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

Yimei Wang; Tomohiro Takano; Yingyu Zhou; Rong Wang; Takayuki Toshimitsu; Toshihiro Sashihara; Masaru Tanokura; Takuya Miyakawa; Haruyo Nakajima-Adachi; Satoshi Hachimura

doi:10.3389/fimmu.2023.1123052

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

Front Immunol. 2023 Feb 23:14:1123052. doi: 10.3389/fimmu.2023.1123052. eCollection 2023.

Authors

Affiliations

¹ Research Center for Food Safety, The University of Tokyo, Tokyo, Japan.
² Department of Applied Biological Chemistry, The University of Tokyo, Tokyo, Japan.
³ Co-Creation Center, Meiji Holdings Co., Ltd, Hachiouji, Japan.
⁴ Graduate School of Biostudies, Kyoto University, Kyoto, Japan.

Abstract

Introduction: Chronic 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.

Methods: We 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.

Results: After 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.

Discussion: Our 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.

Keywords: gut microbiota; intestinal permeability; lactic acid bacteria; macrophages; obesity; proinflammatory cytokines.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Anti-Inflammatory Agents / pharmacology
Gastrointestinal Microbiome*
Ileum
Inflammation
Lactobacillales*
Mice
Obesity / microbiology

Substances

Anti-Inflammatory Agents

Grants and funding

This research was partly supported by Grant-in-Aid for Scientific Research (B) (Grant numbers 18H02152 and 22H02283) from the Japan Society for the Promotion of Science (JSPS) and a grant from the Food Science Institute Foundation (Ryoushoku-kenkyukai).