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Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota

BACKGROUND: Obesity is a major risk factor for a variety of diseases such as diabetes, nonalcoholic fatty liver disease, and cardiovascular diseases. Restricting energy intake, or caloric restriction (CR), can reduce body weight and improve metabolic parameters in overweight or obese patients. We pr...

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Autores principales: Liu, Meng-Ting, Huang, Ying-Juan, Zhang, Ting-Ying, Tan, Lun-Bo, Lu, Xi-Feng, Qin, Jian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Baishideng Publishing Group Inc 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658390/
https://www.ncbi.nlm.nih.gov/pubmed/31367159
http://dx.doi.org/10.3748/wjg.v25.i27.3590
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author Liu, Meng-Ting
Huang, Ying-Juan
Zhang, Ting-Ying
Tan, Lun-Bo
Lu, Xi-Feng
Qin, Jian
author_facet Liu, Meng-Ting
Huang, Ying-Juan
Zhang, Ting-Ying
Tan, Lun-Bo
Lu, Xi-Feng
Qin, Jian
author_sort Liu, Meng-Ting
collection PubMed
description BACKGROUND: Obesity is a major risk factor for a variety of diseases such as diabetes, nonalcoholic fatty liver disease, and cardiovascular diseases. Restricting energy intake, or caloric restriction (CR), can reduce body weight and improve metabolic parameters in overweight or obese patients. We previously found that Lingguizhugan decoction (LZD) in combination with CR can effectively lower plasma lipid levels in patients with metabolic syndrome. However, the mechanism underlying CR and LZD treatment is still unclear. AIM: To investigate whether CR and LZD improve metabolic parameters by modulating gut microbiota. METHODS: We extracted the water-soluble components out of raw materials and dried as LZD extracts. Eight-week old male C57BL/6 mice were treated with a 3-d treatment regime that included 24 h-fasting followed by gavage of LZD extracts for 2 consecutive days, followed by a normal diet (ND) ad libitum for 16 wk. To test the effects of gut microbiota on diet-induced obesity, 8-wk old male C57BL/6 mice received fecal microbiota transplantation (FMT) from CR and LZD-treated mice every 3 d and were fed with high-fat diet (HFD) ad libitum for 16 wk. Control mice received either saline gavage or FMT from ND-fed mice receiving saline gavage as mentioned above. Body weight was monitored bi-weekly. Food consumption of each cage hosting five mice was recorded weekly. To monitor blood glucose, total cholesterol, and total triglycerides, blood samples were collected via submandibular bleeding after 6 h fasting. Oxygen consumption rate was monitored with metabolic cages. Feces were collected, and fecal DNA was extracted. Profiles of gut microbiota were mapped by metagenomic sequencing. RESULTS: We found that CR and LZD treatment significantly reduced the body weight of mice fed with ND (28.71 ± 0.29 vs 28.05 ± 0.15, P < 0.05), but did not affect plasma total cholesterol or total triglyceride levels. We then transplanted the fecal microbiota collected from CR and LZD-treated mice under ND feeding to HFD-fed mice. Intriguingly, transplanting the mice with fecal microbiota from CR and LZD-treated mice potently reduced body weight (44.95 ± 1.02 vs 40.53 ± 0.97, P < 0.001). FMT also reduced HFD-induced hepatosteatosis, in addition to improved glycemic control. Mechanistic studies found that FMT increased OCR of the mice and suppressed the expression and protein abundance of lipogenic genes in the liver. Metagenomic analysis revealed that HFD drastically altered the profile of gut microbiota, and FMT modified the profile of the gut microbiota. CONCLUSION: Our study suggests that CR and LZD improve metabolic parameters by modulating gut microbiota.
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spelling pubmed-66583902019-07-31 Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota Liu, Meng-Ting Huang, Ying-Juan Zhang, Ting-Ying Tan, Lun-Bo Lu, Xi-Feng Qin, Jian World J Gastroenterol Basic Study BACKGROUND: Obesity is a major risk factor for a variety of diseases such as diabetes, nonalcoholic fatty liver disease, and cardiovascular diseases. Restricting energy intake, or caloric restriction (CR), can reduce body weight and improve metabolic parameters in overweight or obese patients. We previously found that Lingguizhugan decoction (LZD) in combination with CR can effectively lower plasma lipid levels in patients with metabolic syndrome. However, the mechanism underlying CR and LZD treatment is still unclear. AIM: To investigate whether CR and LZD improve metabolic parameters by modulating gut microbiota. METHODS: We extracted the water-soluble components out of raw materials and dried as LZD extracts. Eight-week old male C57BL/6 mice were treated with a 3-d treatment regime that included 24 h-fasting followed by gavage of LZD extracts for 2 consecutive days, followed by a normal diet (ND) ad libitum for 16 wk. To test the effects of gut microbiota on diet-induced obesity, 8-wk old male C57BL/6 mice received fecal microbiota transplantation (FMT) from CR and LZD-treated mice every 3 d and were fed with high-fat diet (HFD) ad libitum for 16 wk. Control mice received either saline gavage or FMT from ND-fed mice receiving saline gavage as mentioned above. Body weight was monitored bi-weekly. Food consumption of each cage hosting five mice was recorded weekly. To monitor blood glucose, total cholesterol, and total triglycerides, blood samples were collected via submandibular bleeding after 6 h fasting. Oxygen consumption rate was monitored with metabolic cages. Feces were collected, and fecal DNA was extracted. Profiles of gut microbiota were mapped by metagenomic sequencing. RESULTS: We found that CR and LZD treatment significantly reduced the body weight of mice fed with ND (28.71 ± 0.29 vs 28.05 ± 0.15, P < 0.05), but did not affect plasma total cholesterol or total triglyceride levels. We then transplanted the fecal microbiota collected from CR and LZD-treated mice under ND feeding to HFD-fed mice. Intriguingly, transplanting the mice with fecal microbiota from CR and LZD-treated mice potently reduced body weight (44.95 ± 1.02 vs 40.53 ± 0.97, P < 0.001). FMT also reduced HFD-induced hepatosteatosis, in addition to improved glycemic control. Mechanistic studies found that FMT increased OCR of the mice and suppressed the expression and protein abundance of lipogenic genes in the liver. Metagenomic analysis revealed that HFD drastically altered the profile of gut microbiota, and FMT modified the profile of the gut microbiota. CONCLUSION: Our study suggests that CR and LZD improve metabolic parameters by modulating gut microbiota. Baishideng Publishing Group Inc 2019-07-21 2019-07-21 /pmc/articles/PMC6658390/ /pubmed/31367159 http://dx.doi.org/10.3748/wjg.v25.i27.3590 Text en ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved. http://creativecommons.org/licenses/by-nc/4.0/ This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial.
spellingShingle Basic Study
Liu, Meng-Ting
Huang, Ying-Juan
Zhang, Ting-Ying
Tan, Lun-Bo
Lu, Xi-Feng
Qin, Jian
Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
title Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
title_full Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
title_fullStr Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
title_full_unstemmed Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
title_short Lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
title_sort lingguizhugan decoction attenuates diet-induced obesity and hepatosteatosis via gut microbiota
topic Basic Study
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658390/
https://www.ncbi.nlm.nih.gov/pubmed/31367159
http://dx.doi.org/10.3748/wjg.v25.i27.3590
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