Dynamic control of adipose tissue development and adult tissue homeostasis by platelet-derived growth factor receptor alpha

  1. Sunhye Shin
  2. Yiyu Pang
  3. Jooman Park
  4. Lifeng Liu
  5. Brandon E Lukas
  6. Seung Hyeon Kim
  7. Ki-Wook Kim
  8. Pingwen Xu
  9. Daniel C Berry
  10. Yuwei Jiang  Is a corresponding author
  1. University of Illinois at Chicago, United States
  2. Cornell University, United States

Abstract

Adipocytes arise from distinct progenitor populations during development and adult, but little is known about how developmental progenitors differ from adult progenitors. Here, we investigate the role of platelet-derived growth factor receptor alpha (PDGFRα) in the divergent regulation of the two different adipose progenitor cells (APCs). Using in vivo adipose lineage tracking and deletion mouse models, we found that developmental PDGFRα+ cells are adipogenic and differentiated into mature adipocytes, and the deletion of Pdgfra in developmental adipose lineage disrupted white adipose tissue (WAT) formation. Interestingly, adult PDGFRα+ cells do not significantly contribute to adult adipogenesis, and deleting Pdgfra in adult adipose lineage did not affect WAT homeostasis. Mechanistically, embryonic APCs require PDGFRα for fate maintenance, and without PDGFRα, they underwent fate change from adipogenic to fibrotic lineage. Collectively, our findings indicate that PDGFRα+ cells and Pdgfra gene itself are differentially required for WAT development and adult WAT homeostasis.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Sunhye Shin

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5916-5390
  2. Yiyu Pang

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jooman Park

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Lifeng Liu

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Brandon E Lukas

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Seung Hyeon Kim

    Department of Pharmacology, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ki-Wook Kim

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Pingwen Xu

    Division of Endocrinology, Department of Medicine, University of Illinois at Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Daniel C Berry

    Division of Nutritional Sciences, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5200-1182
  10. Yuwei Jiang

    Department of Physiology and Biophysics, University of Illinois at Chicago, Chicago, United States
    For correspondence
    yuweij@uic.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5082-8012

Funding

NIDDK (K01 DK111771)

  • Yuwei Jiang

NIDDK DRTC (P30DK020595)

  • Yuwei Jiang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Valerie Horsley, Yale University, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#18-184) of the University of Illinois at Chicago. The protocol was reviewed in accordance with the Animal Care Policies and Procedures of the University of Illinois at Chicago and renewed on 10/16/2019. All experimental animals will be euthanized by carbon dioxide gas inhalation in accordance with the guidelines of the American Veterinary Medical Association and the policies of the UIC IACUC.

Version history

  1. Received: February 20, 2020
  2. Accepted: June 18, 2020
  3. Accepted Manuscript published: June 19, 2020 (version 1)
  4. Version of Record published: July 6, 2020 (version 2)

Copyright

© 2020, Shin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sunhye Shin
  2. Yiyu Pang
  3. Jooman Park
  4. Lifeng Liu
  5. Brandon E Lukas
  6. Seung Hyeon Kim
  7. Ki-Wook Kim
  8. Pingwen Xu
  9. Daniel C Berry
  10. Yuwei Jiang
(2020)
Dynamic control of adipose tissue development and adult tissue homeostasis by platelet-derived growth factor receptor alpha
eLife 9:e56189.
https://doi.org/10.7554/eLife.56189

Share this article

https://doi.org/10.7554/eLife.56189

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