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      Platelet-derived growth factor receptor beta is required for embryonic specification and confinement of the adult white adipose lineage

      research-article
      Author(s): 1 , 1 , 2 , 1 , 3 , ∗
      Publication date (Electronic):
      Journal: iScience
      Publisher: Elsevier
      Keywords: Molecular biology, Cell biology, Embryology

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          Summary

          White adipose tissue (WAT) development and adult homeostasis rely on distinct adipocyte progenitor cells (APCs). While adult APCs are defined early during embryogenesis and generate adipocytes after WAT organogenesis, the mechanisms underlying adult adipose lineage determination and preservation remain undefined. Here, we uncover a critical role for platelet-derived growth factor receptor beta (Pdgfrβ) in identifying the adult APC lineage. Without Pdgfrβ, APCs lose their adipogenic competency to incite fibrotic tissue replacement and inflammation. Through lineage tracing analysis, we reveal that the adult APC lineage is lost and develops into macrophages when Pdgfrβ is deleted embryonically. Moreover, to maintain the APC lineage, Pdgfrβ activation stimulates p38/MAPK phosphorylation to promote APC proliferation and maintains the APC state by phosphorylating peroxisome proliferator activated receptor gamma (Pparγ) at serine 112. Together, our findings identify a role for Pdgfrβ acting as a rheostat for adult adipose lineage confinement to prevent unintended lineage switches.

          Graphical abstract

          Highlights

          • •

            Pdgfrβ deletion results in adult-onset white adipose tissue dysfunction

          • •

            Pdgfrβ is required for adult adipose lineage confinement and adult adipogenesis

          • •

            Embryonic deletion of Pdgfrβ results in adipocyte-to-macrophage lineage conversion

          • •

            Pdgfrβ signaling upholds the APC state but halts adipogenesis by Pparγ Ser112

          Abstract

          Molecular biology; Cell biology; Embryology

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          Most cited references61

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          A robust and high-throughput Cre reporting and characterization system for the whole mouse brain

          Linda Madisen, Theresa Zwingman, Susan M. Sunkin … (2009)
          The Cre/lox system is widely used in mice to achieve cell-type-specific gene expression. However, a strong and universal responding system to express genes under Cre control is still lacking. We have generated a set of Cre reporter mice with strong, ubiquitous expression of fluorescent proteins of different spectra. The robust native fluorescence of these reporters enables direct visualization of fine dendritic structures and axonal projections of the labeled neurons, which is useful in mapping neuronal circuitry, imaging and tracking specific cell populations in vivo. Using these reporters and a high-throughput in situ hybridization platform, we are systematically profiling Cre-directed gene expression throughout the mouse brain in a number of Cre-driver lines, including novel Cre lines targeting different cell types in the cortex. Our expression data are displayed in a public online database to help researchers assess the utility of various Cre-driver lines for cell-type-specific genetic manipulation.
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            Macrophage biology in development, homeostasis and disease.

            Thomas A Wynn, Ajay Chawla, Jeffrey W Pollard (2013)
            Macrophages, the most plastic cells of the haematopoietic system, are found in all tissues and show great functional diversity. They have roles in development, homeostasis, tissue repair and immunity. Although tissue macrophages are anatomically distinct from one another, and have different transcriptional profiles and functional capabilities, they are all required for the maintenance of homeostasis. However, these reparative and homeostatic functions can be subverted by chronic insults, resulting in a causal association of macrophages with disease states. In this Review, we discuss how macrophages regulate normal physiology and development, and provide several examples of their pathophysiological roles in disease. We define the 'hallmarks' of macrophages according to the states that they adopt during the performance of their various roles, taking into account new insights into the diversity of their lineages, identities and regulation. It is essential to understand this diversity because macrophages have emerged as important therapeutic targets in many human diseases.
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              Adapting to obesity with adipose tissue inflammation

              Alan Saltiel, Shannon Reilly (2017)
              Adipose tissue inflammation is an adaptive response to overnutrition in the early stages of obesity, but later becomes maladaptive. Here, Reilly and Saltiel review the cellular and molecular mechanisms of obesity-induced inflammation in adipose tissue and discuss potential therapeutic approaches.
              Article 0 comments Cited 486 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Daniel C. Berry
                Journal
                Journal ID (nlm-ta): iScience
                Journal ID (iso-abbrev): iScience
                Title: iScience
                Publisher: Elsevier
                ISSN (Electronic): 2589-0042
                Publication date PMC-release: 12 December 2023
                Publication date Collection: 19 January 2024
                Publication date (Electronic): 12 December 2023
                Volume: 27
                Issue: 1
                Electronic Location Identifier: 108682
                Affiliations
                [1 ]Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, USA
                [2 ]Department of Physiology and Biophysics, University of Illinois College of Medicine at Chicago, Chicago, IL 60612, USA
                Author notes
                [∗ ]Corresponding author dcb37@ 123456cornell.edu
                [3]

                Lead contact

                Article
                Publisher Item ID: S2589-0042(23)02759-1 Publisher ID: 108682
                DOI: 10.1016/j.isci.2023.108682
                PMC ID: 10792241
                PubMed ID: 38235323
                SO-VID: c0f8e1f0-81b7-4ba5-b354-54fca54d164f
                Copyright © © 2023 The Author(s)
                License:

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                Date received : 6 September 2023
                Date revision received : 31 October 2023
                Date accepted : 5 December 2023
                Categories
                Subject: Article

                Keywords: molecular biology,cell biology,embryology
                Data availability:
                Keywords: molecular biology, cell biology, embryology

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