Lipid droplet biology and evolution illuminated by the characterization of a novel perilipin in teleost fish

Author:

Granneman James G1,Kimler Vickie A1,Zhang Huamei1,Ye Xiangqun1,Luo Xixia23,Postlethwait John H45,Thummel Ryan23ORCID

Affiliation:

1. Center for Integrative Metabolic and Endocrine Research, Wayne State University School of Medicine, Detroit, United States

2. Department of Anatomy and Cell Biology, Wayne State University School of Medicine, Detroit, United States

3. Department of Ophthalmology, Wayne State University School of Medicine, Detroit, United States

4. Institute of Neuroscience, University of Oregon, Eugene, United States

5. Department of Biology, University of Oregon, Eugene, 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.

Funder

National Institute of Diabetes and Digestive and Kidney Diseases

Wayne State University

NIH Office of the Director

National Eye Institute

Research to Prevent Blindness

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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