<i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism

Nonalcoholic fatty liver disease (NAFLD) is the most prevalent chronic disease in modern society. It is characterized by an accumulation of lipids in the liver and an excessive inflammatory response. Clinical trials have provided evidence that probiotics may prevent the onset and relapse of NAFLD. T...

Full description

Bibliographic Details
Main Authors: Chang Sun, Chenguang Qiu, Yanyan Zhang, Man Yan, Jiajun Tan, Jiayuan He, Dakai Yang, Dongxu Wang, Liang Wu
Format: Article
Language:English
Published: MDPI AG 2023-05-01
Series:Molecules
Subjects:
Online Access:https://www.mdpi.com/1420-3049/28/10/4042
_version_ 1797598937810468864
author Chang Sun
Chenguang Qiu
Yanyan Zhang
Man Yan
Jiajun Tan
Jiayuan He
Dakai Yang
Dongxu Wang
Liang Wu
author_facet Chang Sun
Chenguang Qiu
Yanyan Zhang
Man Yan
Jiajun Tan
Jiayuan He
Dakai Yang
Dongxu Wang
Liang Wu
author_sort Chang Sun
collection DOAJ
description Nonalcoholic fatty liver disease (NAFLD) is the most prevalent chronic disease in modern society. It is characterized by an accumulation of lipids in the liver and an excessive inflammatory response. Clinical trials have provided evidence that probiotics may prevent the onset and relapse of NAFLD. The aim of this study was to explore the effect of <i>Lactiplantibacillus plantarum</i> NKK20 strain (NKK20) on high-fat-diet-induced NAFLD in an ICR murine model and propose the underlying mechanism whereby NKK20 protects against NAFLD. The results showed that the administration of NKK20 ameliorated hepatocyte fatty degeneration, reduced total cholesterol and triglyceride concentrations, and alleviated inflammatory reactions in NAFLD mice. In addition, the 16S rRNA sequencing results indicated that NKK20 could decrease the abundance of <i>Pseudomonas</i> and <i>Turicibacter</i> and increase the abundance of <i>Akkermansia</i> in NAFLD mice. LC-MS/MS analysis showed that NKK20 could significantly increase the concentration of short-chain fatty acids (SCFAs) in the colon contents of mice. The obtained non-targeted metabolomics results revealed a significant difference between the metabolites in the colon contents of the NKK20 administration group and those in the high-fat diet group, in which a total of 11 different metabolites that were significantly affected by NKK20 were observed, and these metabolites were mainly involved in bile acid anabolism. UPLC-MS technical analysis revealed that NKK20 could change the concentrations of six conjugated and free bile acids in mouse liver. After being treated with NKK20, the concentrations of cholic acid, glycinocholic acid, and glycinodeoxycholic acid in livers of the NAFLD mice were significantly decreased, while the concentration of aminodeoxycholic acid was significantly increased. Thus, our findings indicate that NKK20 can regulate bile acid anabolism and promote the production of SCFA, which can inhibit inflammation and liver damage and thus prevent the development of NAFLD.
first_indexed 2024-03-11T03:27:40Z
format Article
id doaj.art-b62a6f572dcb4d5d99e27c4dc07b5b0a
institution Directory Open Access Journal
issn 1420-3049
language English
last_indexed 2024-03-11T03:27:40Z
publishDate 2023-05-01
publisher MDPI AG
record_format Article
series Molecules
spelling doaj.art-b62a6f572dcb4d5d99e27c4dc07b5b0a2023-11-18T02:38:26ZengMDPI AGMolecules1420-30492023-05-012810404210.3390/molecules28104042<i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid AnabolismChang Sun0Chenguang Qiu1Yanyan Zhang2Man Yan3Jiajun Tan4Jiayuan He5Dakai Yang6Dongxu Wang7Liang Wu8Department of Laboratory Medicine, School of Medicine, Jiangsu University, Zhenjiang 212013, ChinaDepartment of Stomatology, Zhenjiang First People’s Hospital, Zhenjiang 212002, ChinaDepartment of Testing Center, Yangzhou University, Yangzhou 225001, ChinaDepartment of Laboratory Medicine, School of Medicine, Jiangsu University, Zhenjiang 212013, ChinaDepartment of Laboratory Medicine, School of Medicine, Jiangsu University, Zhenjiang 212013, ChinaZhenjiang Center for Disease Control and Prevention, Zhenjiang 212002, ChinaDepartment of Laboratory Medicine, School of Medicine, Jiangsu University, Zhenjiang 212013, ChinaSchool of Grain Science and Technology, Jiangsu University of Science and Technology, Zhenjiang 212100, ChinaDepartment of Laboratory Medicine, School of Medicine, Jiangsu University, Zhenjiang 212013, ChinaNonalcoholic fatty liver disease (NAFLD) is the most prevalent chronic disease in modern society. It is characterized by an accumulation of lipids in the liver and an excessive inflammatory response. Clinical trials have provided evidence that probiotics may prevent the onset and relapse of NAFLD. The aim of this study was to explore the effect of <i>Lactiplantibacillus plantarum</i> NKK20 strain (NKK20) on high-fat-diet-induced NAFLD in an ICR murine model and propose the underlying mechanism whereby NKK20 protects against NAFLD. The results showed that the administration of NKK20 ameliorated hepatocyte fatty degeneration, reduced total cholesterol and triglyceride concentrations, and alleviated inflammatory reactions in NAFLD mice. In addition, the 16S rRNA sequencing results indicated that NKK20 could decrease the abundance of <i>Pseudomonas</i> and <i>Turicibacter</i> and increase the abundance of <i>Akkermansia</i> in NAFLD mice. LC-MS/MS analysis showed that NKK20 could significantly increase the concentration of short-chain fatty acids (SCFAs) in the colon contents of mice. The obtained non-targeted metabolomics results revealed a significant difference between the metabolites in the colon contents of the NKK20 administration group and those in the high-fat diet group, in which a total of 11 different metabolites that were significantly affected by NKK20 were observed, and these metabolites were mainly involved in bile acid anabolism. UPLC-MS technical analysis revealed that NKK20 could change the concentrations of six conjugated and free bile acids in mouse liver. After being treated with NKK20, the concentrations of cholic acid, glycinocholic acid, and glycinodeoxycholic acid in livers of the NAFLD mice were significantly decreased, while the concentration of aminodeoxycholic acid was significantly increased. Thus, our findings indicate that NKK20 can regulate bile acid anabolism and promote the production of SCFA, which can inhibit inflammation and liver damage and thus prevent the development of NAFLD.https://www.mdpi.com/1420-3049/28/10/4042<i>Lactiplantibacillus plantarum</i>NAFLDbile acid anabolisminflammationprobioticsmetabolomics
spellingShingle Chang Sun
Chenguang Qiu
Yanyan Zhang
Man Yan
Jiajun Tan
Jiayuan He
Dakai Yang
Dongxu Wang
Liang Wu
<i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism
Molecules
<i>Lactiplantibacillus plantarum</i>
NAFLD
bile acid anabolism
inflammation
probiotics
metabolomics
title <i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism
title_full <i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism
title_fullStr <i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism
title_full_unstemmed <i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism
title_short <i>Lactiplantibacillus plantarum</i> NKK20 Alleviates High-Fat-Diet-Induced Nonalcoholic Fatty Liver Disease in Mice through Regulating Bile Acid Anabolism
title_sort i lactiplantibacillus plantarum i nkk20 alleviates high fat diet induced nonalcoholic fatty liver disease in mice through regulating bile acid anabolism
topic <i>Lactiplantibacillus plantarum</i>
NAFLD
bile acid anabolism
inflammation
probiotics
metabolomics
url https://www.mdpi.com/1420-3049/28/10/4042
work_keys_str_mv AT changsun ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT chenguangqiu ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT yanyanzhang ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT manyan ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT jiajuntan ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT jiayuanhe ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT dakaiyang ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT dongxuwang ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism
AT liangwu ilactiplantibacillusplantaruminkk20alleviateshighfatdietinducednonalcoholicfattyliverdiseaseinmicethroughregulatingbileacidanabolism