Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity

BackgroundBariatric surgery is associated with a positive effect on the progress of non-alcoholic associated fatty liver disease (NAFLD). Although weight loss is the obvious mechanism, there are also weight-independent mechanisms.MethodsWe collected blood samples from 5 patients with obesity before...

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Main Authors: Geng Wang, Yu Wang, Jie Bai, Gang Li, Yang Liu, Shichang Deng, Rui Zhou, Kaixiong Tao, Zefeng Xia
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Endocrinology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2022.1024769/full
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author Geng Wang
Yu Wang
Yu Wang
Jie Bai
Gang Li
Yang Liu
Shichang Deng
Rui Zhou
Kaixiong Tao
Zefeng Xia
author_facet Geng Wang
Yu Wang
Yu Wang
Jie Bai
Gang Li
Yang Liu
Shichang Deng
Rui Zhou
Kaixiong Tao
Zefeng Xia
author_sort Geng Wang
collection DOAJ
description BackgroundBariatric surgery is associated with a positive effect on the progress of non-alcoholic associated fatty liver disease (NAFLD). Although weight loss is the obvious mechanism, there are also weight-independent mechanisms.MethodsWe collected blood samples from 5 patients with obesity before and 3 months after surgery and performed an LC-MS-based untargeted metabolomics test to detect potential systemic changes. We also constructed sleeve gastrectomy (SG) mice models. The plasma, liver and intestine samples were collected and analyzed by qPCR, ELISA and HPLC. Cohousing experiments and feces transplantation experiments were performed on mice to study the effect of gut microbiota. Genistein administration experiments were used to study the in vivo function of the metabolites.ResultsPlasma genistein (GE) was identified to be elevated after surgery. Both clinical data and rodent models suggested that plasma GE is negatively related to the degree of NAFLD. We fed diet-induced obese (DIO) mice with GE, and we found that there was significant remission of NAFLD. Both in vivo and in vitro experiments showed that GE could restrict the inflammation state in the liver and thus relieve NAFLD. Finally, we used co-housing experiments to alter the gut microbiota in mice, and it was identified that sleeve gastrectomy (SG) mice had a special gut microbiota phenotype, which could result in higher plasma GE levels. By feces transplantation experiment (FMT), we found that only feces from the SG mice (and not from other lean mice) could induce higher plasma GE levels.ConclusionOur studies showed that SG but not calorie restriction could induce higher plasma GE levels by altering the gut microbiota. This change could promote NAFLD remission. Our study provides new insights into the systemic effects of bariatric surgery. Bariatric surgery could affect remote organs via altered metabolites from the gut microbiota. Our study also identified that additional supplement of GE after surgery could be a therapy for NAFLD.
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spelling doaj.art-37bdae1e6ede40109ebcca1a147ef0732023-01-04T14:49:26ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922023-01-011310.3389/fendo.2022.10247691024769Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesityGeng Wang0Yu Wang1Yu Wang2Jie Bai3Gang Li4Yang Liu5Shichang Deng6Rui Zhou7Kaixiong Tao8Zefeng Xia9Department of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaCancer Center, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaDepartment of Gastrointestinal Surgery, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, ChinaBackgroundBariatric surgery is associated with a positive effect on the progress of non-alcoholic associated fatty liver disease (NAFLD). Although weight loss is the obvious mechanism, there are also weight-independent mechanisms.MethodsWe collected blood samples from 5 patients with obesity before and 3 months after surgery and performed an LC-MS-based untargeted metabolomics test to detect potential systemic changes. We also constructed sleeve gastrectomy (SG) mice models. The plasma, liver and intestine samples were collected and analyzed by qPCR, ELISA and HPLC. Cohousing experiments and feces transplantation experiments were performed on mice to study the effect of gut microbiota. Genistein administration experiments were used to study the in vivo function of the metabolites.ResultsPlasma genistein (GE) was identified to be elevated after surgery. Both clinical data and rodent models suggested that plasma GE is negatively related to the degree of NAFLD. We fed diet-induced obese (DIO) mice with GE, and we found that there was significant remission of NAFLD. Both in vivo and in vitro experiments showed that GE could restrict the inflammation state in the liver and thus relieve NAFLD. Finally, we used co-housing experiments to alter the gut microbiota in mice, and it was identified that sleeve gastrectomy (SG) mice had a special gut microbiota phenotype, which could result in higher plasma GE levels. By feces transplantation experiment (FMT), we found that only feces from the SG mice (and not from other lean mice) could induce higher plasma GE levels.ConclusionOur studies showed that SG but not calorie restriction could induce higher plasma GE levels by altering the gut microbiota. This change could promote NAFLD remission. Our study provides new insights into the systemic effects of bariatric surgery. Bariatric surgery could affect remote organs via altered metabolites from the gut microbiota. Our study also identified that additional supplement of GE after surgery could be a therapy for NAFLD.https://www.frontiersin.org/articles/10.3389/fendo.2022.1024769/fullbariatric surgerygenisteingut microbiotanon-alcoholic fatty liver diseaseobesesleeve gastrectomy
spellingShingle Geng Wang
Yu Wang
Yu Wang
Jie Bai
Gang Li
Yang Liu
Shichang Deng
Rui Zhou
Kaixiong Tao
Zefeng Xia
Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity
Frontiers in Endocrinology
bariatric surgery
genistein
gut microbiota
non-alcoholic fatty liver disease
obese
sleeve gastrectomy
title Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity
title_full Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity
title_fullStr Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity
title_full_unstemmed Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity
title_short Increased plasma genistein after bariatric surgery could promote remission of NAFLD in patients with obesity
title_sort increased plasma genistein after bariatric surgery could promote remission of nafld in patients with obesity
topic bariatric surgery
genistein
gut microbiota
non-alcoholic fatty liver disease
obese
sleeve gastrectomy
url https://www.frontiersin.org/articles/10.3389/fendo.2022.1024769/full
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