Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source
Increased visceral adipose tissue has been associated with metabolic dysfunction but the origin of the progenitors that give rise to this tissue, and whether they are the same as the progenitors contributing to the protective subcutaneous adipose tissue, was unclear. Hastie and colleagues have found...
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| Published in: | Nature cell biology Vol. 16; no. 4; pp. 367 - 375 |
|---|---|
| Main Authors: | , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
London
Nature Publishing Group UK
01.04.2014
Nature Publishing Group |
| Subjects: | |
| ISSN: | 1465-7392, 1476-4679, 1476-4679 |
| Online Access: | Get full text |
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| Abstract | Increased visceral adipose tissue has been associated with metabolic dysfunction but the origin of the progenitors that give rise to this tissue, and whether they are the same as the progenitors contributing to the protective subcutaneous adipose tissue, was unclear. Hastie and colleagues have found that Wt1-positive mesothelial cells contribute to visceral adipocytes.
Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes. |
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| AbstractList | Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem/progenitor cells from which it arises. While increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are 6 visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric and it is a subject of much debate whether these have common developmental origins and whether this differs from subcutaneous WAT. Here we show that all 6 visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue (BAT) arises from Wt1 expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1 expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated and provide several lines of evidence that Wt1 expressing mesothelium can produce adipocytes. These results: reveal a major ontogenetic difference between visceral and subcutaneous WAT; pinpoint the lateral plate mesoderm as a major source of visceral WAT; support the notion that visceral WAT progenitors are heterogeneous; and suggest that mesothelium is a source of adipocytes. Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes. : Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes. Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes.Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes. Increased visceral adipose tissue has been associated with metabolic dysfunction but the origin of the progenitors that give rise to this tissue, and whether they are the same as the progenitors contributing to the protective subcutaneous adipose tissue, was unclear. Hastie and colleagues have found that Wt1-positive mesothelial cells contribute to visceral adipocytes. Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells from which it arises. Whereas increased visceral fat mass is associated with metabolic dysfunction, increased subcutaneous WAT is protective. There are six visceral fat depots: perirenal, gonadal, epicardial, retroperitoneal, omental and mesenteric, and it is a subject of much debate whether these have a common developmental origin and whether this differs from that for subcutaneous WAT. Here we show that all six visceral WAT depots receive a significant contribution from cells expressing Wt1 late in gestation. Conversely, no subcutaneous WAT or brown adipose tissue arises from Wt1-expressing cells. Postnatally, a subset of visceral WAT continues to arise from Wt1-expressing cells, consistent with the finding that Wt1 marks a proportion of cell populations enriched in WAT progenitors. We show that all visceral fat depots have a mesothelial layer like the visceral organs with which they are associated, and provide several lines of evidence that Wt1-expressing mesothelium can produce adipocytes. These results reveal a major ontogenetic difference between visceral and subcutaneous WAT, and pinpoint the lateral plate mesoderm as a major source of visceral WAT. They also support the notion that visceral WAT progenitors are heterogeneous, and suggest that mesothelium is a source of adipocytes. |
| Audience | Academic |
| Author | Hastie, Nick Stimson, Roland H. Serrels, Alan Schedl, Andreas Slight, Joan Thornburn, Anna Walker, Brian R. Chapuli, Ramon Muñoz Lee, Martin Chau, You-Ying Berry, Rachel Bandiera, Roberto Qing, Wei Martínez-Estrada, Ofelia M. McHaffie, Sophie |
| AuthorAffiliation | 1 Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road, Edinburgh, EH4 2XU, UK 3 Institute for Genetics and Molecular Medicine at the University of Edinburgh, Edinburgh Cancer Research UK Centre, Western General Hospital Campus, Crewe Road South, Edinburgh, EH4 2XR 4 Department of Cell Biology, Faculty of Biology, University of Barcelona, Av. Diagonal, 643, 08028 Barcelona, Spain 5 BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh EH16 4TJ, UK 2 IBV, INSERM U1091, Univeriste de Nice Sophia-Antipolis, Parc Valrose, Centre de Biochimie, 06100 Nice Cedex-2 FRANCE 6 Department of Animal Biology, University of Málaga, E29071 Málaga, Spain |
| AuthorAffiliation_xml | – name: 1 Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road, Edinburgh, EH4 2XU, UK – name: 5 BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh, Edinburgh EH16 4TJ, UK – name: 3 Institute for Genetics and Molecular Medicine at the University of Edinburgh, Edinburgh Cancer Research UK Centre, Western General Hospital Campus, Crewe Road South, Edinburgh, EH4 2XR – name: 4 Department of Cell Biology, Faculty of Biology, University of Barcelona, Av. Diagonal, 643, 08028 Barcelona, Spain – name: 6 Department of Animal Biology, University of Málaga, E29071 Málaga, Spain – name: 2 IBV, INSERM U1091, Univeriste de Nice Sophia-Antipolis, Parc Valrose, Centre de Biochimie, 06100 Nice Cedex-2 FRANCE |
| Author_xml | – sequence: 1 givenname: You-Ying surname: Chau fullname: Chau, You-Ying email: You-Ying.Chau@igmm.ed.ac.uk organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK – sequence: 2 givenname: Roberto surname: Bandiera fullname: Bandiera, Roberto organization: IBV, INSERM U1091, Université de Nice Sophia-Antipolis, Parc Valrose, Centre de Biochimie 06100 Nice Cedex-2, France – sequence: 3 givenname: Alan surname: Serrels fullname: Serrels, Alan organization: Institute for Genetics and Molecular Medicine at the University of Edinburgh, Edinburgh Cancer Research UK Centre, Western General Hospital Campus, Crewe Road South Edinburgh EH4 2XR, UK – sequence: 4 givenname: Ofelia M. surname: Martínez-Estrada fullname: Martínez-Estrada, Ofelia M. organization: Department of Cell Biology, Faculty of Biology, University of Barcelona, Av. Diagonal, 643 08028 Barcelona, Spain – sequence: 5 givenname: Wei surname: Qing fullname: Qing, Wei organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK – sequence: 6 givenname: Martin surname: Lee fullname: Lee, Martin organization: Institute for Genetics and Molecular Medicine at the University of Edinburgh, Edinburgh Cancer Research UK Centre, Western General Hospital Campus, Crewe Road South Edinburgh EH4 2XR, UK – sequence: 7 givenname: Joan surname: Slight fullname: Slight, Joan organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK – sequence: 8 givenname: Anna surname: Thornburn fullname: Thornburn, Anna organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK – sequence: 9 givenname: Rachel surname: Berry fullname: Berry, Rachel organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK – sequence: 10 givenname: Sophie surname: McHaffie fullname: McHaffie, Sophie organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK – sequence: 11 givenname: Roland H. surname: Stimson fullname: Stimson, Roland H. organization: BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh – sequence: 12 givenname: Brian R. surname: Walker fullname: Walker, Brian R. organization: BHF Centre for Cardiovascular Science, Queen’s Medical Research Institute, University of Edinburgh – sequence: 13 givenname: Ramon Muñoz surname: Chapuli fullname: Chapuli, Ramon Muñoz organization: Department of Animal Biology, University of Málaga – sequence: 14 givenname: Andreas surname: Schedl fullname: Schedl, Andreas organization: IBV, INSERM U1091, Université de Nice Sophia-Antipolis, Parc Valrose, Centre de Biochimie 06100 Nice Cedex-2, France – sequence: 15 givenname: Nick surname: Hastie fullname: Hastie, Nick email: nicholas.hastie@igmm.ed.ac.uk organization: Medical Research Council Human Genetics Unit, Institute of Genetics and Molecular Medicine at the University of Edinburgh, Western General Hospital, Crewe Road Edinburgh EH4 2XU, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24609269$$D View this record in MEDLINE/PubMed https://hal.science/hal-00968725$$DView record in HAL |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 PMCID: PMC4060514 Author Contributions Conceived and designed the experiments: Y-YC, R Bandiera, A Serrels, OME, RMC, AS, and NH. Performed the experiments: Y-YC, R Bandiera, AS, OME, WQ, ML, JS, AT, RB, SM, RHS and RMC. Analyzed the data: Y-YC, R Bandiera, A Serrels, OME, RMC, and NH. Contributed reagents/materials/analysis tools: R Bandiera, A Serrels, ML, RHS, BRW, and RMC. Wrote the paper: Y-YC and NH. |
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| Snippet | Increased visceral adipose tissue has been associated with metabolic dysfunction but the origin of the progenitors that give rise to this tissue, and whether... Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells... : Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem and progenitor cells... Fuelled by the obesity epidemic, there is considerable interest in the developmental origins of white adipose tissue (WAT) and the stem/progenitor cells from... |
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| SubjectTerms | 631/136/142 631/136/334/1874 631/136/532/2074 Adipocytes Adipocytes - cytology Adipocytes - metabolism Adipose tissue Adipose Tissue, Brown - cytology Adipose Tissue, Brown - embryology Adipose Tissue, Brown - metabolism Adipose Tissue, White - cytology Adipose Tissue, White - embryology Adipose Tissue, White - metabolism Adipose tissues Animals Antineoplastic Agents, Hormonal - pharmacology Biology Body fat Cancer Research Cell Biology Cell Lineage - genetics Cell research Cellular control mechanisms Development Biology Developmental Biology Epidemics Gene Knock-In Techniques Genetics Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism letter Life Sciences Lipid metabolism Medical research Mesoderm - cytology Mesoderm - metabolism Metabolisme dels lípids Mice Obesity Physiological aspects Stem Cells Tamoxifen - pharmacology Teixit adipós WT1 Proteins - genetics WT1 Proteins - metabolism |
| Title | Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source |
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