Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice

IntroductionOral exposure to microplastics (MPs) is a global health concern. In our previous study, MPs induced glucose intolerance and non-alcoholic fatty liver disease (NAFLD) under a high-fat diet-induced leaky gut syndrome (LGS). This study aims to evaluate the effects of high concentrations of...

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Main Authors: Yuka Hasegawa, Takuro Okamura, Yuriko Ono, Takahiro Ichikawa, Yuto Saijo, Naoko Nakanishi, Ryoichi Sasano, Masahide Hamaguchi, Hirohisa Takano, Michiaki Fukui
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1407936/full
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author Yuka Hasegawa
Takuro Okamura
Yuriko Ono
Takahiro Ichikawa
Yuto Saijo
Naoko Nakanishi
Ryoichi Sasano
Masahide Hamaguchi
Hirohisa Takano
Hirohisa Takano
Michiaki Fukui
author_facet Yuka Hasegawa
Takuro Okamura
Yuriko Ono
Takahiro Ichikawa
Yuto Saijo
Naoko Nakanishi
Ryoichi Sasano
Masahide Hamaguchi
Hirohisa Takano
Hirohisa Takano
Michiaki Fukui
author_sort Yuka Hasegawa
collection DOAJ
description IntroductionOral exposure to microplastics (MPs) is a global health concern. In our previous study, MPs induced glucose intolerance and non-alcoholic fatty liver disease (NAFLD) under a high-fat diet-induced leaky gut syndrome (LGS). This study aims to evaluate the effects of high concentrations of MP on lipid metabolism under normal dietary conditions and to assess the changes in the intestinal tract resulting from MP exposure.MethodsC57BL6/J mice were fed a normal diet (ND) without polystyrene MPs (PS-MPs) or with PS-MPs (1000 µg/L or 5000 µg/L) for six weeks. Subsequently, intestinal permeability, gut microbiota, and metabolite levels in the serum, feces, and liver were determined.ResultsMice fed the ND showed no increase in intestinal permeability in either group. However, high MPs concentrations led to increased serum lipid levels and exacerbated fatty liver function. Oral exposure to MPs did not affect the number of innate lymphoid cells or short-chain fatty acids in the intestine. However, it increased the number of natural killer cells, altered the gut microbiota, induced inflammation, and modulated the expression of genes related to nutrient transport in the intestine. The severity of intestinal disturbance tended to worsen with dose.DiscussionDespite the absence of LGS, high concentrations of MPs induced dyslipidemia and NAFLD. Oral exposure to MPs triggered intestinal inflammation via natural killer cells, altered the gut microbiota, and modulated nutrient metabolism. Our study highlights the need for environmental measures to reduce oral MPs exposure in the future.
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publishDate 2024-11-01
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spelling doaj-art-df5f30b9176341c489a2598df3abe01e2024-11-12T06:15:38ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-11-011510.3389/fimmu.2024.14079361407936Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in miceYuka Hasegawa0Takuro Okamura1Yuriko Ono2Takahiro Ichikawa3Yuto Saijo4Naoko Nakanishi5Ryoichi Sasano6Masahide Hamaguchi7Hirohisa Takano8Hirohisa Takano9Michiaki Fukui10Department of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanAiSTI Science Co., Ltd., Wakayama, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanGraduate School of Global Environmental Studies, Kyoto University, Kyoto, JapanInstitute for International Academic Research, Kyoto University of Advanced Science, Kyoto, JapanDepartment of Endocrinology and Metabolism, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, JapanIntroductionOral exposure to microplastics (MPs) is a global health concern. In our previous study, MPs induced glucose intolerance and non-alcoholic fatty liver disease (NAFLD) under a high-fat diet-induced leaky gut syndrome (LGS). This study aims to evaluate the effects of high concentrations of MP on lipid metabolism under normal dietary conditions and to assess the changes in the intestinal tract resulting from MP exposure.MethodsC57BL6/J mice were fed a normal diet (ND) without polystyrene MPs (PS-MPs) or with PS-MPs (1000 µg/L or 5000 µg/L) for six weeks. Subsequently, intestinal permeability, gut microbiota, and metabolite levels in the serum, feces, and liver were determined.ResultsMice fed the ND showed no increase in intestinal permeability in either group. However, high MPs concentrations led to increased serum lipid levels and exacerbated fatty liver function. Oral exposure to MPs did not affect the number of innate lymphoid cells or short-chain fatty acids in the intestine. However, it increased the number of natural killer cells, altered the gut microbiota, induced inflammation, and modulated the expression of genes related to nutrient transport in the intestine. The severity of intestinal disturbance tended to worsen with dose.DiscussionDespite the absence of LGS, high concentrations of MPs induced dyslipidemia and NAFLD. Oral exposure to MPs triggered intestinal inflammation via natural killer cells, altered the gut microbiota, and modulated nutrient metabolism. Our study highlights the need for environmental measures to reduce oral MPs exposure in the future.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1407936/fulltoxicologyenvironmental sciencemicroplasticsinflammationdysbiosis
spellingShingle Yuka Hasegawa
Takuro Okamura
Yuriko Ono
Takahiro Ichikawa
Yuto Saijo
Naoko Nakanishi
Ryoichi Sasano
Masahide Hamaguchi
Hirohisa Takano
Hirohisa Takano
Michiaki Fukui
Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
Frontiers in Immunology
toxicology
environmental science
microplastics
inflammation
dysbiosis
title Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
title_full Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
title_fullStr Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
title_full_unstemmed Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
title_short Oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
title_sort oral exposure to high concentrations of polystyrene microplastics alters the intestinal environment and metabolic outcomes in mice
topic toxicology
environmental science
microplastics
inflammation
dysbiosis
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1407936/full
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