Terminal differentiation of villus tip enterocytes is governed by distinct Tgfβ superfamily members
The protective and absorptive functions of the intestinal epithelium rely on differentiated enterocytes in the villi. The differentiation of enterocytes is orchestrated by sub‐epithelial mesenchymal cells producing distinct ligands along the villus axis, in particular Bmps and Tgfβ. Here, we show th...
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| creator | Berková, Linda Fazilaty, Hassan Yang, Qiutan Kubovčiak, Jan Stastna, Monika Hrckulak, Dusan Vojtechova, Martina Dalessi, Tosca Brügger, Michael David Hausmann, George Liberali, Prisca Korinek, Vladimir Basler, Konrad Valenta, Tomas |
| description | The protective and absorptive functions of the intestinal epithelium rely on differentiated enterocytes in the villi. The differentiation of enterocytes is orchestrated by sub‐epithelial mesenchymal cells producing distinct ligands along the villus axis, in particular Bmps and Tgfβ. Here, we show that individual Bmp ligands and Tgfβ drive distinct enterocytic programs specific to villus zonation. Bmp4 is expressed from the centre to the upper part of the villus and activates preferentially genes connected to lipid uptake and metabolism. In contrast, Bmp2 is produced by villus tip mesenchymal cells and it influences the adhesive properties of villus tip epithelial cells and the expression of immunomodulators. Additionally, Tgfβ induces epithelial gene expression programs similar to those triggered by Bmp2. Bmp2‐driven villus tip program is activated by a canonical Bmp receptor type I/Smad‐dependent mechanism. Finally, we establish an organoid cultivation system that enriches villus tip enterocytes and thereby better mimics the cellular composition of the intestinal epithelium. Our data suggest that not only a Bmp gradient but also the activity of individual Bmp drives specific enterocytic programs.
Synopsis
While moving upwards the intestinal villi enterocytes acquire different cellular fates, which is promoted by a gradient of Bmp ligands. In addition to this gradient individual Bmps have distinct activities in the differentiation of enterocytes.
Bmp4 induces the expression of genes involved in lipid metabolism and uptake.
Bmp2 promotes the terminal differentiation of enterocytes by activating villus tip programs.
Bmp2‐driven differentiation depends on Bmp receptor type I and Smad4.
The addition of Bmp2 enriches terminally differentiated enterocytes in intestinal organoids.
Graphical Abstract
While moving upwards, the intestinal villi enterocytes acquire different cellular fates, which are promoted by a gradient of Bmp ligands. In addition to this gradient, individual Bmps have distinct activities in the differentiation of enterocytes. |
| doi_str_mv | 10.15252/embr.202256454 |
| format | Article |
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Synopsis
While moving upwards the intestinal villi enterocytes acquire different cellular fates, which is promoted by a gradient of Bmp ligands. In addition to this gradient individual Bmps have distinct activities in the differentiation of enterocytes.
Bmp4 induces the expression of genes involved in lipid metabolism and uptake.
Bmp2 promotes the terminal differentiation of enterocytes by activating villus tip programs.
Bmp2‐driven differentiation depends on Bmp receptor type I and Smad4.
The addition of Bmp2 enriches terminally differentiated enterocytes in intestinal organoids.
Graphical Abstract
While moving upwards, the intestinal villi enterocytes acquire different cellular fates, which are promoted by a gradient of Bmp ligands. In addition to this gradient, individual Bmps have distinct activities in the differentiation of enterocytes.</description><identifier>ISSN: 1469-221X</identifier><identifier>EISSN: 1469-3178</identifier><identifier>DOI: 10.15252/embr.202256454</identifier><identifier>PMID: 37493498</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Absorptivity ; Bone morphogenetic protein 2 ; Cell adhesion & migration ; Differentiation ; EMBO11 ; EMBO37 ; Enterocytes ; Epithelial cells ; Epithelium ; Gene expression ; Genes ; Immunomodulation ; Immunomodulators ; Intestine ; Life Sciences ; Ligands ; Lipid metabolism ; Lipids ; Mesenchyme ; Metabolism ; Organoids ; Receptors ; Smad protein ; Smad4 protein ; Stromal cells ; Villus ; Zonation</subject><ispartof>EMBO reports, 2023-09, Vol.24 (9), p.e56454-e56454</ispartof><rights>The Author(s) 2023</rights><rights>2023 The Authors. Published under the terms of the CC BY NC ND 4.0 license.</rights><rights>2023. This article is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-f5c2ccbe367a695f3713350aa0f2146a40aa8b4e0b649fa63e81b8192e747e533</citedby><cites>FETCH-LOGICAL-c463t-f5c2ccbe367a695f3713350aa0f2146a40aa8b4e0b649fa63e81b8192e747e533</cites><orcidid>0000-0002-9777-4664 ; 0000-0003-0695-6081 ; 0000-0002-1752-3612 ; 0000-0002-9387-0413 ; 0000-0003-3963-891X ; 0000-0003-3534-1529 ; 0000-0001-8792-2187 ; 0000-0002-3043-1835</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481656/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481656/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,41119,42188,51575,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37493498$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Berková, Linda</creatorcontrib><creatorcontrib>Fazilaty, Hassan</creatorcontrib><creatorcontrib>Yang, Qiutan</creatorcontrib><creatorcontrib>Kubovčiak, Jan</creatorcontrib><creatorcontrib>Stastna, Monika</creatorcontrib><creatorcontrib>Hrckulak, Dusan</creatorcontrib><creatorcontrib>Vojtechova, Martina</creatorcontrib><creatorcontrib>Dalessi, Tosca</creatorcontrib><creatorcontrib>Brügger, Michael David</creatorcontrib><creatorcontrib>Hausmann, George</creatorcontrib><creatorcontrib>Liberali, Prisca</creatorcontrib><creatorcontrib>Korinek, Vladimir</creatorcontrib><creatorcontrib>Basler, Konrad</creatorcontrib><creatorcontrib>Valenta, Tomas</creatorcontrib><title>Terminal differentiation of villus tip enterocytes is governed by distinct Tgfβ superfamily members</title><title>EMBO reports</title><addtitle>EMBO Rep</addtitle><addtitle>EMBO Rep</addtitle><description>The protective and absorptive functions of the intestinal epithelium rely on differentiated enterocytes in the villi. The differentiation of enterocytes is orchestrated by sub‐epithelial mesenchymal cells producing distinct ligands along the villus axis, in particular Bmps and Tgfβ. Here, we show that individual Bmp ligands and Tgfβ drive distinct enterocytic programs specific to villus zonation. Bmp4 is expressed from the centre to the upper part of the villus and activates preferentially genes connected to lipid uptake and metabolism. In contrast, Bmp2 is produced by villus tip mesenchymal cells and it influences the adhesive properties of villus tip epithelial cells and the expression of immunomodulators. Additionally, Tgfβ induces epithelial gene expression programs similar to those triggered by Bmp2. Bmp2‐driven villus tip program is activated by a canonical Bmp receptor type I/Smad‐dependent mechanism. Finally, we establish an organoid cultivation system that enriches villus tip enterocytes and thereby better mimics the cellular composition of the intestinal epithelium. Our data suggest that not only a Bmp gradient but also the activity of individual Bmp drives specific enterocytic programs.
Synopsis
While moving upwards the intestinal villi enterocytes acquire different cellular fates, which is promoted by a gradient of Bmp ligands. In addition to this gradient individual Bmps have distinct activities in the differentiation of enterocytes.
Bmp4 induces the expression of genes involved in lipid metabolism and uptake.
Bmp2 promotes the terminal differentiation of enterocytes by activating villus tip programs.
Bmp2‐driven differentiation depends on Bmp receptor type I and Smad4.
The addition of Bmp2 enriches terminally differentiated enterocytes in intestinal organoids.
Graphical Abstract
While moving upwards, the intestinal villi enterocytes acquire different cellular fates, which are promoted by a gradient of Bmp ligands. In addition to this gradient, individual Bmps have distinct activities in the differentiation of enterocytes.</description><subject>Absorptivity</subject><subject>Bone morphogenetic protein 2</subject><subject>Cell adhesion & migration</subject><subject>Differentiation</subject><subject>EMBO11</subject><subject>EMBO37</subject><subject>Enterocytes</subject><subject>Epithelial cells</subject><subject>Epithelium</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Immunomodulation</subject><subject>Immunomodulators</subject><subject>Intestine</subject><subject>Life Sciences</subject><subject>Ligands</subject><subject>Lipid metabolism</subject><subject>Lipids</subject><subject>Mesenchyme</subject><subject>Metabolism</subject><subject>Organoids</subject><subject>Receptors</subject><subject>Smad protein</subject><subject>Smad4 protein</subject><subject>Stromal cells</subject><subject>Villus</subject><subject>Zonation</subject><issn>1469-221X</issn><issn>1469-3178</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><recordid>eNp1kc1OGzEUha2KqqSha3bIEhs2Sfw_MyuEIvojIXUTJHaWx7kORjPjYM8g5bV4EJ4Jp0nTgsTKV77fPT7XB6FTSqZUMslm0NZxyghjUgkpPqERFaqacFqUR_uaMXp3jL6m9EAIkVVRfkHHvBAVF1U5QssFxNZ3psFL7xxE6Hpveh86HBx-8k0zJNz7Nc73EIPd9JCwT3gVniB2sMT1Jg-m3ne2x4uVe3nGaVhDdKb1zQa32R7EdII-O9Mk-LY_x-j2-_Vi_nNy8_vHr_nVzcQKxfuJk5ZZWwNXhVGVdLygnEtiDHEsr2JELstaAKmVqJxRHEpal7RiUIgCJOdjdLnTXQ91C0ubTUfT6HX0rYkbHYzXbzudv9d5FU2JKKmSKitc7BVieBwg9br1yULTmA7CkDQrBROSUc4yev4OfQhDzD-5pRSlSlFCMzXbUTaGlCK4gxtK9J8I9TZCfYgwT5z9v8SB_5tZBsgOSLnVrSD-e_gjzVd9QKpE</recordid><startdate>20230906</startdate><enddate>20230906</enddate><creator>Berková, Linda</creator><creator>Fazilaty, Hassan</creator><creator>Yang, Qiutan</creator><creator>Kubovčiak, Jan</creator><creator>Stastna, Monika</creator><creator>Hrckulak, Dusan</creator><creator>Vojtechova, Martina</creator><creator>Dalessi, Tosca</creator><creator>Brügger, Michael David</creator><creator>Hausmann, George</creator><creator>Liberali, Prisca</creator><creator>Korinek, Vladimir</creator><creator>Basler, Konrad</creator><creator>Valenta, Tomas</creator><general>Nature Publishing Group UK</general><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9777-4664</orcidid><orcidid>https://orcid.org/0000-0003-0695-6081</orcidid><orcidid>https://orcid.org/0000-0002-1752-3612</orcidid><orcidid>https://orcid.org/0000-0002-9387-0413</orcidid><orcidid>https://orcid.org/0000-0003-3963-891X</orcidid><orcidid>https://orcid.org/0000-0003-3534-1529</orcidid><orcidid>https://orcid.org/0000-0001-8792-2187</orcidid><orcidid>https://orcid.org/0000-0002-3043-1835</orcidid></search><sort><creationdate>20230906</creationdate><title>Terminal differentiation of villus tip enterocytes is governed by distinct Tgfβ superfamily members</title><author>Berková, Linda ; Fazilaty, Hassan ; Yang, Qiutan ; Kubovčiak, Jan ; Stastna, Monika ; Hrckulak, Dusan ; Vojtechova, Martina ; Dalessi, Tosca ; Brügger, Michael David ; Hausmann, George ; Liberali, Prisca ; Korinek, Vladimir ; Basler, Konrad ; Valenta, Tomas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-f5c2ccbe367a695f3713350aa0f2146a40aa8b4e0b649fa63e81b8192e747e533</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Absorptivity</topic><topic>Bone morphogenetic protein 2</topic><topic>Cell adhesion & migration</topic><topic>Differentiation</topic><topic>EMBO11</topic><topic>EMBO37</topic><topic>Enterocytes</topic><topic>Epithelial cells</topic><topic>Epithelium</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Immunomodulation</topic><topic>Immunomodulators</topic><topic>Intestine</topic><topic>Life Sciences</topic><topic>Ligands</topic><topic>Lipid metabolism</topic><topic>Lipids</topic><topic>Mesenchyme</topic><topic>Metabolism</topic><topic>Organoids</topic><topic>Receptors</topic><topic>Smad protein</topic><topic>Smad4 protein</topic><topic>Stromal cells</topic><topic>Villus</topic><topic>Zonation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Berková, Linda</creatorcontrib><creatorcontrib>Fazilaty, Hassan</creatorcontrib><creatorcontrib>Yang, Qiutan</creatorcontrib><creatorcontrib>Kubovčiak, Jan</creatorcontrib><creatorcontrib>Stastna, Monika</creatorcontrib><creatorcontrib>Hrckulak, Dusan</creatorcontrib><creatorcontrib>Vojtechova, Martina</creatorcontrib><creatorcontrib>Dalessi, Tosca</creatorcontrib><creatorcontrib>Brügger, Michael David</creatorcontrib><creatorcontrib>Hausmann, George</creatorcontrib><creatorcontrib>Liberali, Prisca</creatorcontrib><creatorcontrib>Korinek, Vladimir</creatorcontrib><creatorcontrib>Basler, Konrad</creatorcontrib><creatorcontrib>Valenta, Tomas</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>EMBO reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Berková, Linda</au><au>Fazilaty, Hassan</au><au>Yang, Qiutan</au><au>Kubovčiak, Jan</au><au>Stastna, Monika</au><au>Hrckulak, Dusan</au><au>Vojtechova, Martina</au><au>Dalessi, Tosca</au><au>Brügger, Michael David</au><au>Hausmann, George</au><au>Liberali, Prisca</au><au>Korinek, Vladimir</au><au>Basler, Konrad</au><au>Valenta, Tomas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Terminal differentiation of villus tip enterocytes is governed by distinct Tgfβ superfamily members</atitle><jtitle>EMBO reports</jtitle><stitle>EMBO Rep</stitle><addtitle>EMBO Rep</addtitle><date>2023-09-06</date><risdate>2023</risdate><volume>24</volume><issue>9</issue><spage>e56454</spage><epage>e56454</epage><pages>e56454-e56454</pages><issn>1469-221X</issn><eissn>1469-3178</eissn><abstract>The protective and absorptive functions of the intestinal epithelium rely on differentiated enterocytes in the villi. The differentiation of enterocytes is orchestrated by sub‐epithelial mesenchymal cells producing distinct ligands along the villus axis, in particular Bmps and Tgfβ. Here, we show that individual Bmp ligands and Tgfβ drive distinct enterocytic programs specific to villus zonation. Bmp4 is expressed from the centre to the upper part of the villus and activates preferentially genes connected to lipid uptake and metabolism. In contrast, Bmp2 is produced by villus tip mesenchymal cells and it influences the adhesive properties of villus tip epithelial cells and the expression of immunomodulators. Additionally, Tgfβ induces epithelial gene expression programs similar to those triggered by Bmp2. Bmp2‐driven villus tip program is activated by a canonical Bmp receptor type I/Smad‐dependent mechanism. Finally, we establish an organoid cultivation system that enriches villus tip enterocytes and thereby better mimics the cellular composition of the intestinal epithelium. Our data suggest that not only a Bmp gradient but also the activity of individual Bmp drives specific enterocytic programs.
Synopsis
While moving upwards the intestinal villi enterocytes acquire different cellular fates, which is promoted by a gradient of Bmp ligands. In addition to this gradient individual Bmps have distinct activities in the differentiation of enterocytes.
Bmp4 induces the expression of genes involved in lipid metabolism and uptake.
Bmp2 promotes the terminal differentiation of enterocytes by activating villus tip programs.
Bmp2‐driven differentiation depends on Bmp receptor type I and Smad4.
The addition of Bmp2 enriches terminally differentiated enterocytes in intestinal organoids.
Graphical Abstract
While moving upwards, the intestinal villi enterocytes acquire different cellular fates, which are promoted by a gradient of Bmp ligands. In addition to this gradient, individual Bmps have distinct activities in the differentiation of enterocytes.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>37493498</pmid><doi>10.15252/embr.202256454</doi><orcidid>https://orcid.org/0000-0002-9777-4664</orcidid><orcidid>https://orcid.org/0000-0003-0695-6081</orcidid><orcidid>https://orcid.org/0000-0002-1752-3612</orcidid><orcidid>https://orcid.org/0000-0002-9387-0413</orcidid><orcidid>https://orcid.org/0000-0003-3963-891X</orcidid><orcidid>https://orcid.org/0000-0003-3534-1529</orcidid><orcidid>https://orcid.org/0000-0001-8792-2187</orcidid><orcidid>https://orcid.org/0000-0002-3043-1835</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | EMBO reports, 2023-09, Vol.24 (9), p.e56454-e56454 |
| issn | 1469-221X 1469-3178 |
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| source | Springer Nature OA Free Journals; Wiley Free Content; EZB-FREE-00999 freely available EZB journals; Wiley Online Library All Journals; PubMed Central |
| subjects | Absorptivity Bone morphogenetic protein 2 Cell adhesion & migration Differentiation EMBO11 EMBO37 Enterocytes Epithelial cells Epithelium Gene expression Genes Immunomodulation Immunomodulators Intestine Life Sciences Ligands Lipid metabolism Lipids Mesenchyme Metabolism Organoids Receptors Smad protein Smad4 protein Stromal cells Villus Zonation |
| title | Terminal differentiation of villus tip enterocytes is governed by distinct Tgfβ superfamily members |
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