1. Cell Biology
  2. Evolutionary Biology
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Lipid droplet biology and evolution illuminated by the characterization of a novel Perilipin in teleost fish

  1. James G Granneman  Is a corresponding author
  2. Victoria A Kimler
  3. Huamei Zhang
  4. Xiangqun Ye
  5. Xixia Luo
  6. John H Postlethwait
  7. Ryan Thummel  Is a corresponding author
  1. Wayne State University School of Medicine, United States
  2. Oakland University, United States
  3. University of Oregon, United States
Research Article
  • Cited 25
  • Views 1,848
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Cite this article as: eLife 2017;6:e21771 doi: 10.7554/eLife.21771

Abstract

Perilipin (PLIN) proteins constitute an ancient family important in lipid droplet (LD) formation and triglyceride metabolism. We identified an additional PLIN clade (plin6) that is unique to teleosts and can be traced to the two whole genome duplications that occurred early in vertebrate evolution. Plin6 is highly expressed in skin xanthophores, which mediate red/yellow pigmentation and trafficking, but not in tissues associated with lipid metabolism. Biochemical and immunochemical analyses demonstrate that zebrafish Plin6 protein targets the surface of pigment-containing carotenoid droplets (CD). Protein kinase A (PKA) activation, which mediates CD dispersion in xanthophores, phosphorylates Plin6 on conserved residues. Knockout of plin6 in zebrafish severely impairs the ability of CD to concentrate carotenoids and prevents tight clustering of CD within carotenoid bodies. Ultrastructural and functional analyses indicate that LD and CD are homologous structures, and that Plin6 was functionalized early in vertebrate evolution for concentrating and trafficking pigment.

Article and author information

Author details

  1. James G Granneman

    Center for Integrative Metabolic and Endocrine Research, Wayne State University School of Medicine, Detroit, United States
    For correspondence
    jgranne@med.wayne.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Victoria A Kimler

    Eye Research Institute, Oakland University, Rochester, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Huamei Zhang

    Center for Integrative Metabolic and Endocrine Research, Wayne State University School of Medicine, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Xiangqun Ye

    Center for Integrative Metabolic and Endocrine Research, Wayne State University School of Medicine, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Xixia Luo

    Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. John H Postlethwait

    Institute of Neuroscience, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Ryan Thummel

    Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit, United States
    For correspondence
    rthummel@med.wayne.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0522-8704

Funding

National Institute of Diabetes and Digestive and Kidney Diseases (RO1DK076629,RO1DK62292)

  • James G Granneman

NIH Office of the Director (5R01OD011116)

  • John H Postlethwait

National Eye Institute (R21EY019401,P30EY04068)

  • Ryan Thummel

Research to Prevent Blindness (Unrestricted Grant)

  • Ryan Thummel

Wayne State University (Grants Plus,Start-up funds)

  • James G Granneman
  • Ryan Thummel

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

Ethics

Animal experimentation: All protocols used in this study were approved by the Institutional Animal Care and Use Committee at Wayne State University School of Medicine (approval numbers: A12-05-12 and A03-02-13) and were performed in strict compliance with Institutional and NIH Guidelines.

Reviewing Editor

  1. Christian Landry

Publication history

  1. Received: September 22, 2016
  2. Accepted: February 26, 2017
  3. Accepted Manuscript published: February 28, 2017 (version 1)
  4. Version of Record published: March 8, 2017 (version 2)

Copyright

© 2017, Granneman 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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