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Study of the colonic epithelial-mesenchymal dialogue through establishment of two activated or not mesenchymal cell lines: Activated and resting ones differentially modulate colonocytes in co-culture
Continuous and rapid renewal of the colonic epithelium is crucial to resist the plethora of luminal deleterious agents. Subepithelial fibroblasts contribute to this turnover by regulating epithelial proliferation and differentiation. However, when intestinal homeostasis is disturbed, fibroblasts can...
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Published in: | PloS one 2022-08, Vol.17 (8), p.e0273858-e0273858 |
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description | Continuous and rapid renewal of the colonic epithelium is crucial to resist the plethora of luminal deleterious agents. Subepithelial fibroblasts contribute to this turnover by regulating epithelial proliferation and differentiation. However, when intestinal homeostasis is disturbed, fibroblasts can acquire an activated phenotype and play a major role in the progression of intestinal pathologies. To evaluate the involvement of fibroblasts in the regulation of colonocytes under homeostatic or pathological conditions, we established resting and activated conditionally immortalized fibroblast cell lines (nF and mF) from mouse colonic mucosa. We then studied the epithelial-mesenchymal interactions between activated or resting fibroblasts and the normal mouse colonocytes (Co) using a co-culture model. Both fibroblastic cell lines were characterized by RT-qPCR, western blot and immunofluorescence assay. Our results showed that nF and mF cells were positive for fibroblastic markers such as vimentin and collagen 1, and negative for cytokeratin 18 and E-cadherin, attesting to their fibroblastic type. They also expressed proteins characteristic of the epithelial stem cell niche such as Grem1, CD90 or Wnt5a. Only rare nF fibroblasts were positive for [alpha]-SMA, whereas all mF fibroblasts strongly expressed this marker, supporting that mF cells were activated fibroblasts/myofibroblasts. In coculture, nF fibroblasts and Co cells strongly interacted via paracrine exchanges resulting in BMP4 production in nF fibroblasts, activation of BMP signaling in Co colonocytes, and decreased growth of colonocytes. Activated-type mF fibroblasts did not exert the same effects on Co cells, allowing colonocytes free to proliferate. In conclusion, these two colonic fibroblast lines, associated with Co cells in coculture, should allow to better understand the role of mesenchymal cells in the preservation of homeostasis and the development of intestinal pathologies. |
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Subepithelial fibroblasts contribute to this turnover by regulating epithelial proliferation and differentiation. However, when intestinal homeostasis is disturbed, fibroblasts can acquire an activated phenotype and play a major role in the progression of intestinal pathologies. To evaluate the involvement of fibroblasts in the regulation of colonocytes under homeostatic or pathological conditions, we established resting and activated conditionally immortalized fibroblast cell lines (nF and mF) from mouse colonic mucosa. We then studied the epithelial-mesenchymal interactions between activated or resting fibroblasts and the normal mouse colonocytes (Co) using a co-culture model. Both fibroblastic cell lines were characterized by RT-qPCR, western blot and immunofluorescence assay. Our results showed that nF and mF cells were positive for fibroblastic markers such as vimentin and collagen 1, and negative for cytokeratin 18 and E-cadherin, attesting to their fibroblastic type. They also expressed proteins characteristic of the epithelial stem cell niche such as Grem1, CD90 or Wnt5a. Only rare nF fibroblasts were positive for [alpha]-SMA, whereas all mF fibroblasts strongly expressed this marker, supporting that mF cells were activated fibroblasts/myofibroblasts. In coculture, nF fibroblasts and Co cells strongly interacted via paracrine exchanges resulting in BMP4 production in nF fibroblasts, activation of BMP signaling in Co colonocytes, and decreased growth of colonocytes. Activated-type mF fibroblasts did not exert the same effects on Co cells, allowing colonocytes free to proliferate. In conclusion, these two colonic fibroblast lines, associated with Co cells in coculture, should allow to better understand the role of mesenchymal cells in the preservation of homeostasis and the development of intestinal pathologies.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0273858</identifier><identifier>PMID: 36040985</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>Analysis ; Antigens ; Apoptosis ; Bioinformatics ; Biology and Life Sciences ; Biomarkers ; Cell culture ; Cell lines ; Cloning ; Collagen ; Colorectal cancer ; Cytokeratin ; Cytokines ; E-cadherin ; Epithelium ; Extracellular matrix ; Fibroblasts ; Genomes ; Health aspects ; Homeostasis ; Immunofluorescence ; Inflammation ; Inflammatory bowel disease ; Intestine ; Life Sciences ; Medicine and Health Sciences ; Mesenchyme ; Mutation ; Paracrine signalling ; Phenotypes ; Proteins ; Research and Analysis Methods ; Stem cells ; Vimentin ; Wnt protein</subject><ispartof>PloS one, 2022-08, Vol.17 (8), p.e0273858-e0273858</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Plaisancié et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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In conclusion, these two colonic fibroblast lines, associated with Co cells in coculture, should allow to better understand the role of mesenchymal cells in the preservation of homeostasis and the development of intestinal pathologies.</description><subject>Analysis</subject><subject>Antigens</subject><subject>Apoptosis</subject><subject>Bioinformatics</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers</subject><subject>Cell culture</subject><subject>Cell lines</subject><subject>Cloning</subject><subject>Collagen</subject><subject>Colorectal cancer</subject><subject>Cytokeratin</subject><subject>Cytokines</subject><subject>E-cadherin</subject><subject>Epithelium</subject><subject>Extracellular matrix</subject><subject>Fibroblasts</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>Homeostasis</subject><subject>Immunofluorescence</subject><subject>Inflammation</subject><subject>Inflammatory bowel 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Jacques</au><au>Guéraud, Françoise</au><au>Pierre, Fabrice</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Study of the colonic epithelial-mesenchymal dialogue through establishment of two activated or not mesenchymal cell lines: Activated and resting ones differentially modulate colonocytes in co-culture</atitle><jtitle>PloS one</jtitle><date>2022-08-30</date><risdate>2022</risdate><volume>17</volume><issue>8</issue><spage>e0273858</spage><epage>e0273858</epage><pages>e0273858-e0273858</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Competing Interests: The authors have declared that no competing interests exist</notes><abstract>Continuous and rapid renewal of the colonic epithelium is crucial to resist the plethora of luminal deleterious agents. Subepithelial fibroblasts contribute to this turnover by regulating epithelial proliferation and differentiation. However, when intestinal homeostasis is disturbed, fibroblasts can acquire an activated phenotype and play a major role in the progression of intestinal pathologies. To evaluate the involvement of fibroblasts in the regulation of colonocytes under homeostatic or pathological conditions, we established resting and activated conditionally immortalized fibroblast cell lines (nF and mF) from mouse colonic mucosa. We then studied the epithelial-mesenchymal interactions between activated or resting fibroblasts and the normal mouse colonocytes (Co) using a co-culture model. Both fibroblastic cell lines were characterized by RT-qPCR, western blot and immunofluorescence assay. Our results showed that nF and mF cells were positive for fibroblastic markers such as vimentin and collagen 1, and negative for cytokeratin 18 and E-cadherin, attesting to their fibroblastic type. They also expressed proteins characteristic of the epithelial stem cell niche such as Grem1, CD90 or Wnt5a. Only rare nF fibroblasts were positive for [alpha]-SMA, whereas all mF fibroblasts strongly expressed this marker, supporting that mF cells were activated fibroblasts/myofibroblasts. In coculture, nF fibroblasts and Co cells strongly interacted via paracrine exchanges resulting in BMP4 production in nF fibroblasts, activation of BMP signaling in Co colonocytes, and decreased growth of colonocytes. Activated-type mF fibroblasts did not exert the same effects on Co cells, allowing colonocytes free to proliferate. In conclusion, these two colonic fibroblast lines, associated with Co cells in coculture, should allow to better understand the role of mesenchymal cells in the preservation of homeostasis and the development of intestinal pathologies.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>36040985</pmid><doi>10.1371/journal.pone.0273858</doi><tpages>e0273858</tpages><orcidid>https://orcid.org/0000-0003-1289-2870</orcidid><orcidid>https://orcid.org/0000-0001-5455-1244</orcidid><orcidid>https://orcid.org/0000-0002-3670-6684</orcidid><orcidid>https://orcid.org/0000-0001-6106-8146</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Antigens Apoptosis Bioinformatics Biology and Life Sciences Biomarkers Cell culture Cell lines Cloning Collagen Colorectal cancer Cytokeratin Cytokines E-cadherin Epithelium Extracellular matrix Fibroblasts Genomes Health aspects Homeostasis Immunofluorescence Inflammation Inflammatory bowel disease Intestine Life Sciences Medicine and Health Sciences Mesenchyme Mutation Paracrine signalling Phenotypes Proteins Research and Analysis Methods Stem cells Vimentin Wnt protein |
title | Study of the colonic epithelial-mesenchymal dialogue through establishment of two activated or not mesenchymal cell lines: Activated and resting ones differentially modulate colonocytes in co-culture |
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