Lipid droplet biology and evolution illuminated by the characterization of a novel perilipin in teleost fish
Open accessAbstract
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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The yellow-orange color of xanthophores can depend on pteridine pigments, carotenoid pigments, or both.
“The yellow-orange color of xanthophores can depend on pteridine pigments, carotenoid pigments, or both”
From Thyroid hormone regulates distinct paths to maturation in pigment cell lineages (2019) · cites this paper as Granneman et al., 2017
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A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751 · see citing works
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MESSENGER, J. B. (2001) · Biological Reviews · doi:10.1017/s1464793101005772 · Cited by 414 · cited 1× · see citing works
“Carotenoid-based pigmentation is found in both vertebrates (Cote et al., 2010; Walsh et al., 2012) and invertebrates (Yang et al., 1999; Messenger, 2001), and substantial evidence indicates that CD and LD are homologous structures with a shared evolutionary history.”
BackgroundOrban, T., Palczewska, G., & Palczewski, K. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.195198 · Cited by 89 · cited 1× · see citing works
“Mammalian LD that concentrate carotenoids (specifically retinylesters) contain PLIN proteins (Higashi and Senoo, 2003; Straub et al., 2008; Orban et al., 2011), and we show that zebrafish Plin6 and mouse PLIN1 target the same LD structures in mammalian cells.”
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Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
Saunders, L. M., Mishra, A. K., Aman, A. J., Lewis, V. M., Toomey, M. B., Packer, J. S., Qiu, X., McFaline-Figueroa, J. L., Corbo, J. C., Trapnell, C., et al. (2019) · eLife · doi:10.7554/elife.45181 · Cited by 170 · see citing works
- Authors
- Granneman, J. G., Kimler, V. A., Zhang, H., Ye, X., Luo, X., Postlethwait, J. H., & Thummel, R.
- Affiliations
- Wayne State University (US)
- University of Oregon (US)
- Corresponding author
- Granneman, James G
- Thummel, Ryan
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2017-02-28
- Volume
- 6
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5342826
- OpenAlex
- W2592576198
- Cited by
- 77
- References
- 3
- Citations by year
- 2026: 12 · 2025: 8 · 2024: 13 · 2023: 10 · 2022: 3 · 2021: 13 · 2020: 10 · 2019: 4 · 2018: 3 · 2017: 1
- FWCI
- 2.41
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (RO1DK076629, RO1DK62292)
- Wayne State University (Grants Plus,Start-up funds)
- NIH Office of the Director (5R01OD011116)
- National Eye Institute (R21EY019401, P30EY04068)
- Research to Prevent Blindness (Unrestricted Grant)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Lipid metabolism and disorders
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Aquaculture Nutrition and Growth
- Keywords
- perilipin, lipid droplets, xanthophores, teleost evolution, whole-genome duplication, protein kinase A phosphorylation, zebrafish, carotenoid content
- MeSH terms
- Perilipin-1, Animals, Carotenoids, Phosphorylation, Protein Processing, Post-Translational, Zebrafish, Cyclic AMP-Dependent Protein Kinases, Gene Expression Profiling, Gene Knockout Techniques, Lipid Droplets
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