Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota
IntroductionChronic inflammation caused by dietary obesity has been considered to induce lifestyle-related diseases and functional ingredients with anti-inflammatory effects are attracting attention. Although multiple studies on obesity had proved the anti-inflammatory effects of ingestion of lactic...
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1123052/full |
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| author | Yimei Wang Tomohiro Takano Yingyu Zhou Rong Wang Takayuki Toshimitsu Toshihiro Sashihara Masaru Tanokura Masaru Tanokura Takuya Miyakawa Takuya Miyakawa Haruyo Nakajima-Adachi Satoshi Hachimura |
| author_facet | Yimei Wang Tomohiro Takano Yingyu Zhou Rong Wang Takayuki Toshimitsu Toshihiro Sashihara Masaru Tanokura Masaru Tanokura Takuya Miyakawa Takuya Miyakawa Haruyo Nakajima-Adachi Satoshi Hachimura |
| author_sort | Yimei Wang |
| collection | DOAJ |
| description | IntroductionChronic inflammation caused by dietary obesity has been considered to induce lifestyle-related diseases and functional ingredients with anti-inflammatory effects are attracting attention. Although multiple studies on obesity had proved the anti-inflammatory effects of ingestion of lactic acid bacteria (LAB) and other functional ingredients on adipose tissue, the precise effects on the intestine, especially on the individual intestinal segments have not been made clear. In this study, we elucidated the mechanisms of Lactiplantibacillus plantarum (basonym: Lactobacillus plantarum) OLL2712 in suppressing obesity-induced inflammation using high fat diet (HFD)-fed mice obesity model.MethodsWe orally administered heat-treated LAB to HFD-fed mice model, and investigated the inflammatory changes in adipose tissue and intestinal immune cells. We also analyzed gut microbiota, and evaluated the inflammation and permeability of the duodenum, jejunum, ileum and colon; four intestinal segments differing in gut bacteria composition and immune response.ResultsAfter 3-week LAB administration, the gene expression levels of proinflammatory cytokines were downregulated in adipose tissue, colon, and Peyer’s patches (PP)-derived F4/80+ cells. The LAB treatment alleviated obesity-related gut microbiota imbalance. L. plantarum OLL2712 treatment helps maintain intestinal barrier function, especially in the ileum, possibly by preventing ZO-1 and Occludin downregulation.DiscussionOur results suggest that the oral administration of the LAB strain regulated the gut microbiota, suppressed intestinal inflammation, and improved the gut barrier, which could inhibit the products of obesity-induced gut dysbiosis from translocating into the bloodstream and the adipose tissue, through which the LAB finally alleviated the inflammation caused by dietary obesity. Barrier improvement was observed, especially in the ileum, suggesting collaborative modulation of the intestinal immune responses by ingested LAB and microbiota. |
| first_indexed | 2024-04-10T07:55:20Z |
| format | Article |
| id | doaj.art-65684b9e306f4dd6b1a30cdd5d086023 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-10T07:55:20Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj.art-65684b9e306f4dd6b1a30cdd5d0860232023-02-23T04:50:10ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-02-011410.3389/fimmu.2023.11230521123052Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiotaYimei Wang0Tomohiro Takano1Yingyu Zhou2Rong Wang3Takayuki Toshimitsu4Toshihiro Sashihara5Masaru Tanokura6Masaru Tanokura7Takuya Miyakawa8Takuya Miyakawa9Haruyo Nakajima-Adachi10Satoshi Hachimura11Research Center for Food Safety, The University of Tokyo, Tokyo, JapanResearch Center for Food Safety, The University of Tokyo, Tokyo, JapanDepartment of Applied Biological Chemistry, The University of Tokyo, Tokyo, JapanDepartment of Applied Biological Chemistry, The University of Tokyo, Tokyo, JapanCo-Creation Center, Meiji Holdings Co., Ltd, Hachiouji, JapanCo-Creation Center, Meiji Holdings Co., Ltd, Hachiouji, JapanResearch Center for Food Safety, The University of Tokyo, Tokyo, JapanDepartment of Applied Biological Chemistry, The University of Tokyo, Tokyo, JapanDepartment of Applied Biological Chemistry, The University of Tokyo, Tokyo, JapanGraduate School of Biostudies, Kyoto University, Kyoto, JapanResearch Center for Food Safety, The University of Tokyo, Tokyo, JapanResearch Center for Food Safety, The University of Tokyo, Tokyo, JapanIntroductionChronic inflammation caused by dietary obesity has been considered to induce lifestyle-related diseases and functional ingredients with anti-inflammatory effects are attracting attention. Although multiple studies on obesity had proved the anti-inflammatory effects of ingestion of lactic acid bacteria (LAB) and other functional ingredients on adipose tissue, the precise effects on the intestine, especially on the individual intestinal segments have not been made clear. In this study, we elucidated the mechanisms of Lactiplantibacillus plantarum (basonym: Lactobacillus plantarum) OLL2712 in suppressing obesity-induced inflammation using high fat diet (HFD)-fed mice obesity model.MethodsWe orally administered heat-treated LAB to HFD-fed mice model, and investigated the inflammatory changes in adipose tissue and intestinal immune cells. We also analyzed gut microbiota, and evaluated the inflammation and permeability of the duodenum, jejunum, ileum and colon; four intestinal segments differing in gut bacteria composition and immune response.ResultsAfter 3-week LAB administration, the gene expression levels of proinflammatory cytokines were downregulated in adipose tissue, colon, and Peyer’s patches (PP)-derived F4/80+ cells. The LAB treatment alleviated obesity-related gut microbiota imbalance. L. plantarum OLL2712 treatment helps maintain intestinal barrier function, especially in the ileum, possibly by preventing ZO-1 and Occludin downregulation.DiscussionOur results suggest that the oral administration of the LAB strain regulated the gut microbiota, suppressed intestinal inflammation, and improved the gut barrier, which could inhibit the products of obesity-induced gut dysbiosis from translocating into the bloodstream and the adipose tissue, through which the LAB finally alleviated the inflammation caused by dietary obesity. Barrier improvement was observed, especially in the ileum, suggesting collaborative modulation of the intestinal immune responses by ingested LAB and microbiota.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1123052/fullobesityproinflammatory cytokinesmacrophagesgut microbiotaintestinal permeabilitylactic acid bacteria |
| spellingShingle | Yimei Wang Tomohiro Takano Yingyu Zhou Rong Wang Takayuki Toshimitsu Toshihiro Sashihara Masaru Tanokura Masaru Tanokura Takuya Miyakawa Takuya Miyakawa Haruyo Nakajima-Adachi Satoshi Hachimura Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota Frontiers in Immunology obesity proinflammatory cytokines macrophages gut microbiota intestinal permeability lactic acid bacteria |
| title | Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota |
| title_full | Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota |
| title_fullStr | Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota |
| title_full_unstemmed | Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota |
| title_short | Orally administered Lactiplantibacillus plantarum OLL2712 decreased intestinal permeability, especially in the ileum: Ingested lactic acid bacteria alleviated obesity-induced inflammation by collaborating with gut microbiota |
| title_sort | orally administered lactiplantibacillus plantarum oll2712 decreased intestinal permeability especially in the ileum ingested lactic acid bacteria alleviated obesity induced inflammation by collaborating with gut microbiota |
| topic | obesity proinflammatory cytokines macrophages gut microbiota intestinal permeability lactic acid bacteria |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1123052/full |
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