the other FSGTs, SGT166, i.e., SGT fermented with L. plantarum 166, had high conversion efficiency, as indicated by increased amounts of glycyrrhizin, liquiritigenin, and atractylenolides I–III. In SH-SY5Y cells, protection against cell death induced by H2O2 and etoposide was high using SGT166 and very low using SGT. Furthermore, ROS production and mitochondrial membrane potential disruption in SH-SY5Y cells were markedly suppressed by SGT166 treatment, which demonstrated that inhibition of ROS generation may be one of the neuroprotective mechanisms of SGT166.

Conclusions

This study demonstrated that fermentation of SGT with L. plantarum 166 enhanced suppression of oxidative stress and MMP loss. This enhanced neuroprotective effect was thought to be caused by the conversion of SGT phytochemicals by fermentation. SGT166 shows potential for treating neurological damage-related diseases.
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Literature
1.
go back to reference Liu Y, Yang J, Cai Z. Chemical investigation on Sijunzi decoction and its two major herbs Panax ginseng and Glycyrrhiza uralensis by LC/MS/MS. J Pharm Biomed Anal. 2006;41(5):1642–7.CrossRef Liu Y, Yang J, Cai Z. Chemical investigation on Sijunzi decoction and its two major herbs Panax ginseng and Glycyrrhiza uralensis by LC/MS/MS. J Pharm Biomed Anal. 2006;41(5):1642–7.CrossRef
2.
go back to reference Lu Y, Lin H, Zhang J, Wei J, Sun J, Han L. Sijunzi decoction attenuates 2, 4, 6-trinitrobenzene sulfonic acid (TNBS)-induced colitis in rats and ameliorates TNBS-induced claudin-2 damage via NF-kappaB pathway in Caco2 cells. BMC Complement Altern Med. 2017;17(1):35.CrossRef Lu Y, Lin H, Zhang J, Wei J, Sun J, Han L. Sijunzi decoction attenuates 2, 4, 6-trinitrobenzene sulfonic acid (TNBS)-induced colitis in rats and ameliorates TNBS-induced claudin-2 damage via NF-kappaB pathway in Caco2 cells. BMC Complement Altern Med. 2017;17(1):35.CrossRef
3.
go back to reference Yu W, Lu B, Zhang H, Zhang Y, Yan J. Effects of the Sijunzi decoction on the immunological function in rats with dextran sulfate-induced ulcerative colitis. Biomed Rep. 2016;5(1):83–6.CrossRef Yu W, Lu B, Zhang H, Zhang Y, Yan J. Effects of the Sijunzi decoction on the immunological function in rats with dextran sulfate-induced ulcerative colitis. Biomed Rep. 2016;5(1):83–6.CrossRef
4.
go back to reference Zhao AG, Zhao HL, Jin XJ, Yang JK, Tang LD. Effects of Chinese Jianpi herbs on cell apoptosis and related gene expression in human gastric cancer grafted onto nude mice. World J Gastroenterol. 2002;8(5):792–6.CrossRef Zhao AG, Zhao HL, Jin XJ, Yang JK, Tang LD. Effects of Chinese Jianpi herbs on cell apoptosis and related gene expression in human gastric cancer grafted onto nude mice. World J Gastroenterol. 2002;8(5):792–6.CrossRef
5.
go back to reference Zheng J, Liu JL, Lin MF, Wang ZF, Liu CY, Wu XH, Lin HY, Chen CF, Zheng XM, Chen XY. Effect of modified sijunzi decoction on the bone metabolism of adriamycin induced nephropathy rats. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2013;33(10):1376–81.PubMed Zheng J, Liu JL, Lin MF, Wang ZF, Liu CY, Wu XH, Lin HY, Chen CF, Zheng XM, Chen XY. Effect of modified sijunzi decoction on the bone metabolism of adriamycin induced nephropathy rats. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2013;33(10):1376–81.PubMed
6.
go back to reference Kang A, Guo JR, Zhang Z, Wang XL. Simultaneous quantification of ten active components in traditional Chinese formula Sijunzi decoction using a UPLC-PDA method. J Anal Methods Chem. 2014;2014:570359. Kang A, Guo JR, Zhang Z, Wang XL. Simultaneous quantification of ten active components in traditional Chinese formula Sijunzi decoction using a UPLC-PDA method. J Anal Methods Chem. 2014;2014:570359.
7.
go back to reference Trinh HT, Han SJ, Kim SW, Lee YC, Kim DH. Bifidus fermentation increases hypolipidemic and hypoglycemic effects of red ginseng. J Microbiol Biotechnol. 2007;17(7):1127–33.PubMed Trinh HT, Han SJ, Kim SW, Lee YC, Kim DH. Bifidus fermentation increases hypolipidemic and hypoglycemic effects of red ginseng. J Microbiol Biotechnol. 2007;17(7):1127–33.PubMed
8.
go back to reference Dai Z, Liu Y, Zhang X, Shi M, Wang B, Wang D, Huang L, Zhang X. Metabolic engineering of Saccharomyces cerevisiae for production of ginsenosides. Metab Eng. 2013;20:146–56.CrossRef Dai Z, Liu Y, Zhang X, Shi M, Wang B, Wang D, Huang L, Zhang X. Metabolic engineering of Saccharomyces cerevisiae for production of ginsenosides. Metab Eng. 2013;20:146–56.CrossRef
9.
go back to reference Marazza JA, Garro MS, de Giori GS. Aglycone production by lactobacillus rhamnosus CRL981 during soymilk fermentation. Food Microbiol. 2009;26(3):333–9.CrossRef Marazza JA, Garro MS, de Giori GS. Aglycone production by lactobacillus rhamnosus CRL981 during soymilk fermentation. Food Microbiol. 2009;26(3):333–9.CrossRef
10.
go back to reference Ng CC, Wang CY, Wang YP, Tzeng WS, Shyu YT. Lactic acid bacterial fermentation on the production of functional antioxidant herbal Anoectochilus formosanus Hayata. J Biosci Bioeng. 2011;111(3):289–93.CrossRef Ng CC, Wang CY, Wang YP, Tzeng WS, Shyu YT. Lactic acid bacterial fermentation on the production of functional antioxidant herbal Anoectochilus formosanus Hayata. J Biosci Bioeng. 2011;111(3):289–93.CrossRef
11.
go back to reference Oh YC, Cho WK, Jeong YH, Im GY, Yang MC, Ma JY. Fermentation improves anti-inflammatory effect of sipjeondaebotang on LPS-stimulated RAW 264.7 cells. Am J Chin Med. 2012;40(4):813–31.CrossRef Oh YC, Cho WK, Jeong YH, Im GY, Yang MC, Ma JY. Fermentation improves anti-inflammatory effect of sipjeondaebotang on LPS-stimulated RAW 264.7 cells. Am J Chin Med. 2012;40(4):813–31.CrossRef
12.
go back to reference Shim KS, Kim T, Ha H, Lee KJ, Cho CW, Kim HS, Seo DH, Ma JY. Lactobacillus fermentation enhances the inhibitory effect of Hwangryun-haedok-tang in an ovariectomy-induced bone loss. BMC Complement Altern Med. 2013;13:106.CrossRef Shim KS, Kim T, Ha H, Lee KJ, Cho CW, Kim HS, Seo DH, Ma JY. Lactobacillus fermentation enhances the inhibitory effect of Hwangryun-haedok-tang in an ovariectomy-induced bone loss. BMC Complement Altern Med. 2013;13:106.CrossRef
13.
go back to reference Lee JJ, Kwon H, Lee JH, Kim DG, Jung SH, Ma JY. Fermented soshiho-tang with lactobacillus plantarum enhances the antiproliferative activity in vascular smooth muscle cell. BMC Complement Altern Med. 2014;14:78.CrossRef Lee JJ, Kwon H, Lee JH, Kim DG, Jung SH, Ma JY. Fermented soshiho-tang with lactobacillus plantarum enhances the antiproliferative activity in vascular smooth muscle cell. BMC Complement Altern Med. 2014;14:78.CrossRef
14.
go back to reference Park HR, Lee H, Park H, Cho WK, Ma JY. Fermented Sipjeondaebo-tang alleviates memory deficits and loss of hippocampal neurogenesis in scopolamine-induced amnesia in mice. Sci Rep. 2016;6:22405.CrossRef Park HR, Lee H, Park H, Cho WK, Ma JY. Fermented Sipjeondaebo-tang alleviates memory deficits and loss of hippocampal neurogenesis in scopolamine-induced amnesia in mice. Sci Rep. 2016;6:22405.CrossRef
15.
go back to reference Hsieh HL, Yang CM. Role of redox signaling in neuroinflammation and neurodegenerative diseases. Biomed Res Int. 2013;2013:484613.PubMedPubMedCentral Hsieh HL, Yang CM. Role of redox signaling in neuroinflammation and neurodegenerative diseases. Biomed Res Int. 2013;2013:484613.PubMedPubMedCentral
16.
go back to reference Pollari E, Goldsteins G, Bart G, Koistinaho J, Giniatullin R. The role of oxidative stress in degeneration of the neuromuscular junction in amyotrophic lateral sclerosis. Front Cell Neurosci. 2014;8:131.CrossRef Pollari E, Goldsteins G, Bart G, Koistinaho J, Giniatullin R. The role of oxidative stress in degeneration of the neuromuscular junction in amyotrophic lateral sclerosis. Front Cell Neurosci. 2014;8:131.CrossRef
17.
go back to reference Padurariu M, Ciobica A, Lefter R, Serban IL, Stefanescu C, Chirita R. The oxidative stress hypothesis in Alzheimer’s disease. Psychiatr Danub. 2013;25(4):401–9.PubMed Padurariu M, Ciobica A, Lefter R, Serban IL, Stefanescu C, Chirita R. The oxidative stress hypothesis in Alzheimer’s disease. Psychiatr Danub. 2013;25(4):401–9.PubMed
18.
go back to reference Murakami S, Miyazaki I, Sogawa N, Miyoshi K, Asanuma M. Neuroprotective effects of metallothionein against rotenone-induced myenteric neurodegeneration in parkinsonian mice. Neurotox Res. 2014;26(3):285–98.CrossRef Murakami S, Miyazaki I, Sogawa N, Miyoshi K, Asanuma M. Neuroprotective effects of metallothionein against rotenone-induced myenteric neurodegeneration in parkinsonian mice. Neurotox Res. 2014;26(3):285–98.CrossRef
19.
go back to reference Liu CY, Lee CF, Wei YH. Role of reactive oxygen species-elicited apoptosis in the pathophysiology of mitochondrial and neurodegenerative diseases associated with mitochondrial DNA mutations. J Formos Med Assoc. 2009;108(8):599–611.CrossRef Liu CY, Lee CF, Wei YH. Role of reactive oxygen species-elicited apoptosis in the pathophysiology of mitochondrial and neurodegenerative diseases associated with mitochondrial DNA mutations. J Formos Med Assoc. 2009;108(8):599–611.CrossRef
20.
go back to reference Akopova OV, Kolchynskayia LY, Nosar VY, Smyrnov AN, Malisheva MK, Man'kovskaia YN, Sahach VF. The effect of permeability transition pore opening on reactive oxygen species production in rat brain mitochondria. Ukr Biokhim Zh (1999). 2011;83(6):46–55. Akopova OV, Kolchynskayia LY, Nosar VY, Smyrnov AN, Malisheva MK, Man'kovskaia YN, Sahach VF. The effect of permeability transition pore opening on reactive oxygen species production in rat brain mitochondria. Ukr Biokhim Zh (1999). 2011;83(6):46–55.
21.
go back to reference Park HR, Lee H, Park H, Jeon JW, Cho WK, Ma JY. Neuroprotective effects of Liriope platyphylla extract against hydrogen peroxide-induced cytotoxicity in human neuroblastoma SH-SY5Y cells. BMC Complement Altern Med. 2015;15:171.CrossRef Park HR, Lee H, Park H, Jeon JW, Cho WK, Ma JY. Neuroprotective effects of Liriope platyphylla extract against hydrogen peroxide-induced cytotoxicity in human neuroblastoma SH-SY5Y cells. BMC Complement Altern Med. 2015;15:171.CrossRef
22.
go back to reference Castro JJ, Gomez A, White B, Loften JR, Drackley JK. Changes in the intestinal bacterial community, short-chain fatty acid profile, and intestinal development of preweaned Holstein calves. 2. Effects of gastrointestinal site and age. J Dairy Sci. 2016;99(12):9703–15.CrossRef Castro JJ, Gomez A, White B, Loften JR, Drackley JK. Changes in the intestinal bacterial community, short-chain fatty acid profile, and intestinal development of preweaned Holstein calves. 2. Effects of gastrointestinal site and age. J Dairy Sci. 2016;99(12):9703–15.CrossRef
23.
go back to reference Masood MI, Qadir MI, Shirazi JH, Khan IU. Beneficial effects of lactic acid bacteria on human beings. Crit Rev Microbiol. 2011;37(1):91–8.CrossRef Masood MI, Qadir MI, Shirazi JH, Khan IU. Beneficial effects of lactic acid bacteria on human beings. Crit Rev Microbiol. 2011;37(1):91–8.CrossRef
24.
go back to reference Michlmayr H, Schumann C, da Silva NM, Kulbe KD, del Hierro AM. Isolation and basic characterization of a beta-glucosidase from a strain of lactobacillus brevis isolated from a malolactic starter culture. J Appl Microbiol. 2010;108(2):550–9.CrossRef Michlmayr H, Schumann C, da Silva NM, Kulbe KD, del Hierro AM. Isolation and basic characterization of a beta-glucosidase from a strain of lactobacillus brevis isolated from a malolactic starter culture. J Appl Microbiol. 2010;108(2):550–9.CrossRef
25.
go back to reference Cho CW, Jeong HC, Hong HD, Kim YC, Choi SY, Kim K, Ma JY, Lee YC. Bioconversion of isoflavones during the fermentation of Samso-Eum with lactobacillus strains. Biotechnol Bioprocess Eng. 2012;17(5):1062–7.CrossRef Cho CW, Jeong HC, Hong HD, Kim YC, Choi SY, Kim K, Ma JY, Lee YC. Bioconversion of isoflavones during the fermentation of Samso-Eum with lactobacillus strains. Biotechnol Bioprocess Eng. 2012;17(5):1062–7.CrossRef
26.
go back to reference Glavac NK, Kreft S. Excretion profile of glycyrrhizin metabolite in human urine. Food Chem. 2012;131(1):305–8.CrossRef Glavac NK, Kreft S. Excretion profile of glycyrrhizin metabolite in human urine. Food Chem. 2012;131(1):305–8.CrossRef
27.
go back to reference Li J, Liu S, Wang J, Li J, Li J, Gao W. Gene expression of glycyrrhizin acid and accumulation of endogenous signaling molecule in Glycyrrhiza uralensis Fisch adventitious roots after Saccharomyces cerevisiae and Meyerozyma guilliermondii applications. Biotechnol Appl Biochem. 2017;64(5):700–11.CrossRef Li J, Liu S, Wang J, Li J, Li J, Gao W. Gene expression of glycyrrhizin acid and accumulation of endogenous signaling molecule in Glycyrrhiza uralensis Fisch adventitious roots after Saccharomyces cerevisiae and Meyerozyma guilliermondii applications. Biotechnol Appl Biochem. 2017;64(5):700–11.CrossRef
28.
go back to reference Yang HJ, Yim NH, Lee KJ, Gu MJ, Lee B, Hwang YH, Ma JY. Simultaneous determination of nine bioactive compounds in Yijin-tang via high-performance liquid chromatography and liquid chromatography-electrospray ionization-mass spectrometry. Integr Med Res. 2016;5(2):140–50.CrossRef Yang HJ, Yim NH, Lee KJ, Gu MJ, Lee B, Hwang YH, Ma JY. Simultaneous determination of nine bioactive compounds in Yijin-tang via high-performance liquid chromatography and liquid chromatography-electrospray ionization-mass spectrometry. Integr Med Res. 2016;5(2):140–50.CrossRef
29.
go back to reference Dai DF, Chiao YA, Marcinek DJ, Szeto HH, Rabinovitch PS. Mitochondrial oxidative stress in aging and healthspan. Longev Healthspan. 2014;3:6.CrossRef Dai DF, Chiao YA, Marcinek DJ, Szeto HH, Rabinovitch PS. Mitochondrial oxidative stress in aging and healthspan. Longev Healthspan. 2014;3:6.CrossRef
30.
go back to reference Lee HK, Yang EJ, Kim JY, Song KS, Seong YH. Inhibitory effects of Glycyrrhizae radix and its active component, isoliquiritigenin, on Abeta(25-35)-induced neurotoxicity in cultured rat cortical neurons. Arch Pharm Res. 2012;35(5):897–904.CrossRef Lee HK, Yang EJ, Kim JY, Song KS, Seong YH. Inhibitory effects of Glycyrrhizae radix and its active component, isoliquiritigenin, on Abeta(25-35)-induced neurotoxicity in cultured rat cortical neurons. Arch Pharm Res. 2012;35(5):897–904.CrossRef
31.
go back to reference Gao Q, Ji ZH, Yang Y, Cheng R, Yu XY. Neuroprotective effect of Rhizoma Atractylodis macrocephalae against excitotoxicity-induced apoptosis in cultured cerebral cortical neurons. Phytother Res. 2012;26(4):557–61.CrossRef Gao Q, Ji ZH, Yang Y, Cheng R, Yu XY. Neuroprotective effect of Rhizoma Atractylodis macrocephalae against excitotoxicity-induced apoptosis in cultured cerebral cortical neurons. Phytother Res. 2012;26(4):557–61.CrossRef
32.
go back to reference Ji ZH, Liu C, Zhao H, Yu XY. Neuroprotective effect of biatractylenolide against memory impairment in D-galactose-induced aging mice. J Mol Neurosci. 2015;55(3):678–83.CrossRef Ji ZH, Liu C, Zhao H, Yu XY. Neuroprotective effect of biatractylenolide against memory impairment in D-galactose-induced aging mice. J Mol Neurosci. 2015;55(3):678–83.CrossRef
33.
go back to reference Liu C, Zhao H, Ji ZH, Yu XY. Neuroprotection of atractylenolide III from Atractylodis macrocephalae against glutamate-induced neuronal apoptosis via inhibiting caspase signaling pathway. Neurochem Res. 2014;39(9):1753–8.CrossRef Liu C, Zhao H, Ji ZH, Yu XY. Neuroprotection of atractylenolide III from Atractylodis macrocephalae against glutamate-induced neuronal apoptosis via inhibiting caspase signaling pathway. Neurochem Res. 2014;39(9):1753–8.CrossRef
34.
go back to reference More S, Choi DK. Neuroprotective role of Atractylenolide-I in an in vitro and in vivo model of Parkinson’s disease. Nutrients. 2017;9(5):451. More S, Choi DK. Neuroprotective role of Atractylenolide-I in an in vitro and in vivo model of Parkinson’s disease. Nutrients. 2017;9(5):451.
Metadata
Title
Enhancement of neuroprotective activity of Sagunja-tang by fermentation with lactobacillus strains
Authors
Nam-Hui Yim
Min Jung Gu
Hee Ra Park
Youn-Hwan Hwang
Jin Yeul Ma
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2018
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-018-2361-z

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