Lactiplantibacillus plantarum Regulates Intestinal Physiology and Enteric Neurons in IBS through Microbial Tryptophan Metabolites
Irritable bowel syndrome (IBS) is a prevalent functional gastrointestinal disorder characterized by visceral pain and gut dysmotility. However, the specific mechanisms by which Lactobacillus strains relieve IBS remain unclear. Here, we screened Lactobacillus strains from traditional Chinese fermente...
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| Veröffentlicht in: | Journal of agricultural and food chemistry 2024-08, Vol.72 (32), p.17989-18002 |
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| creator | Xia, Bing Lin, Tongkui Li, Zhiqing Wang, Jialin Sun, Yuwei Wang, Danna Ye, Jin Zhang, Yajuan Kou, Rongwei Zhao, Beita Yi, Junjie Bai, Gaiyan Liu, Xuebo |
| description | Irritable bowel syndrome (IBS) is a prevalent functional gastrointestinal disorder characterized by visceral pain and gut dysmotility. However, the specific mechanisms by which Lactobacillus strains relieve IBS remain unclear. Here, we screened Lactobacillus strains from traditional Chinese fermented foods with potential IBS-alleviating properties through in vitro and in vivo experiments. We demonstrated that Lactiplantibacillus plantarum D266 (Lp D266) administration effectively modulates intestinal peristalsis, enteric neurons, visceral hypersensitivity, colonic inflammation, gut barrier function, and mast cell activation. Additionally, Lp D266 shapes gut microbiota and enhances tryptophan (Trp) metabolism, thus activating the aryl hydrocarbon receptor (AhR) and subsequently enhancing IL-22 production to maintain gut homeostasis. Mechanistically, Lp D266 potentially modulates colonic physiology and enteric neurons by microbial tryptophan metabolites. Further, our study indicates that combining Lp D266 with Trp synergistically ameliorates IBS symptoms. Together, our experiments identify the therapeutic efficacy of tryptophan-catabolizing Lp D266 in regulating gut physiology and enteric neurons, providing new insights into the development of probiotic-mediated nutritional intervention for IBS management. |
| doi_str_mv | 10.1021/acs.jafc.4c03087 |
| format | Article |
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However, the specific mechanisms by which Lactobacillus strains relieve IBS remain unclear. Here, we screened Lactobacillus strains from traditional Chinese fermented foods with potential IBS-alleviating properties through in vitro and in vivo experiments. We demonstrated that Lactiplantibacillus plantarum D266 (Lp D266) administration effectively modulates intestinal peristalsis, enteric neurons, visceral hypersensitivity, colonic inflammation, gut barrier function, and mast cell activation. Additionally, Lp D266 shapes gut microbiota and enhances tryptophan (Trp) metabolism, thus activating the aryl hydrocarbon receptor (AhR) and subsequently enhancing IL-22 production to maintain gut homeostasis. Mechanistically, Lp D266 potentially modulates colonic physiology and enteric neurons by microbial tryptophan metabolites. Further, our study indicates that combining Lp D266 with Trp synergistically ameliorates IBS symptoms. Together, our experiments identify the therapeutic efficacy of tryptophan-catabolizing Lp D266 in regulating gut physiology and enteric neurons, providing new insights into the development of probiotic-mediated nutritional intervention for IBS management.</description><identifier>ISSN: 0021-8561</identifier><identifier>ISSN: 1520-5118</identifier><identifier>EISSN: 1520-5118</identifier><identifier>DOI: 10.1021/acs.jafc.4c03087</identifier><identifier>PMID: 39082086</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>absorption barrier ; aryl hydrocarbon receptors ; Bioactive Constituents, Metabolites, and Functions ; fermentation ; food chemistry ; homeostasis ; hypersensitivity ; inflammation ; intestinal microorganisms ; intestines ; irritable bowel syndrome ; Lactobacillus ; mast cells ; metabolites ; nutritional intervention ; pain ; peristalsis ; tryptophan</subject><ispartof>Journal of agricultural and food chemistry, 2024-08, Vol.72 (32), p.17989-18002</ispartof><rights>2024 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a252t-836419d7f410f5824d9146d2aa89fceef1a71d7720797751bbd9c4823e0778583</cites><orcidid>0000-0002-7916-5881 ; 0000-0002-1774-9902 ; 0000-0001-6370-2868</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acs.jafc.4c03087$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acs.jafc.4c03087$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39082086$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xia, Bing</creatorcontrib><creatorcontrib>Lin, Tongkui</creatorcontrib><creatorcontrib>Li, Zhiqing</creatorcontrib><creatorcontrib>Wang, Jialin</creatorcontrib><creatorcontrib>Sun, Yuwei</creatorcontrib><creatorcontrib>Wang, Danna</creatorcontrib><creatorcontrib>Ye, Jin</creatorcontrib><creatorcontrib>Zhang, Yajuan</creatorcontrib><creatorcontrib>Kou, Rongwei</creatorcontrib><creatorcontrib>Zhao, Beita</creatorcontrib><creatorcontrib>Yi, Junjie</creatorcontrib><creatorcontrib>Bai, Gaiyan</creatorcontrib><creatorcontrib>Liu, Xuebo</creatorcontrib><title>Lactiplantibacillus plantarum Regulates Intestinal Physiology and Enteric Neurons in IBS through Microbial Tryptophan Metabolites</title><title>Journal of agricultural and food chemistry</title><addtitle>J. Agric. Food Chem</addtitle><description>Irritable bowel syndrome (IBS) is a prevalent functional gastrointestinal disorder characterized by visceral pain and gut dysmotility. However, the specific mechanisms by which Lactobacillus strains relieve IBS remain unclear. Here, we screened Lactobacillus strains from traditional Chinese fermented foods with potential IBS-alleviating properties through in vitro and in vivo experiments. We demonstrated that Lactiplantibacillus plantarum D266 (Lp D266) administration effectively modulates intestinal peristalsis, enteric neurons, visceral hypersensitivity, colonic inflammation, gut barrier function, and mast cell activation. Additionally, Lp D266 shapes gut microbiota and enhances tryptophan (Trp) metabolism, thus activating the aryl hydrocarbon receptor (AhR) and subsequently enhancing IL-22 production to maintain gut homeostasis. Mechanistically, Lp D266 potentially modulates colonic physiology and enteric neurons by microbial tryptophan metabolites. Further, our study indicates that combining Lp D266 with Trp synergistically ameliorates IBS symptoms. Together, our experiments identify the therapeutic efficacy of tryptophan-catabolizing Lp D266 in regulating gut physiology and enteric neurons, providing new insights into the development of probiotic-mediated nutritional intervention for IBS management.</description><subject>absorption barrier</subject><subject>aryl hydrocarbon receptors</subject><subject>Bioactive Constituents, Metabolites, and Functions</subject><subject>fermentation</subject><subject>food chemistry</subject><subject>homeostasis</subject><subject>hypersensitivity</subject><subject>inflammation</subject><subject>intestinal microorganisms</subject><subject>intestines</subject><subject>irritable bowel syndrome</subject><subject>Lactobacillus</subject><subject>mast cells</subject><subject>metabolites</subject><subject>nutritional intervention</subject><subject>pain</subject><subject>peristalsis</subject><subject>tryptophan</subject><issn>0021-8561</issn><issn>1520-5118</issn><issn>1520-5118</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkUFvEzEQhS0EoqFw54R85MCGsb2OvUeoSomUtgjKeTXr9SaunPVirw858s_rNoEb4jLWyN970ptHyFsGSwacfUSTlvc4mGVtQIBWz8iCSQ6VZEw_JwsoTKXlip2RVyndA4CWCl6SM9GA5qBXC_J7g2Z2k8dxdh0a531O9GnFmPf0u91mj7NNdD2WObsRPf22OyQXfNgeKI49vSw_0Rl6Y3MMY6JupOvPP-i8iyFvd_TamRg6V3R38TDNYdrhSK_tjF3wrni-Ji8G9Mm-Ob3n5OeXy7uLr9Xm9mp98WlTIZd8rrRY1azp1VAzGKTmdd-wetVzRN0MxtqBoWK9UhxUo5RkXdc3ptZcWFBKSy3Oyfuj7xTDr1yytHuXjPUlqw05tYJJoUA2IP6PltMJzTnUBYUjWkKmFO3QTtHtMR5aBu1jR23pqH3sqD11VCTvTu6529v-r-BPKQX4cASepCHHcvT0b78HXAWe0A</recordid><startdate>20240814</startdate><enddate>20240814</enddate><creator>Xia, Bing</creator><creator>Lin, Tongkui</creator><creator>Li, Zhiqing</creator><creator>Wang, Jialin</creator><creator>Sun, Yuwei</creator><creator>Wang, Danna</creator><creator>Ye, Jin</creator><creator>Zhang, Yajuan</creator><creator>Kou, Rongwei</creator><creator>Zhao, Beita</creator><creator>Yi, Junjie</creator><creator>Bai, Gaiyan</creator><creator>Liu, Xuebo</creator><general>American Chemical Society</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-7916-5881</orcidid><orcidid>https://orcid.org/0000-0002-1774-9902</orcidid><orcidid>https://orcid.org/0000-0001-6370-2868</orcidid></search><sort><creationdate>20240814</creationdate><title>Lactiplantibacillus plantarum Regulates Intestinal Physiology and Enteric Neurons in IBS through Microbial Tryptophan Metabolites</title><author>Xia, Bing ; Lin, Tongkui ; Li, Zhiqing ; Wang, Jialin ; Sun, Yuwei ; Wang, Danna ; Ye, Jin ; Zhang, Yajuan ; Kou, Rongwei ; Zhao, Beita ; Yi, Junjie ; Bai, Gaiyan ; Liu, Xuebo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a252t-836419d7f410f5824d9146d2aa89fceef1a71d7720797751bbd9c4823e0778583</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>absorption barrier</topic><topic>aryl hydrocarbon receptors</topic><topic>Bioactive Constituents, Metabolites, and Functions</topic><topic>fermentation</topic><topic>food chemistry</topic><topic>homeostasis</topic><topic>hypersensitivity</topic><topic>inflammation</topic><topic>intestinal microorganisms</topic><topic>intestines</topic><topic>irritable bowel syndrome</topic><topic>Lactobacillus</topic><topic>mast cells</topic><topic>metabolites</topic><topic>nutritional intervention</topic><topic>pain</topic><topic>peristalsis</topic><topic>tryptophan</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xia, Bing</creatorcontrib><creatorcontrib>Lin, Tongkui</creatorcontrib><creatorcontrib>Li, Zhiqing</creatorcontrib><creatorcontrib>Wang, Jialin</creatorcontrib><creatorcontrib>Sun, Yuwei</creatorcontrib><creatorcontrib>Wang, Danna</creatorcontrib><creatorcontrib>Ye, Jin</creatorcontrib><creatorcontrib>Zhang, Yajuan</creatorcontrib><creatorcontrib>Kou, Rongwei</creatorcontrib><creatorcontrib>Zhao, Beita</creatorcontrib><creatorcontrib>Yi, Junjie</creatorcontrib><creatorcontrib>Bai, Gaiyan</creatorcontrib><creatorcontrib>Liu, Xuebo</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Journal of agricultural and food chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xia, Bing</au><au>Lin, Tongkui</au><au>Li, Zhiqing</au><au>Wang, Jialin</au><au>Sun, Yuwei</au><au>Wang, Danna</au><au>Ye, Jin</au><au>Zhang, Yajuan</au><au>Kou, Rongwei</au><au>Zhao, Beita</au><au>Yi, Junjie</au><au>Bai, Gaiyan</au><au>Liu, Xuebo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lactiplantibacillus plantarum Regulates Intestinal Physiology and Enteric Neurons in IBS through Microbial Tryptophan Metabolites</atitle><jtitle>Journal of agricultural and food chemistry</jtitle><addtitle>J. Agric. Food Chem</addtitle><date>2024-08-14</date><risdate>2024</risdate><volume>72</volume><issue>32</issue><spage>17989</spage><epage>18002</epage><pages>17989-18002</pages><issn>0021-8561</issn><issn>1520-5118</issn><eissn>1520-5118</eissn><abstract>Irritable bowel syndrome (IBS) is a prevalent functional gastrointestinal disorder characterized by visceral pain and gut dysmotility. However, the specific mechanisms by which Lactobacillus strains relieve IBS remain unclear. Here, we screened Lactobacillus strains from traditional Chinese fermented foods with potential IBS-alleviating properties through in vitro and in vivo experiments. We demonstrated that Lactiplantibacillus plantarum D266 (Lp D266) administration effectively modulates intestinal peristalsis, enteric neurons, visceral hypersensitivity, colonic inflammation, gut barrier function, and mast cell activation. Additionally, Lp D266 shapes gut microbiota and enhances tryptophan (Trp) metabolism, thus activating the aryl hydrocarbon receptor (AhR) and subsequently enhancing IL-22 production to maintain gut homeostasis. Mechanistically, Lp D266 potentially modulates colonic physiology and enteric neurons by microbial tryptophan metabolites. Further, our study indicates that combining Lp D266 with Trp synergistically ameliorates IBS symptoms. 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| subjects | absorption barrier aryl hydrocarbon receptors Bioactive Constituents, Metabolites, and Functions fermentation food chemistry homeostasis hypersensitivity inflammation intestinal microorganisms intestines irritable bowel syndrome Lactobacillus mast cells metabolites nutritional intervention pain peristalsis tryptophan |
| title | Lactiplantibacillus plantarum Regulates Intestinal Physiology and Enteric Neurons in IBS through Microbial Tryptophan Metabolites |
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