Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats

Traditionally made doenjang (TMD) produced by the long-term fermentation of soybeans with salt may improve symptoms of estrogen deficiency. We aimed to evaluate the effects of four TMD types, containing low and high amounts of <i>Bacillus</i> species and biogenic amines (HBHA, HBLA, LBHA...

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Main Authors: Ting Zhang, Yu Yue, Su-Ji Jeong, Myeong-Seon Ryu, Xuangao Wu, Hee-Jong Yang, Chen Li, Do-Youn Jeong, Sunmin Park
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Foods
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Online Access:https://www.mdpi.com/2304-8158/12/6/1143
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author Ting Zhang
Yu Yue
Su-Ji Jeong
Myeong-Seon Ryu
Xuangao Wu
Hee-Jong Yang
Chen Li
Do-Youn Jeong
Sunmin Park
author_facet Ting Zhang
Yu Yue
Su-Ji Jeong
Myeong-Seon Ryu
Xuangao Wu
Hee-Jong Yang
Chen Li
Do-Youn Jeong
Sunmin Park
author_sort Ting Zhang
collection DOAJ
description Traditionally made doenjang (TMD) produced by the long-term fermentation of soybeans with salt may improve symptoms of estrogen deficiency. We aimed to evaluate the effects of four TMD types, containing low and high amounts of <i>Bacillus</i> species and biogenic amines (HBHA, HBLA, LBHA, and LBLA), on energy, glucose, and lipid metabolism, by altering the gut microbiota in estrogen-deficient ovariectomized (OVX) rats. Their mechanisms were also examined. The OVX rats were divided into the control, cooked soybean (CSB), HBHA, LBHA, HBLA, and LBLA groups. Sham-operated rats were the normal control group. Serum 17β-estradiol concentrations were similar among all OVX groups. Tail skin temperatures, which are indicative of hot flashes, were higher in the control than the HBHA and HBLA groups and were similar to the normal control group. Weight gain and visceral fat mass were lower in the TMD and CSB intake groups but not as low as in the normal control group. Lean body mass showed a trend opposite to that of visceral fat in the respective groups. The hepatic triglyceride content decreased with the TMD intake compared to the control and CSB groups. mRNA expressions of the peroxisome proliferator-activated receptor-γ (<i>PPAR-γ</i>) and carnitine palmitoyltransferase-1 in the TMD and CSB groups were as high as in the normal control group, and the <i>PPAR-γ</i> mRNA expression was more elevated in the HBLA group than in the normal control group. The morphology of the intestines improved in the TMD groups compared to the control, and the HBHA and HBLA groups showed an enhanced improvement compared to the CSB group. The HBHA, HBLA, and LBHA groups increased the α-diversity of the cecal microbiota compared to the control. <i>Akkermenia</i> and <i>Lactobacillus</i> were higher in the HBLA and LBLA groups compared to the control. The expression of the estrogen, forkhead box proteins of the class-O subgroup, and insulin-signaling pathways were lower in the control group, and HBHA and HBLA prevented their decrement. In conclusion, long-term treatment with TMD containing high amounts of <i>Bacillus</i> potentially improves estrogen deficiency symptoms more than unfermented soybeans.
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spelling doaj.art-5f07d1b485bc44aba28728dfc602a0042023-11-17T11:05:20ZengMDPI AGFoods2304-81582023-03-01126114310.3390/foods12061143Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient RatsTing Zhang0Yu Yue1Su-Ji Jeong2Myeong-Seon Ryu3Xuangao Wu4Hee-Jong Yang5Chen Li6Do-Youn Jeong7Sunmin Park8Department of Bioconvergence, Hoseo University, 20 hoseoro79bun-gil, Baebang-yup, Asan 31499, Republic of KoreaObesity/Diabetes Research Center, Department of Food and Nutrition, Hoseo University, Asan 31499, Republic of KoreaSunchang Research Center for Fermentation Microbes, Department of R & D, Microbial Institute for Fermentation Industry, 61-27 Minsokmaeul-gil, Sunchang-Gun 56048, Republic of KoreaSunchang Research Center for Fermentation Microbes, Department of R & D, Microbial Institute for Fermentation Industry, 61-27 Minsokmaeul-gil, Sunchang-Gun 56048, Republic of KoreaDepartment of Bioconvergence, Hoseo University, 20 hoseoro79bun-gil, Baebang-yup, Asan 31499, Republic of KoreaSunchang Research Center for Fermentation Microbes, Department of R & D, Microbial Institute for Fermentation Industry, 61-27 Minsokmaeul-gil, Sunchang-Gun 56048, Republic of KoreaObesity/Diabetes Research Center, Department of Food and Nutrition, Hoseo University, Asan 31499, Republic of KoreaSunchang Research Center for Fermentation Microbes, Department of R & D, Microbial Institute for Fermentation Industry, 61-27 Minsokmaeul-gil, Sunchang-Gun 56048, Republic of KoreaDepartment of Bioconvergence, Hoseo University, 20 hoseoro79bun-gil, Baebang-yup, Asan 31499, Republic of KoreaTraditionally made doenjang (TMD) produced by the long-term fermentation of soybeans with salt may improve symptoms of estrogen deficiency. We aimed to evaluate the effects of four TMD types, containing low and high amounts of <i>Bacillus</i> species and biogenic amines (HBHA, HBLA, LBHA, and LBLA), on energy, glucose, and lipid metabolism, by altering the gut microbiota in estrogen-deficient ovariectomized (OVX) rats. Their mechanisms were also examined. The OVX rats were divided into the control, cooked soybean (CSB), HBHA, LBHA, HBLA, and LBLA groups. Sham-operated rats were the normal control group. Serum 17β-estradiol concentrations were similar among all OVX groups. Tail skin temperatures, which are indicative of hot flashes, were higher in the control than the HBHA and HBLA groups and were similar to the normal control group. Weight gain and visceral fat mass were lower in the TMD and CSB intake groups but not as low as in the normal control group. Lean body mass showed a trend opposite to that of visceral fat in the respective groups. The hepatic triglyceride content decreased with the TMD intake compared to the control and CSB groups. mRNA expressions of the peroxisome proliferator-activated receptor-γ (<i>PPAR-γ</i>) and carnitine palmitoyltransferase-1 in the TMD and CSB groups were as high as in the normal control group, and the <i>PPAR-γ</i> mRNA expression was more elevated in the HBLA group than in the normal control group. The morphology of the intestines improved in the TMD groups compared to the control, and the HBHA and HBLA groups showed an enhanced improvement compared to the CSB group. The HBHA, HBLA, and LBHA groups increased the α-diversity of the cecal microbiota compared to the control. <i>Akkermenia</i> and <i>Lactobacillus</i> were higher in the HBLA and LBLA groups compared to the control. The expression of the estrogen, forkhead box proteins of the class-O subgroup, and insulin-signaling pathways were lower in the control group, and HBHA and HBLA prevented their decrement. In conclusion, long-term treatment with TMD containing high amounts of <i>Bacillus</i> potentially improves estrogen deficiency symptoms more than unfermented soybeans.https://www.mdpi.com/2304-8158/12/6/1143long-term fermented soybeansestrogen deficiency<i>Bacillus</i>biogenic aminesgut microbiotametagenome function
spellingShingle Ting Zhang
Yu Yue
Su-Ji Jeong
Myeong-Seon Ryu
Xuangao Wu
Hee-Jong Yang
Chen Li
Do-Youn Jeong
Sunmin Park
Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats
Foods
long-term fermented soybeans
estrogen deficiency
<i>Bacillus</i>
biogenic amines
gut microbiota
metagenome function
title Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats
title_full Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats
title_fullStr Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats
title_full_unstemmed Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats
title_short Improvement of Estrogen Deficiency Symptoms by the Intake of Long-Term Fermented Soybeans (Doenjang) Rich in <i>Bacillus</i> Species through Modulating Gut Microbiota in Estrogen-Deficient Rats
title_sort improvement of estrogen deficiency symptoms by the intake of long term fermented soybeans doenjang rich in i bacillus i species through modulating gut microbiota in estrogen deficient rats
topic long-term fermented soybeans
estrogen deficiency
<i>Bacillus</i>
biogenic amines
gut microbiota
metagenome function
url https://www.mdpi.com/2304-8158/12/6/1143
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