Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers
Butyrate, one of the SCFA, promotes the development of the intestinal barrier. However, the molecular mechanisms underlying the butyrate regulation of the intestinal barrier are unknown. To test the hypothesis that the effect of butyrate on the intestinal barrier is mediated by the regulation of the...
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| Veröffentlicht in: | The Journal of nutrition 2009-09, Vol.139 (9), p.1619-1625 |
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| creator | Peng, Luying Li, Zhong-Rong Green, Robert S Holzman, Ian R Lin, Jing |
| description | Butyrate, one of the SCFA, promotes the development of the intestinal barrier. However, the molecular mechanisms underlying the butyrate regulation of the intestinal barrier are unknown. To test the hypothesis that the effect of butyrate on the intestinal barrier is mediated by the regulation of the assembly of tight junctions involving the activation of the AMP-activated protein kinase (AMPK), we determined the effect of butyrate on the intestinal barrier by measuring the transepithelial electrical resistance (TER) and inulin permeability in a Caco-2 cell monolayer model. We further used a calcium switch assay to study the assembly of epithelial tight junctions and determined the effect of butyrate on the assembly of epithelial tight junctions and AMPK activity. We demonstrated that the butyrate treatment increased AMPK activity and accelerated the assembly of tight junctions as shown by the reorganization of tight junction proteins, as well as the development of TER. AMPK activity was also upregulated by butyrate during calcium switch-induced tight junction assembly. Compound C, a specific AMPK inhibitor, inhibited the butyrate-induced activation of AMPK. The facilitating effect of butyrate on the increases in TER in standard culture media, as well as after calcium switch, was abolished by compound C. We conclude that butyrate enhances the intestinal barrier by regulating the assembly of tight junctions. This dynamic process is mediated by the activation of AMPK. These results suggest an intriguing link between SCFA and the intracellular energy sensor for the development of the intestinal barrier. |
| doi_str_mv | 10.3945/jn.109.104638 |
| format | Article |
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However, the molecular mechanisms underlying the butyrate regulation of the intestinal barrier are unknown. To test the hypothesis that the effect of butyrate on the intestinal barrier is mediated by the regulation of the assembly of tight junctions involving the activation of the AMP-activated protein kinase (AMPK), we determined the effect of butyrate on the intestinal barrier by measuring the transepithelial electrical resistance (TER) and inulin permeability in a Caco-2 cell monolayer model. We further used a calcium switch assay to study the assembly of epithelial tight junctions and determined the effect of butyrate on the assembly of epithelial tight junctions and AMPK activity. We demonstrated that the butyrate treatment increased AMPK activity and accelerated the assembly of tight junctions as shown by the reorganization of tight junction proteins, as well as the development of TER. AMPK activity was also upregulated by butyrate during calcium switch-induced tight junction assembly. Compound C, a specific AMPK inhibitor, inhibited the butyrate-induced activation of AMPK. The facilitating effect of butyrate on the increases in TER in standard culture media, as well as after calcium switch, was abolished by compound C. We conclude that butyrate enhances the intestinal barrier by regulating the assembly of tight junctions. This dynamic process is mediated by the activation of AMPK. These results suggest an intriguing link between SCFA and the intracellular energy sensor for the development of the intestinal barrier.</description><identifier>ISSN: 0022-3166</identifier><identifier>EISSN: 1541-6100</identifier><identifier>DOI: 10.3945/jn.109.104638</identifier><identifier>PMID: 19625695</identifier><identifier>CODEN: JONUAI</identifier><language>eng</language><publisher>Bethesda, MD: American Society for Nutrition</publisher><subject>adenosine monophosphate ; AMP-Activated Protein Kinases - metabolism ; Biochemical, Molecular, and Genetic Mechanisms ; Biological and medical sciences ; Butyrates - metabolism ; butyric acid ; Caco-2 Cells ; colon ; dose response ; Electric Impedance ; electrical resistance ; enzyme activation ; epithelial cells ; Epithelium - enzymology ; Epithelium - metabolism ; Feeding. Feeding behavior ; Fundamental and applied biological sciences. Psychology ; human cell lines ; human physiology ; Humans ; intestinal absorption ; Intestinal Mucosa - cytology ; Intestinal Mucosa - enzymology ; Intestinal Mucosa - metabolism ; inulin ; Inulin - metabolism ; measurement ; Membrane Proteins - metabolism ; nutrient uptake ; permeability ; Permeability - drug effects ; Phosphorylation ; Protein Kinase Inhibitors - metabolism ; protein kinases ; tight junctions ; Tight Junctions - enzymology ; Tight Junctions - metabolism ; Up-Regulation ; Vertebrates: anatomy and physiology, studies on body, several organs or systems</subject><ispartof>The Journal of nutrition, 2009-09, Vol.139 (9), p.1619-1625</ispartof><rights>2009 INIST-CNRS</rights><rights>Copyright © 2009, American Society for Nutrition 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c549t-152dba96ce2d52b15368d6c68c592e5e04c692ea6f565da096c2005a91b233393</citedby><cites>FETCH-LOGICAL-c549t-152dba96ce2d52b15368d6c68c592e5e04c692ea6f565da096c2005a91b233393</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=21888418$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19625695$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Peng, Luying</creatorcontrib><creatorcontrib>Li, Zhong-Rong</creatorcontrib><creatorcontrib>Green, Robert S</creatorcontrib><creatorcontrib>Holzman, Ian R</creatorcontrib><creatorcontrib>Lin, Jing</creatorcontrib><title>Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers</title><title>The Journal of nutrition</title><addtitle>J Nutr</addtitle><description>Butyrate, one of the SCFA, promotes the development of the intestinal barrier. However, the molecular mechanisms underlying the butyrate regulation of the intestinal barrier are unknown. To test the hypothesis that the effect of butyrate on the intestinal barrier is mediated by the regulation of the assembly of tight junctions involving the activation of the AMP-activated protein kinase (AMPK), we determined the effect of butyrate on the intestinal barrier by measuring the transepithelial electrical resistance (TER) and inulin permeability in a Caco-2 cell monolayer model. We further used a calcium switch assay to study the assembly of epithelial tight junctions and determined the effect of butyrate on the assembly of epithelial tight junctions and AMPK activity. We demonstrated that the butyrate treatment increased AMPK activity and accelerated the assembly of tight junctions as shown by the reorganization of tight junction proteins, as well as the development of TER. AMPK activity was also upregulated by butyrate during calcium switch-induced tight junction assembly. Compound C, a specific AMPK inhibitor, inhibited the butyrate-induced activation of AMPK. The facilitating effect of butyrate on the increases in TER in standard culture media, as well as after calcium switch, was abolished by compound C. We conclude that butyrate enhances the intestinal barrier by regulating the assembly of tight junctions. This dynamic process is mediated by the activation of AMPK. These results suggest an intriguing link between SCFA and the intracellular energy sensor for the development of the intestinal barrier.</description><subject>adenosine monophosphate</subject><subject>AMP-Activated Protein Kinases - metabolism</subject><subject>Biochemical, Molecular, and Genetic Mechanisms</subject><subject>Biological and medical sciences</subject><subject>Butyrates - metabolism</subject><subject>butyric acid</subject><subject>Caco-2 Cells</subject><subject>colon</subject><subject>dose response</subject><subject>Electric Impedance</subject><subject>electrical resistance</subject><subject>enzyme activation</subject><subject>epithelial cells</subject><subject>Epithelium - enzymology</subject><subject>Epithelium - metabolism</subject><subject>Feeding. Feeding behavior</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>human cell lines</subject><subject>human physiology</subject><subject>Humans</subject><subject>intestinal absorption</subject><subject>Intestinal Mucosa - cytology</subject><subject>Intestinal Mucosa - enzymology</subject><subject>Intestinal Mucosa - metabolism</subject><subject>inulin</subject><subject>Inulin - metabolism</subject><subject>measurement</subject><subject>Membrane Proteins - metabolism</subject><subject>nutrient uptake</subject><subject>permeability</subject><subject>Permeability - drug effects</subject><subject>Phosphorylation</subject><subject>Protein Kinase Inhibitors - metabolism</subject><subject>protein kinases</subject><subject>tight junctions</subject><subject>Tight Junctions - enzymology</subject><subject>Tight Junctions - metabolism</subject><subject>Up-Regulation</subject><subject>Vertebrates: anatomy and physiology, studies on body, several organs or systems</subject><issn>0022-3166</issn><issn>1541-6100</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVks1uEzEUhS0EoqGwZAvewG6Kf8bueIOURm0ptKIS7dq64_EkjiZ2azuR5lF42zpkVGBh-ercT-faPkboPSUnXNXiy9qfUKLKqiVvXqAZFTWtJCXkJZoRwljFqZRH6E1Ka0IIrVXzGh1RJZmQSszQ77NtHiNki8_9CryxCeeVxVc-25SdhwGfQYzORtyO-AKMG1yG0ljiO7dcZfx96012weN5SnbTDiPeOcDzou3gjx56PL-5rSbFdvg2hmydxz-Ke7K4VAswoWJ4YYcB3wQfBhhtTG_Rqx6GZN9N-zG6vzi_W3yrrn9eXi3m15URtcoVFaxrQUljWSdYSwWXTSeNbIxQzApLaiNLAbIXUnRACskIEaBoyzjnih-jrwffh227sZ2xPkcY9EN0G4ijDuD0_x3vVnoZdpqdskY2e4PPk0EMj9vybHrjkimXAW_DNml5KhSv6R6sDqCJIaVo--chlOh9mHrtS6n0IczCf_j3ZH_pKb0CfJoASAaGPpYAXXrmGG2apqZ7o48HroegYRkLc_-LEcpJ-RuKcMqfAMrPsu0</recordid><startdate>20090901</startdate><enddate>20090901</enddate><creator>Peng, Luying</creator><creator>Li, Zhong-Rong</creator><creator>Green, Robert S</creator><creator>Holzman, Ian R</creator><creator>Lin, Jing</creator><general>American Society for Nutrition</general><scope>FBQ</scope><scope>IQODW</scope><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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20090901</creationdate><title>Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers</title><author>Peng, Luying ; Li, Zhong-Rong ; Green, Robert S ; Holzman, Ian R ; Lin, Jing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c549t-152dba96ce2d52b15368d6c68c592e5e04c692ea6f565da096c2005a91b233393</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>adenosine monophosphate</topic><topic>AMP-Activated Protein Kinases - metabolism</topic><topic>Biochemical, Molecular, and Genetic Mechanisms</topic><topic>Biological and medical sciences</topic><topic>Butyrates - metabolism</topic><topic>butyric acid</topic><topic>Caco-2 Cells</topic><topic>colon</topic><topic>dose response</topic><topic>Electric Impedance</topic><topic>electrical resistance</topic><topic>enzyme activation</topic><topic>epithelial cells</topic><topic>Epithelium - enzymology</topic><topic>Epithelium - metabolism</topic><topic>Feeding. Feeding behavior</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>human cell lines</topic><topic>human physiology</topic><topic>Humans</topic><topic>intestinal absorption</topic><topic>Intestinal Mucosa - cytology</topic><topic>Intestinal Mucosa - enzymology</topic><topic>Intestinal Mucosa - metabolism</topic><topic>inulin</topic><topic>Inulin - metabolism</topic><topic>measurement</topic><topic>Membrane Proteins - metabolism</topic><topic>nutrient uptake</topic><topic>permeability</topic><topic>Permeability - drug effects</topic><topic>Phosphorylation</topic><topic>Protein Kinase Inhibitors - metabolism</topic><topic>protein kinases</topic><topic>tight junctions</topic><topic>Tight Junctions - enzymology</topic><topic>Tight Junctions - metabolism</topic><topic>Up-Regulation</topic><topic>Vertebrates: anatomy and physiology, studies on body, several organs or systems</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Peng, Luying</creatorcontrib><creatorcontrib>Li, Zhong-Rong</creatorcontrib><creatorcontrib>Green, Robert S</creatorcontrib><creatorcontrib>Holzman, Ian R</creatorcontrib><creatorcontrib>Lin, Jing</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of nutrition</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Peng, Luying</au><au>Li, Zhong-Rong</au><au>Green, Robert S</au><au>Holzman, Ian R</au><au>Lin, Jing</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers</atitle><jtitle>The Journal of nutrition</jtitle><addtitle>J Nutr</addtitle><date>2009-09-01</date><risdate>2009</risdate><volume>139</volume><issue>9</issue><spage>1619</spage><epage>1625</epage><pages>1619-1625</pages><issn>0022-3166</issn><eissn>1541-6100</eissn><coden>JONUAI</coden><abstract>Butyrate, one of the SCFA, promotes the development of the intestinal barrier. However, the molecular mechanisms underlying the butyrate regulation of the intestinal barrier are unknown. To test the hypothesis that the effect of butyrate on the intestinal barrier is mediated by the regulation of the assembly of tight junctions involving the activation of the AMP-activated protein kinase (AMPK), we determined the effect of butyrate on the intestinal barrier by measuring the transepithelial electrical resistance (TER) and inulin permeability in a Caco-2 cell monolayer model. We further used a calcium switch assay to study the assembly of epithelial tight junctions and determined the effect of butyrate on the assembly of epithelial tight junctions and AMPK activity. We demonstrated that the butyrate treatment increased AMPK activity and accelerated the assembly of tight junctions as shown by the reorganization of tight junction proteins, as well as the development of TER. AMPK activity was also upregulated by butyrate during calcium switch-induced tight junction assembly. Compound C, a specific AMPK inhibitor, inhibited the butyrate-induced activation of AMPK. The facilitating effect of butyrate on the increases in TER in standard culture media, as well as after calcium switch, was abolished by compound C. We conclude that butyrate enhances the intestinal barrier by regulating the assembly of tight junctions. This dynamic process is mediated by the activation of AMPK. These results suggest an intriguing link between SCFA and the intracellular energy sensor for the development of the intestinal barrier.</abstract><cop>Bethesda, MD</cop><pub>American Society for Nutrition</pub><pmid>19625695</pmid><doi>10.3945/jn.109.104638</doi><tpages>7</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | adenosine monophosphate AMP-Activated Protein Kinases - metabolism Biochemical, Molecular, and Genetic Mechanisms Biological and medical sciences Butyrates - metabolism butyric acid Caco-2 Cells colon dose response Electric Impedance electrical resistance enzyme activation epithelial cells Epithelium - enzymology Epithelium - metabolism Feeding. Feeding behavior Fundamental and applied biological sciences. Psychology human cell lines human physiology Humans intestinal absorption Intestinal Mucosa - cytology Intestinal Mucosa - enzymology Intestinal Mucosa - metabolism inulin Inulin - metabolism measurement Membrane Proteins - metabolism nutrient uptake permeability Permeability - drug effects Phosphorylation Protein Kinase Inhibitors - metabolism protein kinases tight junctions Tight Junctions - enzymology Tight Junctions - metabolism Up-Regulation Vertebrates: anatomy and physiology, studies on body, several organs or systems |
| title | Butyrate Enhances the Intestinal Barrier by Facilitating Tight Junction Assembly via Activation of AMP-Activated Protein Kinase in Caco-2 Cell Monolayers |
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