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FSP1-positive fibroblasts are adipogenic niche and regulate adipose homeostasis
Adipocyte progenitors reside in the stromal vascular fraction (SVF) of adipose tissues that are composed of fibroblasts, immune cells, and endothelial cells. It remains to be elucidated how the SVF regulates adipocyte progenitor fate determination and adipose homeostasis. Here, we report that fibrob...
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| Published in: | PLoS biology 2018-08, Vol.16 (8), p.e2001493-e2001493 |
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| container_end_page | e2001493 |
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| creator | Zhang, Rui Gao, Yuan Zhao, Xiaotong Gao, Mei Wu, Yanjun Han, Yingying Qiao, Yuemei Luo, Zheng Yang, Li Chen, Jianfeng Ge, Gaoxiang |
| description | Adipocyte progenitors reside in the stromal vascular fraction (SVF) of adipose tissues that are composed of fibroblasts, immune cells, and endothelial cells. It remains to be elucidated how the SVF regulates adipocyte progenitor fate determination and adipose homeostasis. Here, we report that fibroblast-specific protein-1 (FSP1)+ fibroblasts in the SVF are essential to adipose homeostasis. FSP1+ fibroblasts, devoid of adipogenic potential, are adjacent to the preadipocytes in the SVF. Ablation of FSP1+ fibroblasts in mice severely diminishes fat content of adipose depots. Activation of canonical Wnt signaling in the FSP1+ fibroblasts results in gradual loss of adipose tissues and resistance to diet-induced obesity. Alterations in the FSP1+ fibroblasts reduce platelet-derived growth factor (PDGF)-BB signaling and result in the loss of preadipocytes. Reduced PDGF-BB signaling, meanwhile, impairs the adipogenic differentiation capability of preadipocytes by regulating matrix metalloproteinase (MMP) expression, extracellular matrix remodeling, and the activation of Yes-associated protein (YAP) signaling. Thus, FSP1+ fibroblasts are an important niche essential to the maintenance of the preadipocyte pool and its adipogenic potential in adipose homeostasis. |
| doi_str_mv | 10.1371/journal.pbio.2001493 |
| format | article |
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It remains to be elucidated how the SVF regulates adipocyte progenitor fate determination and adipose homeostasis. Here, we report that fibroblast-specific protein-1 (FSP1)+ fibroblasts in the SVF are essential to adipose homeostasis. FSP1+ fibroblasts, devoid of adipogenic potential, are adjacent to the preadipocytes in the SVF. Ablation of FSP1+ fibroblasts in mice severely diminishes fat content of adipose depots. Activation of canonical Wnt signaling in the FSP1+ fibroblasts results in gradual loss of adipose tissues and resistance to diet-induced obesity. Alterations in the FSP1+ fibroblasts reduce platelet-derived growth factor (PDGF)-BB signaling and result in the loss of preadipocytes. Reduced PDGF-BB signaling, meanwhile, impairs the adipogenic differentiation capability of preadipocytes by regulating matrix metalloproteinase (MMP) expression, extracellular matrix remodeling, and the activation of Yes-associated protein (YAP) signaling. Thus, FSP1+ fibroblasts are an important niche essential to the maintenance of the preadipocyte pool and its adipogenic potential in adipose homeostasis.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.2001493</identifier><identifier>PMID: 30080858</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Ablation ; Activation ; Adaptor Proteins, Signal Transducing - genetics ; Adaptor Proteins, Signal Transducing - metabolism ; Adipocytes ; Adipocytes - cytology ; Adipocytes - metabolism ; Adipose tissue ; Adipose Tissue - cytology ; Adipose Tissue - metabolism ; Animals ; Becaplermin - genetics ; Becaplermin - metabolism ; Biochemistry ; Biology ; Biology and Life Sciences ; Cancer ; Cell Cycle Proteins ; Cell Differentiation ; Diet, High-Fat - adverse effects ; Endothelial cells ; Extracellular Matrix ; Fibroblasts ; Fibroblasts - cytology ; Fibroblasts - metabolism ; Five year plans ; Gene Expression Regulation ; Growth factors ; Homeostasis ; Homeostasis - genetics ; Immune system ; Laboratories ; Male ; Matrix metalloproteinase ; Matrix metalloproteinases ; Matrix Metalloproteinases - genetics ; Matrix Metalloproteinases - metabolism ; Medicine and Health Sciences ; Metalloproteinase ; Mice ; Mice, Transgenic ; Obesity - etiology ; Obesity - genetics ; Obesity - metabolism ; Obesity - pathology ; Phosphoproteins - genetics ; Phosphoproteins - metabolism ; Platelet-derived growth factor ; Platelet-derived growth factor BB ; Preadipocytes ; Proteins ; Research and Analysis Methods ; S100 Calcium-Binding Protein A4 - genetics ; S100 Calcium-Binding Protein A4 - metabolism ; Signaling ; Stem Cells - cytology ; Stem Cells - metabolism ; Supervision ; Wnt protein ; Wnt Signaling Pathway ; Yes-associated protein ; Zhang, Yuan</subject><ispartof>PLoS biology, 2018-08, Vol.16 (8), p.e2001493-e2001493</ispartof><rights>2018 Zhang 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2018 Zhang et al 2018 Zhang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-e927096d6b6643756ddb345c2e6a107664c3a9f85eec3cb90ad900253693bf2d3</citedby><cites>FETCH-LOGICAL-c526t-e927096d6b6643756ddb345c2e6a107664c3a9f85eec3cb90ad900253693bf2d3</cites><orcidid>0000-0003-3189-8928</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2249753259/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2249753259?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768,75096</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30080858$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Rui</creatorcontrib><creatorcontrib>Gao, Yuan</creatorcontrib><creatorcontrib>Zhao, Xiaotong</creatorcontrib><creatorcontrib>Gao, Mei</creatorcontrib><creatorcontrib>Wu, Yanjun</creatorcontrib><creatorcontrib>Han, Yingying</creatorcontrib><creatorcontrib>Qiao, Yuemei</creatorcontrib><creatorcontrib>Luo, Zheng</creatorcontrib><creatorcontrib>Yang, Li</creatorcontrib><creatorcontrib>Chen, Jianfeng</creatorcontrib><creatorcontrib>Ge, Gaoxiang</creatorcontrib><title>FSP1-positive fibroblasts are adipogenic niche and regulate adipose homeostasis</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>Adipocyte progenitors reside in the stromal vascular fraction (SVF) of adipose tissues that are composed of fibroblasts, immune cells, and endothelial cells. It remains to be elucidated how the SVF regulates adipocyte progenitor fate determination and adipose homeostasis. Here, we report that fibroblast-specific protein-1 (FSP1)+ fibroblasts in the SVF are essential to adipose homeostasis. FSP1+ fibroblasts, devoid of adipogenic potential, are adjacent to the preadipocytes in the SVF. Ablation of FSP1+ fibroblasts in mice severely diminishes fat content of adipose depots. Activation of canonical Wnt signaling in the FSP1+ fibroblasts results in gradual loss of adipose tissues and resistance to diet-induced obesity. Alterations in the FSP1+ fibroblasts reduce platelet-derived growth factor (PDGF)-BB signaling and result in the loss of preadipocytes. Reduced PDGF-BB signaling, meanwhile, impairs the adipogenic differentiation capability of preadipocytes by regulating matrix metalloproteinase (MMP) expression, extracellular matrix remodeling, and the activation of Yes-associated protein (YAP) signaling. Thus, FSP1+ fibroblasts are an important niche essential to the maintenance of the preadipocyte pool and its adipogenic potential in adipose homeostasis.</description><subject>Ablation</subject><subject>Activation</subject><subject>Adaptor Proteins, Signal Transducing - genetics</subject><subject>Adaptor Proteins, Signal Transducing - metabolism</subject><subject>Adipocytes</subject><subject>Adipocytes - cytology</subject><subject>Adipocytes - metabolism</subject><subject>Adipose tissue</subject><subject>Adipose Tissue - cytology</subject><subject>Adipose Tissue - metabolism</subject><subject>Animals</subject><subject>Becaplermin - genetics</subject><subject>Becaplermin - metabolism</subject><subject>Biochemistry</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Cancer</subject><subject>Cell Cycle Proteins</subject><subject>Cell Differentiation</subject><subject>Diet, High-Fat - adverse effects</subject><subject>Endothelial cells</subject><subject>Extracellular Matrix</subject><subject>Fibroblasts</subject><subject>Fibroblasts - cytology</subject><subject>Fibroblasts - metabolism</subject><subject>Five year plans</subject><subject>Gene Expression Regulation</subject><subject>Growth factors</subject><subject>Homeostasis</subject><subject>Homeostasis - genetics</subject><subject>Immune system</subject><subject>Laboratories</subject><subject>Male</subject><subject>Matrix metalloproteinase</subject><subject>Matrix metalloproteinases</subject><subject>Matrix Metalloproteinases - genetics</subject><subject>Matrix Metalloproteinases - metabolism</subject><subject>Medicine and Health Sciences</subject><subject>Metalloproteinase</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Obesity - etiology</subject><subject>Obesity - genetics</subject><subject>Obesity - metabolism</subject><subject>Obesity - pathology</subject><subject>Phosphoproteins - genetics</subject><subject>Phosphoproteins - metabolism</subject><subject>Platelet-derived growth factor</subject><subject>Platelet-derived growth factor BB</subject><subject>Preadipocytes</subject><subject>Proteins</subject><subject>Research and Analysis Methods</subject><subject>S100 Calcium-Binding Protein A4 - genetics</subject><subject>S100 Calcium-Binding Protein A4 - metabolism</subject><subject>Signaling</subject><subject>Stem Cells - cytology</subject><subject>Stem Cells - metabolism</subject><subject>Supervision</subject><subject>Wnt protein</subject><subject>Wnt Signaling Pathway</subject><subject>Yes-associated protein</subject><subject>Zhang, Yuan</subject><issn>1545-7885</issn><issn>1544-9173</issn><issn>1545-7885</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptUk1r3DAQNaWh-Wj_QWkNueTirb4tXQolNG0gkEDbsxjJ410tXsuV7ED_fbxdJySlByHx5s2bN-IVxXtKVpTX9NM2TqmHbjW4EFeMECoMf1WcUClkVWstXz97HxenOW8JYcww_aY45oRooqU-KW6vftzRaog5jOEeyza4FF0HecwlJCyhCUNcYx98OZ_NDPRNmXA9dTAu1YzlJu4w5hFyyG-Loxa6jO-W-6z4dfX15-X36ub22_Xll5vKS6bGCg2riVGNckoJXkvVNI4L6RkqoKSeQc_BtFoieu6dIdCY2b7kynDXsoafFR8PukMXs13-IlvGhKklZ9LMjOsDo4mwtUMKO0h_bIRg_wIxrS2kMfgOLTUISjglKAWBqEFrwYwjDhkxXtBZ6_MybXI7bDz2Y4LuhejLSh82dh3vrSK1ZlrMAheLQIq_J8yj3YXsseugxzjNvokWhhrC99Tzf6j_304cWD7FnBO2T2Yosft8PHbZfT7sko-57cPzRZ6aHgPBHwBJRri1</recordid><startdate>20180801</startdate><enddate>20180801</enddate><creator>Zhang, Rui</creator><creator>Gao, Yuan</creator><creator>Zhao, Xiaotong</creator><creator>Gao, Mei</creator><creator>Wu, Yanjun</creator><creator>Han, Yingying</creator><creator>Qiao, Yuemei</creator><creator>Luo, Zheng</creator><creator>Yang, Li</creator><creator>Chen, Jianfeng</creator><creator>Ge, Gaoxiang</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><scope>CZG</scope><orcidid>https://orcid.org/0000-0003-3189-8928</orcidid></search><sort><creationdate>20180801</creationdate><title>FSP1-positive fibroblasts are adipogenic niche and regulate adipose homeostasis</title><author>Zhang, Rui ; Gao, Yuan ; Zhao, Xiaotong ; Gao, Mei ; Wu, Yanjun ; Han, Yingying ; Qiao, Yuemei ; Luo, Zheng ; Yang, Li ; Chen, Jianfeng ; Ge, Gaoxiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-e927096d6b6643756ddb345c2e6a107664c3a9f85eec3cb90ad900253693bf2d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Ablation</topic><topic>Activation</topic><topic>Adaptor Proteins, Signal Transducing - 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It remains to be elucidated how the SVF regulates adipocyte progenitor fate determination and adipose homeostasis. Here, we report that fibroblast-specific protein-1 (FSP1)+ fibroblasts in the SVF are essential to adipose homeostasis. FSP1+ fibroblasts, devoid of adipogenic potential, are adjacent to the preadipocytes in the SVF. Ablation of FSP1+ fibroblasts in mice severely diminishes fat content of adipose depots. Activation of canonical Wnt signaling in the FSP1+ fibroblasts results in gradual loss of adipose tissues and resistance to diet-induced obesity. Alterations in the FSP1+ fibroblasts reduce platelet-derived growth factor (PDGF)-BB signaling and result in the loss of preadipocytes. Reduced PDGF-BB signaling, meanwhile, impairs the adipogenic differentiation capability of preadipocytes by regulating matrix metalloproteinase (MMP) expression, extracellular matrix remodeling, and the activation of Yes-associated protein (YAP) signaling. Thus, FSP1+ fibroblasts are an important niche essential to the maintenance of the preadipocyte pool and its adipogenic potential in adipose homeostasis.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>30080858</pmid><doi>10.1371/journal.pbio.2001493</doi><orcidid>https://orcid.org/0000-0003-3189-8928</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Ablation Activation Adaptor Proteins, Signal Transducing - genetics Adaptor Proteins, Signal Transducing - metabolism Adipocytes Adipocytes - cytology Adipocytes - metabolism Adipose tissue Adipose Tissue - cytology Adipose Tissue - metabolism Animals Becaplermin - genetics Becaplermin - metabolism Biochemistry Biology Biology and Life Sciences Cancer Cell Cycle Proteins Cell Differentiation Diet, High-Fat - adverse effects Endothelial cells Extracellular Matrix Fibroblasts Fibroblasts - cytology Fibroblasts - metabolism Five year plans Gene Expression Regulation Growth factors Homeostasis Homeostasis - genetics Immune system Laboratories Male Matrix metalloproteinase Matrix metalloproteinases Matrix Metalloproteinases - genetics Matrix Metalloproteinases - metabolism Medicine and Health Sciences Metalloproteinase Mice Mice, Transgenic Obesity - etiology Obesity - genetics Obesity - metabolism Obesity - pathology Phosphoproteins - genetics Phosphoproteins - metabolism Platelet-derived growth factor Platelet-derived growth factor BB Preadipocytes Proteins Research and Analysis Methods S100 Calcium-Binding Protein A4 - genetics S100 Calcium-Binding Protein A4 - metabolism Signaling Stem Cells - cytology Stem Cells - metabolism Supervision Wnt protein Wnt Signaling Pathway Yes-associated protein Zhang, Yuan |
| title | FSP1-positive fibroblasts are adipogenic niche and regulate adipose homeostasis |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-23T16%3A15%3A54IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=FSP1-positive%20fibroblasts%20are%20adipogenic%20niche%20and%20regulate%20adipose%20homeostasis&rft.jtitle=PLoS%20biology&rft.au=Zhang,%20Rui&rft.date=2018-08-01&rft.volume=16&rft.issue=8&rft.spage=e2001493&rft.epage=e2001493&rft.pages=e2001493-e2001493&rft.issn=1545-7885&rft.eissn=1545-7885&rft_id=info:doi/10.1371/journal.pbio.2001493&rft_dat=%3Cproquest_plos_%3E2084919034%3C/proquest_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c526t-e927096d6b6643756ddb345c2e6a107664c3a9f85eec3cb90ad900253693bf2d3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2249753259&rft_id=info:pmid/30080858&rfr_iscdi=true |