Lipid droplet biology and evolution illuminated by the characterization of a novel Perilipin in teleost fish
- Wayne State University School of Medicine, United States
- Oakland University, United States
- University of Oregon, United States
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.
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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.
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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Lipid droplet biology and evolution illuminated by the characterization of a novel Perilipin in teleost fish
eLife 6:e21771.
https://doi.org/10.7554/eLife.21771
