Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis
Abstract Probiotics have been proposed as a potential strategy for managing ulcerative colitis (UC). However, the underlying mechanisms mediating microbiota-host crosstalk remain largely elusive. Here, we report that Limosilactobacillus reuteri (L. reuteri), as a probiotic, secretes cytoplasmic memb...
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| Language: | English |
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BMC
2025-01-01
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| Series: | Journal of Nanobiotechnology |
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| Online Access: | https://doi.org/10.1186/s12951-025-03158-8 |
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| author | Ningning Yue Hailan Zhao Peng Hu Yuan Zhang Chengmei Tian Chen Kong Zhiliang Mai Longbin Huang Qianjun Luo Daoru Wei Ruiyue Shi Shaohui Tang Yuqiang Nie Yujie Liang Jun Yao Lisheng Wang Defeng Li |
| author_facet | Ningning Yue Hailan Zhao Peng Hu Yuan Zhang Chengmei Tian Chen Kong Zhiliang Mai Longbin Huang Qianjun Luo Daoru Wei Ruiyue Shi Shaohui Tang Yuqiang Nie Yujie Liang Jun Yao Lisheng Wang Defeng Li |
| author_sort | Ningning Yue |
| collection | DOAJ |
| description | Abstract Probiotics have been proposed as a potential strategy for managing ulcerative colitis (UC). However, the underlying mechanisms mediating microbiota-host crosstalk remain largely elusive. Here, we report that Limosilactobacillus reuteri (L. reuteri), as a probiotic, secretes cytoplasmic membrane vesicles (CMVs) that communicate with host cells, alter host physiology, and alleviate dextran sulfate sodium (DSS)-induced colitis. First, L. reuteri-CMVs selectively promoted the proliferation of the beneficial bacterium Akkermansia muciniphila (AKK) by upregulating the expression of glycosidases (beta-N-acetylhexosaminidase and alpha-N-acetylglucosaminidase) involved in glycan degradation and metabolic pathways and restored the disrupted gut microbiota balance. Second, L. reuteri-CMVs were taken up by intestinal epithelial cells (IECs), elevated the expression of ZO-1, E-cadherin (Cdh1), and Occludin (Ocln), decreased intestinal permeability, and exerted protective effects on epithelial tight junction functionality. RNA sequencing analysis demonstrated that L. reuteri-CMVs repaired intestinal barrier by activating the HIF-1 signaling pathway and upregulating HMOX1 expression. Third, L. reuteri-CMVs increased the population of double positive (DP) CD4+CD8+ T cells in the intestinal epithelial layer, suppressing gut inflammation and maintaining gut mucosal homeostasis. Finally, L. reuteri-CMVs exhibited satisfactory stability and safety in the gastrointestinal tract and specifically targeted the desired sites in colitis mice. Collectively, these findings shed light on how L. reuteri interact with the host in colitis, and provide new insights into potential strategies for alleviating colitis. Graphical Abstract |
| format | Article |
| id | doaj-art-67e838f10b0e4c52b4eabdecdd57e9ce |
| institution | Kabale University |
| issn | 1477-3155 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Nanobiotechnology |
| spelling | doaj-art-67e838f10b0e4c52b4eabdecdd57e9ce2025-02-02T12:40:58ZengBMCJournal of Nanobiotechnology1477-31552025-01-0123112310.1186/s12951-025-03158-8Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitisNingning Yue0Hailan Zhao1Peng Hu2Yuan Zhang3Chengmei Tian4Chen Kong5Zhiliang Mai6Longbin Huang7Qianjun Luo8Daoru Wei9Ruiyue Shi10Shaohui Tang11Yuqiang Nie12Yujie Liang13Jun Yao14Lisheng Wang15Defeng Li16Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)School of Health Science and Engineering, University of Shanghai for Science and TechnologyDepartment of Medical Administration, Huizhou Institute of Occupational Diseases Control and PreventionDepartment of Emergency, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University; The First Affiliated Hospital, Southern University of Science and Technology)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Endocrine, Shenzhen Qianhai Shekou Free Trade Zone HospitalDepartment of Rehabilitation, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University; The First Affiliated Hospital, Southern University of Science and Technology)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Gastroenterology, The First Affiliated Hospital, Jinan UniversityDepartment of Gastroenterology and Hepatology, Guangzhou Digestive Disease Center, Guangzhou First People’s Hospital, School of Medicine, South China University of TechnologyDepartment of Child and Adolescent Psychiatry, Shenzhen Kangning Hospital, Shenzhen Mental Health CenterDepartment of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Department of Gastroenterology, Shenzhen People’s Hospital (The Second Clinical Medical College, Jinan University)Abstract Probiotics have been proposed as a potential strategy for managing ulcerative colitis (UC). However, the underlying mechanisms mediating microbiota-host crosstalk remain largely elusive. Here, we report that Limosilactobacillus reuteri (L. reuteri), as a probiotic, secretes cytoplasmic membrane vesicles (CMVs) that communicate with host cells, alter host physiology, and alleviate dextran sulfate sodium (DSS)-induced colitis. First, L. reuteri-CMVs selectively promoted the proliferation of the beneficial bacterium Akkermansia muciniphila (AKK) by upregulating the expression of glycosidases (beta-N-acetylhexosaminidase and alpha-N-acetylglucosaminidase) involved in glycan degradation and metabolic pathways and restored the disrupted gut microbiota balance. Second, L. reuteri-CMVs were taken up by intestinal epithelial cells (IECs), elevated the expression of ZO-1, E-cadherin (Cdh1), and Occludin (Ocln), decreased intestinal permeability, and exerted protective effects on epithelial tight junction functionality. RNA sequencing analysis demonstrated that L. reuteri-CMVs repaired intestinal barrier by activating the HIF-1 signaling pathway and upregulating HMOX1 expression. Third, L. reuteri-CMVs increased the population of double positive (DP) CD4+CD8+ T cells in the intestinal epithelial layer, suppressing gut inflammation and maintaining gut mucosal homeostasis. Finally, L. reuteri-CMVs exhibited satisfactory stability and safety in the gastrointestinal tract and specifically targeted the desired sites in colitis mice. Collectively, these findings shed light on how L. reuteri interact with the host in colitis, and provide new insights into potential strategies for alleviating colitis. Graphical Abstracthttps://doi.org/10.1186/s12951-025-03158-8Limosilactobacillus reuteriCytoplasmic membrane vesiclesGut microbiotaIntestinal barrierDouble positive CD4+CD8+ T cellsColitis |
| spellingShingle | Ningning Yue Hailan Zhao Peng Hu Yuan Zhang Chengmei Tian Chen Kong Zhiliang Mai Longbin Huang Qianjun Luo Daoru Wei Ruiyue Shi Shaohui Tang Yuqiang Nie Yujie Liang Jun Yao Lisheng Wang Defeng Li Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis Journal of Nanobiotechnology Limosilactobacillus reuteri Cytoplasmic membrane vesicles Gut microbiota Intestinal barrier Double positive CD4+CD8+ T cells Colitis |
| title | Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis |
| title_full | Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis |
| title_fullStr | Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis |
| title_full_unstemmed | Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis |
| title_short | Real-world of Limosilactobacillus reuteri in mitigation of acute experimental colitis |
| title_sort | real world of limosilactobacillus reuteri in mitigation of acute experimental colitis |
| topic | Limosilactobacillus reuteri Cytoplasmic membrane vesicles Gut microbiota Intestinal barrier Double positive CD4+CD8+ T cells Colitis |
| url | https://doi.org/10.1186/s12951-025-03158-8 |
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