Depot specific differences in the adipogenic potential of precursors are mediated by collagenous extracellular matrix and Flotillin 2 dependent signaling
Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remo...
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| Published in | Molecular metabolism (Germany) Vol. 5; no. 10; pp. 937 - 947 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Germany
Elsevier GmbH
01.10.2016
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2212-8778 2212-8778 |
| DOI | 10.1016/j.molmet.2016.07.008 |
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| Abstract | Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remodeling and a high degree of interaction between cells and ECM.
We studied decellularized primary adipose stromal cell derived ECM of different adipose depots and reseeded them with primary adipose precursors. We tested ECM effect on adipocyte differentiation and analyzed ECM composition using proteomic and immunohistochemical approaches to identify factors in the ECM influencing adipogenesis.
We show that the ECM of an adipose depot is the major determinant for the differentiation capacity of primary preadipocytes. Visceral adipose tissue stromal cells differentiate less than subcutaneous cells, which, in turn, are less adipogenic than BAT-derived cells. This effect is based on the ECM composition of the respective depot and not dependent on the precursor origin. Addition of vitamin C pronounces the pro-adipogenic effects of the ECM, indicating the importance of collagenous ECM in mediating the effect. Using a proteomic global and a targeted downstream analysis, we identify Flotillin 2 as a protein enriched in pro-adipogenic ECM, which is involved in orchestrating ECM to preadipocyte signaling.
We show that adipose tissue SVF secretes collagenous ECM, which directly modulates terminal differentiation of adipocyte precursors in a depot specific manner. These data demonstrate the importance of the tissue microenvironment in preadipocyte differentiation.
•Different adipose tissue depots have different differentiation capacities.•Differentiation of preadipocytes is enhanced by vitamin c through formation of collagenous ECM.•Collagenous ECM is the main determinant of adipose depot specific differences in adipogenic potential.•FLOT2 plays a role in mediating collagenous-ECM specific effects. |
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| AbstractList | Abstract Objective Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remodeling and a high degree of interaction between cells and ECM. Methods We studied decellularized primary adipose stromal cell derived ECM of different adipose depots and reseeded them with primary adipose precursors. We tested ECM effect on adipocyte differentiation and analyzed ECM composition using proteomic and immunohistochemical approaches to identify factors in the ECM influencing adipogenesis. Results We show that the ECM of an adipose depot is the major determinant for the differentiation capacity of primary preadipocytes. Visceral adipose tissue stromal cells differentiate less than subcutaneous cells, which, in turn, are less adipogenic than BAT-derived cells. This effect is based on the ECM composition of the respective depot and not dependent on the precursor origin. Addition of vitamin C pronounces the pro-adipogenic effects of the ECM, indicating the importance of collagenous ECM in mediating the effect. Using a proteomic global and a targeted downstream analysis, we identify Flotillin 2 as a protein enriched in pro-adipogenic ECM, which is involved in orchestrating ECM to preadipocyte signaling. Conclusions We show that adipose tissue SVF secretes collagenous ECM, which directly modulates terminal differentiation of adipocyte precursors in a depot specific manner. These data demonstrate the importance of the tissue microenvironment in preadipocyte differentiation. Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remodeling and a high degree of interaction between cells and ECM. We studied decellularized primary adipose stromal cell derived ECM of different adipose depots and reseeded them with primary adipose precursors. We tested ECM effect on adipocyte differentiation and analyzed ECM composition using proteomic and immunohistochemical approaches to identify factors in the ECM influencing adipogenesis. We show that the ECM of an adipose depot is the major determinant for the differentiation capacity of primary preadipocytes. Visceral adipose tissue stromal cells differentiate less than subcutaneous cells, which, in turn, are less adipogenic than BAT-derived cells. This effect is based on the ECM composition of the respective depot and not dependent on the precursor origin. Addition of vitamin C pronounces the pro-adipogenic effects of the ECM, indicating the importance of collagenous ECM in mediating the effect. Using a proteomic global and a targeted downstream analysis, we identify Flotillin 2 as a protein enriched in pro-adipogenic ECM, which is involved in orchestrating ECM to preadipocyte signaling. We show that adipose tissue SVF secretes collagenous ECM, which directly modulates terminal differentiation of adipocyte precursors in a depot specific manner. These data demonstrate the importance of the tissue microenvironment in preadipocyte differentiation. Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remodeling and a high degree of interaction between cells and ECM. We studied decellularized primary adipose stromal cell derived ECM of different adipose depots and reseeded them with primary adipose precursors. We tested ECM effect on adipocyte differentiation and analyzed ECM composition using proteomic and immunohistochemical approaches to identify factors in the ECM influencing adipogenesis. We show that the ECM of an adipose depot is the major determinant for the differentiation capacity of primary preadipocytes. Visceral adipose tissue stromal cells differentiate less than subcutaneous cells, which, in turn, are less adipogenic than BAT-derived cells. This effect is based on the ECM composition of the respective depot and not dependent on the precursor origin. Addition of vitamin C pronounces the pro-adipogenic effects of the ECM, indicating the importance of collagenous ECM in mediating the effect. Using a proteomic global and a targeted downstream analysis, we identify Flotillin 2 as a protein enriched in pro-adipogenic ECM, which is involved in orchestrating ECM to preadipocyte signaling. We show that adipose tissue SVF secretes collagenous ECM, which directly modulates terminal differentiation of adipocyte precursors in a depot specific manner. These data demonstrate the importance of the tissue microenvironment in preadipocyte differentiation. •Different adipose tissue depots have different differentiation capacities.•Differentiation of preadipocytes is enhanced by vitamin c through formation of collagenous ECM.•Collagenous ECM is the main determinant of adipose depot specific differences in adipogenic potential.•FLOT2 plays a role in mediating collagenous-ECM specific effects. • Different adipose tissue depots have different differentiation capacities. • Differentiation of preadipocytes is enhanced by vitamin c through formation of collagenous ECM. • Collagenous ECM is the main determinant of adipose depot specific differences in adipogenic potential. • FLOT2 plays a role in mediating collagenous-ECM specific effects. OBJECTIVEAdipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remodeling and a high degree of interaction between cells and ECM.METHODSWe studied decellularized primary adipose stromal cell derived ECM of different adipose depots and reseeded them with primary adipose precursors. We tested ECM effect on adipocyte differentiation and analyzed ECM composition using proteomic and immunohistochemical approaches to identify factors in the ECM influencing adipogenesis.RESULTSWe show that the ECM of an adipose depot is the major determinant for the differentiation capacity of primary preadipocytes. Visceral adipose tissue stromal cells differentiate less than subcutaneous cells, which, in turn, are less adipogenic than BAT-derived cells. This effect is based on the ECM composition of the respective depot and not dependent on the precursor origin. Addition of vitamin C pronounces the pro-adipogenic effects of the ECM, indicating the importance of collagenous ECM in mediating the effect. Using a proteomic global and a targeted downstream analysis, we identify Flotillin 2 as a protein enriched in pro-adipogenic ECM, which is involved in orchestrating ECM to preadipocyte signaling.CONCLUSIONSWe show that adipose tissue SVF secretes collagenous ECM, which directly modulates terminal differentiation of adipocyte precursors in a depot specific manner. These data demonstrate the importance of the tissue microenvironment in preadipocyte differentiation. Objective: Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots respond differently to an increased demand for lipid storage. Orchestrating cellular expansion in vivo requires extracellular matrix (ECM) remodeling and a high degree of interaction between cells and ECM. Methods: We studied decellularized primary adipose stromal cell derived ECM of different adipose depots and reseeded them with primary adipose precursors. We tested ECM effect on adipocyte differentiation and analyzed ECM composition using proteomic and immunohistochemical approaches to identify factors in the ECM influencing adipogenesis. Results: We show that the ECM of an adipose depot is the major determinant for the differentiation capacity of primary preadipocytes. Visceral adipose tissue stromal cells differentiate less than subcutaneous cells, which, in turn, are less adipogenic than BAT-derived cells. This effect is based on the ECM composition of the respective depot and not dependent on the precursor origin. Addition of vitamin C pronounces the pro-adipogenic effects of the ECM, indicating the importance of collagenous ECM in mediating the effect. Using a proteomic global and a targeted downstream analysis, we identify Flotillin 2 as a protein enriched in pro-adipogenic ECM, which is involved in orchestrating ECM to preadipocyte signaling. Conclusions: We show that adipose tissue SVF secretes collagenous ECM, which directly modulates terminal differentiation of adipocyte precursors in a depot specific manner. These data demonstrate the importance of the tissue microenvironment in preadipocyte differentiation. Keywords: Adipocyte precursors, Extracellular matrix, Collagen, Stem cell niche, Flotillin 2 |
| Author | Müller, Sebastian Moest, Hansjörg Moser, Caroline Wollscheid, Bernd Wolfrum, Christian Grandl, Gerald |
| AuthorAffiliation | 2 Institute of Molecular Systems Biology, ETH Zürich, Switzerland 1 Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland |
| AuthorAffiliation_xml | – name: 1 Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland – name: 2 Institute of Molecular Systems Biology, ETH Zürich, Switzerland |
| Author_xml | – sequence: 1 givenname: Gerald surname: Grandl fullname: Grandl, Gerald organization: Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland – sequence: 2 givenname: Sebastian surname: Müller fullname: Müller, Sebastian organization: Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland – sequence: 3 givenname: Hansjörg surname: Moest fullname: Moest, Hansjörg organization: Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland – sequence: 4 givenname: Caroline surname: Moser fullname: Moser, Caroline organization: Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland – sequence: 5 givenname: Bernd surname: Wollscheid fullname: Wollscheid, Bernd organization: Institute of Molecular Systems Biology, ETH Zürich, Switzerland – sequence: 6 givenname: Christian surname: Wolfrum fullname: Wolfrum, Christian email: christian-wolfrum@ethz.ch organization: Institute of Food, Nutrition and Health, ETH Zurich, Schwerzenbach, Switzerland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27689006$$D View this record in MEDLINE/PubMed |
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| Keywords | Stem cell niche Extracellular matrix Flotillin 2 Adipocyte precursors Collagen |
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| Snippet | Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose depots... Abstract Objective Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion.... OBJECTIVEAdipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different adipose... • Different adipose tissue depots have different differentiation capacities. • Differentiation of preadipocytes is enhanced by vitamin c through formation of... Objective: Adipose tissue shows a high degree of plasticity, and adipocyte hyperplasia is an important mechanism for adipose tissue expansion. Different... |
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| SubjectTerms | Adipocyte precursors Collagen Endocrinology & Metabolism Extracellular matrix Flotillin 2 Original Stem cell niche |
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| Title | Depot specific differences in the adipogenic potential of precursors are mediated by collagenous extracellular matrix and Flotillin 2 dependent signaling |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S2212877816301016 https://www.clinicalkey.es/playcontent/1-s2.0-S2212877816301016 https://www.ncbi.nlm.nih.gov/pubmed/27689006 https://www.proquest.com/docview/1825216800 https://pubmed.ncbi.nlm.nih.gov/PMC5034610 https://doaj.org/article/8a97ace8af1e47c4a71b5ca8ed9bc4a6 |
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