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Tannic acid alleviates ETEC K88‐induced intestinal damage through regulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway in IPEC‐J2 cells
BACKGROUND Tannic acid (TA), a naturally occurring polyphenol, has shown diverse potential in preventing intestinal damage in piglet diarrhea induced by Enterotoxigenic Escherichia coli (ETEC) K88. However, the protective effect of TA on ETEC k88 infection‐induced post‐weaning diarrhea and its poten...
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| Published in: | Journal of the science of food and agriculture 2024-07, Vol.104 (9), p.5186-5196 |
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| container_end_page | 5196 |
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| container_title | Journal of the science of food and agriculture |
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| creator | Liu, Wenhui Guo, Kangkang |
| description | BACKGROUND
Tannic acid (TA), a naturally occurring polyphenol, has shown diverse potential in preventing intestinal damage in piglet diarrhea induced by Enterotoxigenic Escherichia coli (ETEC) K88. However, the protective effect of TA on ETEC k88 infection‐induced post‐weaning diarrhea and its potential mechanism has not been well elucidated. Therefore, an animal trial was carried out to investigate the effects of dietary supplementation with TA on the intestinal diarrhea of weaned piglets challenged with ETEC K88. In addition, porcine intestinal epithelial cells were used as an in vitro model to explore the mechanism through which TA alleviates intestinal oxidative damage and inflammation.
RESULTS
The results indicated that TA supplementation (2 and 4 g kg−1) reduced diarrhea rate, enzyme activity (diamine oxidase [DAO] and Malondialdehyde [MAD]) and serum inflammatory cytokines concentration (TNF‐α and IL‐1β) (P |
| doi_str_mv | 10.1002/jsfa.13343 |
| format | article |
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Tannic acid (TA), a naturally occurring polyphenol, has shown diverse potential in preventing intestinal damage in piglet diarrhea induced by Enterotoxigenic Escherichia coli (ETEC) K88. However, the protective effect of TA on ETEC k88 infection‐induced post‐weaning diarrhea and its potential mechanism has not been well elucidated. Therefore, an animal trial was carried out to investigate the effects of dietary supplementation with TA on the intestinal diarrhea of weaned piglets challenged with ETEC K88. In addition, porcine intestinal epithelial cells were used as an in vitro model to explore the mechanism through which TA alleviates intestinal oxidative damage and inflammation.
RESULTS
The results indicated that TA supplementation (2 and 4 g kg−1) reduced diarrhea rate, enzyme activity (diamine oxidase [DAO] and Malondialdehyde [MAD]) and serum inflammatory cytokines concentration (TNF‐α and IL‐1β) (P < 0.05) compared to the Infection group (IG), group in vivo. In vitro, TA treatment effectively alleviated ETEC‐induced cytotoxicity, increased the expression of ZO‐1, occludin and claudin‐1 at both mRNA and protein levels. Moreover, TA pre‐treatment increased the activity of antioxidant enzymes (such as T‐SOD) and decreased serum cytokine levels (TNF‐α and IL‐1β). Furthermore, TA increased cellular antioxidant capacity by activating the Nrf2 signaling pathway and decreased inflammatory response by down‐regulating the expression of TLR4, MyD88, NF‐kB and NLRP3.
CONCLUSION
The present study showed that TA reduced the diarrhea rate of weaned piglets by restoring the intestinal mucosal mechanical barrier function, alleviating oxidative stress and inflammation. The underlying mechanism was achieved by modulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway. © 2024 Society of Chemical Industry.</description><identifier>ISSN: 0022-5142</identifier><identifier>EISSN: 1097-0010</identifier><identifier>DOI: 10.1002/jsfa.13343</identifier><identifier>PMID: 38288747</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Animals ; Antioxidants ; Barriers ; Biocompatibility ; Cell Line ; Cytokines ; Cytotoxicity ; Damage prevention ; Diamines ; Diarrhea ; Diarrhea - drug therapy ; Diarrhea - microbiology ; Dietary supplements ; E coli ; Enterotoxigenic Escherichia coli ; Enzymatic activity ; Enzyme activity ; Epithelial cells ; Epithelial Cells - drug effects ; Epithelial Cells - metabolism ; Epithelium ; Escherichia coli Infections - drug therapy ; Escherichia coli Infections - microbiology ; ETEC K88 ; Immunoglobulins ; Inflammation ; Inflammatory response ; Intestinal Mucosa - drug effects ; Intestinal Mucosa - metabolism ; Intestinal Mucosa - microbiology ; Intestine ; Intestines - drug effects ; Intestines - microbiology ; Kelch-Like ECH-Associated Protein 1 - genetics ; Kelch-Like ECH-Associated Protein 1 - metabolism ; Mechanical properties ; mRNA ; MyD88 protein ; NF-E2-Related Factor 2 - genetics ; NF-E2-Related Factor 2 - metabolism ; NF-kappa B - genetics ; NF-kappa B - metabolism ; NLR Family, Pyrin Domain-Containing 3 Protein - metabolism ; Oxidative stress ; p62‐Nrf2‐keap1 ; Polyphenols ; post‐weaning diarrhea ; Signal transduction ; Signal Transduction - drug effects ; Swine ; Swine Diseases - drug therapy ; Swine Diseases - metabolism ; Swine Diseases - microbiology ; Tannic acid ; Tannins - pharmacology ; TLR4 protein ; TLR4‐NF‐κB‐NLRP3 ; Toll-Like Receptor 4 - genetics ; Toll-Like Receptor 4 - metabolism ; Toll-like receptors ; Weaning</subject><ispartof>Journal of the science of food and agriculture, 2024-07, Vol.104 (9), p.5186-5196</ispartof><rights>2024 Society of Chemical Industry.</rights><rights>2024 Society of Chemical Industry</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3163-6ed2ecda9a3c04f587ea321c6bb8fc75c726fabf94dc7f77bec31084d58c2e833</cites><orcidid>0009-0002-2350-4247</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38288747$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Wenhui</creatorcontrib><creatorcontrib>Guo, Kangkang</creatorcontrib><title>Tannic acid alleviates ETEC K88‐induced intestinal damage through regulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway in IPEC‐J2 cells</title><title>Journal of the science of food and agriculture</title><addtitle>J Sci Food Agric</addtitle><description>BACKGROUND
Tannic acid (TA), a naturally occurring polyphenol, has shown diverse potential in preventing intestinal damage in piglet diarrhea induced by Enterotoxigenic Escherichia coli (ETEC) K88. However, the protective effect of TA on ETEC k88 infection‐induced post‐weaning diarrhea and its potential mechanism has not been well elucidated. Therefore, an animal trial was carried out to investigate the effects of dietary supplementation with TA on the intestinal diarrhea of weaned piglets challenged with ETEC K88. In addition, porcine intestinal epithelial cells were used as an in vitro model to explore the mechanism through which TA alleviates intestinal oxidative damage and inflammation.
RESULTS
The results indicated that TA supplementation (2 and 4 g kg−1) reduced diarrhea rate, enzyme activity (diamine oxidase [DAO] and Malondialdehyde [MAD]) and serum inflammatory cytokines concentration (TNF‐α and IL‐1β) (P < 0.05) compared to the Infection group (IG), group in vivo. In vitro, TA treatment effectively alleviated ETEC‐induced cytotoxicity, increased the expression of ZO‐1, occludin and claudin‐1 at both mRNA and protein levels. Moreover, TA pre‐treatment increased the activity of antioxidant enzymes (such as T‐SOD) and decreased serum cytokine levels (TNF‐α and IL‐1β). Furthermore, TA increased cellular antioxidant capacity by activating the Nrf2 signaling pathway and decreased inflammatory response by down‐regulating the expression of TLR4, MyD88, NF‐kB and NLRP3.
CONCLUSION
The present study showed that TA reduced the diarrhea rate of weaned piglets by restoring the intestinal mucosal mechanical barrier function, alleviating oxidative stress and inflammation. The underlying mechanism was achieved by modulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway. © 2024 Society of Chemical Industry.</description><subject>Animals</subject><subject>Antioxidants</subject><subject>Barriers</subject><subject>Biocompatibility</subject><subject>Cell Line</subject><subject>Cytokines</subject><subject>Cytotoxicity</subject><subject>Damage prevention</subject><subject>Diamines</subject><subject>Diarrhea</subject><subject>Diarrhea - drug therapy</subject><subject>Diarrhea - microbiology</subject><subject>Dietary supplements</subject><subject>E coli</subject><subject>Enterotoxigenic Escherichia coli</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Epithelial cells</subject><subject>Epithelial Cells - drug effects</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelium</subject><subject>Escherichia coli Infections - drug therapy</subject><subject>Escherichia coli Infections - microbiology</subject><subject>ETEC K88</subject><subject>Immunoglobulins</subject><subject>Inflammation</subject><subject>Inflammatory response</subject><subject>Intestinal Mucosa - drug effects</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestinal Mucosa - microbiology</subject><subject>Intestine</subject><subject>Intestines - drug effects</subject><subject>Intestines - microbiology</subject><subject>Kelch-Like ECH-Associated Protein 1 - genetics</subject><subject>Kelch-Like ECH-Associated Protein 1 - metabolism</subject><subject>Mechanical properties</subject><subject>mRNA</subject><subject>MyD88 protein</subject><subject>NF-E2-Related Factor 2 - genetics</subject><subject>NF-E2-Related Factor 2 - metabolism</subject><subject>NF-kappa B - genetics</subject><subject>NF-kappa B - metabolism</subject><subject>NLR Family, Pyrin Domain-Containing 3 Protein - metabolism</subject><subject>Oxidative stress</subject><subject>p62‐Nrf2‐keap1</subject><subject>Polyphenols</subject><subject>post‐weaning diarrhea</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Swine</subject><subject>Swine Diseases - drug therapy</subject><subject>Swine Diseases - metabolism</subject><subject>Swine Diseases - microbiology</subject><subject>Tannic acid</subject><subject>Tannins - pharmacology</subject><subject>TLR4 protein</subject><subject>TLR4‐NF‐κB‐NLRP3</subject><subject>Toll-Like Receptor 4 - genetics</subject><subject>Toll-Like Receptor 4 - metabolism</subject><subject>Toll-like receptors</subject><subject>Weaning</subject><issn>0022-5142</issn><issn>1097-0010</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kU9uEzEUxi0EoqGw4QDIEhuENMV_ZmzPskQJtI1oVcLaemN7EofJzGBnqLLjCByAk3AIDsFJ8DSlCxZs_Oz3_d4n2x9Czyk5oYSwN5tYwwnlPOcP0ISSUmaEUPIQTZLIsoLm7Ag9iXFDCClLIR6jI66YUjKXE_RjCW3rDQbjLYamcV897FzEs-Vsii-U-v3tu2_tYJzFvk3CzrfQYAtbWDm8W4duWK1xcKuhgSStUsvhXrA09tlBT1P9EGqGobV4ubjOx_M8Lb9-vh23i-srjnvYrW9gn_zx2dVsmvrnDBvXNPEpelRDE92zu3qMPs1ny-n7bHH57mx6usgMp4JnwlnmjIUSuCF5XSjpgDNqRFWp2sjCSCZqqOoyt0bWUlYuzRGV20IZ5hTnx-jVwbcP3ZchPVJvfRxvAK3rhqhZyQhVkskioS__QTfdENKfRM2JkIITXtBEvT5QJnQxBlfrPvgthL2mRI-Z6TEzfZtZgl_cWQ7V1tl79G9ICaAH4MY3bv8fK33-cX56MP0DUP-nlg</recordid><startdate>202407</startdate><enddate>202407</enddate><creator>Liu, Wenhui</creator><creator>Guo, Kangkang</creator><general>John Wiley & Sons, Ltd</general><general>John Wiley and Sons, Limited</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QL</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7ST</scope><scope>7T5</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0009-0002-2350-4247</orcidid></search><sort><creationdate>202407</creationdate><title>Tannic acid alleviates ETEC K88‐induced intestinal damage through regulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway in IPEC‐J2 cells</title><author>Liu, Wenhui ; Guo, Kangkang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3163-6ed2ecda9a3c04f587ea321c6bb8fc75c726fabf94dc7f77bec31084d58c2e833</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Antioxidants</topic><topic>Barriers</topic><topic>Biocompatibility</topic><topic>Cell Line</topic><topic>Cytokines</topic><topic>Cytotoxicity</topic><topic>Damage prevention</topic><topic>Diamines</topic><topic>Diarrhea</topic><topic>Diarrhea - drug therapy</topic><topic>Diarrhea - microbiology</topic><topic>Dietary supplements</topic><topic>E coli</topic><topic>Enterotoxigenic Escherichia coli</topic><topic>Enzymatic activity</topic><topic>Enzyme activity</topic><topic>Epithelial cells</topic><topic>Epithelial Cells - drug effects</topic><topic>Epithelial Cells - metabolism</topic><topic>Epithelium</topic><topic>Escherichia coli Infections - drug therapy</topic><topic>Escherichia coli Infections - microbiology</topic><topic>ETEC K88</topic><topic>Immunoglobulins</topic><topic>Inflammation</topic><topic>Inflammatory response</topic><topic>Intestinal Mucosa - drug effects</topic><topic>Intestinal Mucosa - metabolism</topic><topic>Intestinal Mucosa - microbiology</topic><topic>Intestine</topic><topic>Intestines - drug effects</topic><topic>Intestines - microbiology</topic><topic>Kelch-Like ECH-Associated Protein 1 - genetics</topic><topic>Kelch-Like ECH-Associated Protein 1 - metabolism</topic><topic>Mechanical properties</topic><topic>mRNA</topic><topic>MyD88 protein</topic><topic>NF-E2-Related Factor 2 - genetics</topic><topic>NF-E2-Related Factor 2 - metabolism</topic><topic>NF-kappa B - genetics</topic><topic>NF-kappa B - metabolism</topic><topic>NLR Family, Pyrin Domain-Containing 3 Protein - metabolism</topic><topic>Oxidative stress</topic><topic>p62‐Nrf2‐keap1</topic><topic>Polyphenols</topic><topic>post‐weaning diarrhea</topic><topic>Signal transduction</topic><topic>Signal Transduction - drug effects</topic><topic>Swine</topic><topic>Swine Diseases - drug therapy</topic><topic>Swine Diseases - metabolism</topic><topic>Swine Diseases - microbiology</topic><topic>Tannic acid</topic><topic>Tannins - pharmacology</topic><topic>TLR4 protein</topic><topic>TLR4‐NF‐κB‐NLRP3</topic><topic>Toll-Like Receptor 4 - genetics</topic><topic>Toll-Like Receptor 4 - metabolism</topic><topic>Toll-like receptors</topic><topic>Weaning</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Wenhui</creatorcontrib><creatorcontrib>Guo, Kangkang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of the science of food and agriculture</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Wenhui</au><au>Guo, Kangkang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tannic acid alleviates ETEC K88‐induced intestinal damage through regulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway in IPEC‐J2 cells</atitle><jtitle>Journal of the science of food and agriculture</jtitle><addtitle>J Sci Food Agric</addtitle><date>2024-07</date><risdate>2024</risdate><volume>104</volume><issue>9</issue><spage>5186</spage><epage>5196</epage><pages>5186-5196</pages><issn>0022-5142</issn><eissn>1097-0010</eissn><abstract>BACKGROUND
Tannic acid (TA), a naturally occurring polyphenol, has shown diverse potential in preventing intestinal damage in piglet diarrhea induced by Enterotoxigenic Escherichia coli (ETEC) K88. However, the protective effect of TA on ETEC k88 infection‐induced post‐weaning diarrhea and its potential mechanism has not been well elucidated. Therefore, an animal trial was carried out to investigate the effects of dietary supplementation with TA on the intestinal diarrhea of weaned piglets challenged with ETEC K88. In addition, porcine intestinal epithelial cells were used as an in vitro model to explore the mechanism through which TA alleviates intestinal oxidative damage and inflammation.
RESULTS
The results indicated that TA supplementation (2 and 4 g kg−1) reduced diarrhea rate, enzyme activity (diamine oxidase [DAO] and Malondialdehyde [MAD]) and serum inflammatory cytokines concentration (TNF‐α and IL‐1β) (P < 0.05) compared to the Infection group (IG), group in vivo. In vitro, TA treatment effectively alleviated ETEC‐induced cytotoxicity, increased the expression of ZO‐1, occludin and claudin‐1 at both mRNA and protein levels. Moreover, TA pre‐treatment increased the activity of antioxidant enzymes (such as T‐SOD) and decreased serum cytokine levels (TNF‐α and IL‐1β). Furthermore, TA increased cellular antioxidant capacity by activating the Nrf2 signaling pathway and decreased inflammatory response by down‐regulating the expression of TLR4, MyD88, NF‐kB and NLRP3.
CONCLUSION
The present study showed that TA reduced the diarrhea rate of weaned piglets by restoring the intestinal mucosal mechanical barrier function, alleviating oxidative stress and inflammation. The underlying mechanism was achieved by modulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway. © 2024 Society of Chemical Industry.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>38288747</pmid><doi>10.1002/jsfa.13343</doi><tpages>11</tpages><orcidid>https://orcid.org/0009-0002-2350-4247</orcidid></addata></record> |
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| ispartof | Journal of the science of food and agriculture, 2024-07, Vol.104 (9), p.5186-5196 |
| issn | 0022-5142 1097-0010 |
| language | eng |
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| source | Wiley |
| subjects | Animals Antioxidants Barriers Biocompatibility Cell Line Cytokines Cytotoxicity Damage prevention Diamines Diarrhea Diarrhea - drug therapy Diarrhea - microbiology Dietary supplements E coli Enterotoxigenic Escherichia coli Enzymatic activity Enzyme activity Epithelial cells Epithelial Cells - drug effects Epithelial Cells - metabolism Epithelium Escherichia coli Infections - drug therapy Escherichia coli Infections - microbiology ETEC K88 Immunoglobulins Inflammation Inflammatory response Intestinal Mucosa - drug effects Intestinal Mucosa - metabolism Intestinal Mucosa - microbiology Intestine Intestines - drug effects Intestines - microbiology Kelch-Like ECH-Associated Protein 1 - genetics Kelch-Like ECH-Associated Protein 1 - metabolism Mechanical properties mRNA MyD88 protein NF-E2-Related Factor 2 - genetics NF-E2-Related Factor 2 - metabolism NF-kappa B - genetics NF-kappa B - metabolism NLR Family, Pyrin Domain-Containing 3 Protein - metabolism Oxidative stress p62‐Nrf2‐keap1 Polyphenols post‐weaning diarrhea Signal transduction Signal Transduction - drug effects Swine Swine Diseases - drug therapy Swine Diseases - metabolism Swine Diseases - microbiology Tannic acid Tannins - pharmacology TLR4 protein TLR4‐NF‐κB‐NLRP3 Toll-Like Receptor 4 - genetics Toll-Like Receptor 4 - metabolism Toll-like receptors Weaning |
| title | Tannic acid alleviates ETEC K88‐induced intestinal damage through regulating the p62‐keap1‐Nrf2 and TLR4‐NF‐κB‐NLRP3 pathway in IPEC‐J2 cells |
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