Perilipin-related protein regulates lipid metabolism in <i>C. elegans</i>

Chughtai, Ahmed Ali; Kaššák, Filip; Novotný, Jan Philipp; Krause, Michael; Saudek, Vladimı́r; Kostrouch, Zdeněk

doi:10.7287/peerj.preprints.904

Cited by 4 publications

(14 citation statements)

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“…2). GFP expression in VS20 control animals was more frequently concentrated in annular structures than in the crossed KV7 animals, which is compatible with the previously observed smaller basal LDs in PLIN-1-defficient animals (Chughtai et al 2015). However, when fasted for five hours at room temperature, a decrease in overall GFP fluorescence in plin-1 wt/wt animals is marked with few remaining enlarged annular structures, likely due to completed lipolysis.…”

Section: Plin-1 Is Critical For the Fasting-induced Lipolysis But Not For Atgl-1 Recruitment To Lipid Dropletssupporting

confidence: 89%

“…elegans. We have identified C. elegans locus W01A8.1 (previously annotated as mdt-28) as the sole PLIN gene orthologue in this nematode, henceforth labeled plin-1 (Chughtai et al 2015). Concurrently with our work, other groups have also independently identified this locus as a major LD protein influencing lipid metabolism (Na et al, 2015;Vrablik et al, 2015).…”

Section: Introductionsupporting

confidence: 62%

“…Several locus-modified and other transgenic lines were obtained from their respective authors, from the Caenorhabditis Genetic Center (CGC) of the University of Minnesota (Minneapolis, Minnesota, USA) and from the National BioResource Project (NBRP) (https://shigen.nig.ac.jp/c.elegans/top.xhtml), specifically: VS20 [atgl-1p::atgl-1::GFP + mec-7::RFP], tm2369 [hosl -/-] and RD204 [Ppie-1-lgg-1::gfp] ( Manil-Ségalen et al 2014). The strain KV1 [plin-1 -/-] was prepared previously by Cas9/CRISPR-induced gene deletion (Chughtai et al 2015).…”

Section: Strains Transgenic Lines and Genome Editingmentioning

confidence: 99%

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Supplemental Information 4: Raw Images Used in Object Analysis Represented in Fig. 4

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Neutral lipids and namely triacyl-glycerols (TAGs) are the prevalent excess energy storage molecules in all eukaryotic organisms. They are universally organized in active cytoplasmic organelles called lipid droplets (LDs) and their breakdown is performed and regulated in an evolutionarily conserved manner. In mammals, two distinct but inter-connected pathways are believed to mediate this catabolism: conventional cytoplasmic lipolysis with effector neutral lipases; and lipophagy, a specific kind of autophagy exploiting lysosomal acidic lipases. Central molecules in this regulation are LD-resident proteins, perilipins (PLINs). Our recent discovery of a sole PLIN orthologue in C. elegans offers a unique opportunity to study these regulatory pathways, provided that the interactive mechanisms are orthologous. To determine this, we employed classical genetics with genome editing tools and in vivo microscopy to provide three lines of evidence demonstrating the conserved role of the C. elegansperilipin. Firstly, we proved the common presence of a standard lipolytic apparatus on LDs. Next, we ascertained a functional connection between nematode PLIN-1 and the effector enzyme, hormone-sensitive lipase (HOSL-1). Finally, we identified lipophagy as a secondary lipolytic pathway, which is consistent with the mammalian model. Our data provide not only a proof of concept but also suggests interesting implications by questioning the physiological role of lipophagy in lipolysis.

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Section: Plin-1 Is Critical For the Fasting-induced Lipolysis But Not For Atgl-1 Recruitment To Lipid Dropletssupporting

confidence: 89%

Section: Introductionsupporting

confidence: 62%

Section: Strains Transgenic Lines and Genome Editingmentioning

confidence: 99%

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Supplemental Information 4: Raw Images Used in Object Analysis Represented in Fig. 4

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“…While fluorescently-tagged perilipin reporter proteins are used extensively in cell culture to visualize lipid droplets (for example (Chung et al, 2019;Granneman et al, 2017;Kaushik and Cuervo, 2015;Miura et al, 2002;Schulze et al, 2020;Targett-Adams et al, 2003)), lipid droplets in vivo have been historically studied in fixed tissues using immunohistochemistry (Frank et al, 2015;Lee et al, 2009), staining with lipid dyes (Oil red O, Sudan Black, LipidTox), or by electron microscopy (Chughtai et al, 2015;Marza et al, 2005;Zhang et al, 2010). Lipid droplets can also be labeled in live organisms with fluorescent lipophilic dyes such as BODIPY (Mather et al, 2019) & Nile red (Minchin and Rawls, 2017b), fed with fluorescently-tagged fatty acids (BODIPY & TopFluor) which are synthesized into stored fluorescent triglycerides or cholesterol esters (Ashrafi et al, 2003;Carten et al, 2011;Furlong et al, 1995;Quinlivan et al, 2017), or imaged in the absence of any label using CARS or SRS microscopy (Chien et al, 2012;Chughtai et al, 2015;Wang et al, 2011). However, expression of fluorescently-tagged lipid droplet associated proteins in vivo has been primarily limited to yeast (Gao et al, 2017), Drosophila (Bi et al, 2012;Gronke et al, 2005) and C. elegans (Chughtai et al, 2015;Xie et al, 2019;Zhang et al, 2010), although a transgenic zebrafish plin2-tdtomato line was very recently described (Lumaquin et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…Lipid droplets can also be labeled in live organisms with fluorescent lipophilic dyes such as BODIPY (Mather et al, 2019) & Nile red (Minchin and Rawls, 2017b), fed with fluorescently-tagged fatty acids (BODIPY & TopFluor) which are synthesized into stored fluorescent triglycerides or cholesterol esters (Ashrafi et al, 2003;Carten et al, 2011;Furlong et al, 1995;Quinlivan et al, 2017), or imaged in the absence of any label using CARS or SRS microscopy (Chien et al, 2012;Chughtai et al, 2015;Wang et al, 2011). However, expression of fluorescently-tagged lipid droplet associated proteins in vivo has been primarily limited to yeast (Gao et al, 2017), Drosophila (Bi et al, 2012;Gronke et al, 2005) and C. elegans (Chughtai et al, 2015;Xie et al, 2019;Zhang et al, 2010), although a transgenic zebrafish plin2-tdtomato line was very recently described (Lumaquin et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Imaging cytoplasmic lipid dropletsin vivowith fluorescent perilipin 2 and perilipin 3 knockin zebrafish

Wilson

Ekker

Farber

2021

Preprint

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Cytoplasmic lipid droplets are highly dynamic storage organelles; their rapid synthesis, expansion, and degradation, as well as their varied interactions with other organelles allow cells to maintain lipid homeostasis. While the molecular details of lipid droplet dynamics are currently a very active area of investigation, this work has been primarily performed in cultured cells and in vitro systems. By taking advantage of the powerful transgenic and in vivo imaging opportunities afforded by the zebrafish model system, we have built a suite of tools to allow lipid droplets to be studied in real-time from the subcellular to the whole organism level. Fluorescently-tagging the lipid droplet associated proteins, perilipin 2 and perilipin 3, in the endogenous loci, permits visualization of lipid droplets in the intestine, liver, lateral line and adipose tissue. Using these transgenic lines we have found that perilipin 3 is rapidly loaded on intestinal lipid droplets following a high fat meal and then largely replaced by perilipin 2 a few hours later. These powerful new tools will facilitate studies on the role of lipid droplets in different tissues and under different genetic and physiological manipulations.

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The Puzzling Conservation and Diversification of Lipid Droplets from Bacteria to Eukaryotes

Lupette

Maréchal

2020

Results and Problems in Cell Differentiation

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Membrane compartments are amongst the most fascinating markers of cell evolution from prokaryotes to eukaryotes, some being conserved and the others having emerged via a series of primary and secondary endosymbiosis events.Membrane compartments comprise the system limiting cells (one or two membranes in bacteria, a unique plasma membrane in eukaryotes) and a variety of internal vesicular, subspherical, tubular, or reticulated organelles. In eukaryotes, the internal membranes comprise on the one hand the general endomembrane system, a dynamic network including organelles like the endoplasmic reticulum, the Golgi apparatus, the nuclear envelope, etc. and also the plasma membrane, which are linked via direct lateral connectivity (e.g. between the endoplasmic reticulum and the nuclear outer envelope membrane) or indirectly via vesicular trafficking. On the other hand, semiautonomous organelles, i.e. mitochondria and chloroplasts, are disconnected from the endomembrane system and request vertical transmission following cell division.Membranes are organized as lipid bilayers in which proteins are embedded. The budding of some of these membranes, leading to the formation of the so-called lipid droplets (LDs) loaded with hydrophobic molecules, most notably triacylglycerol, is conserved in all clades. The evolution of eukaryotes is marked by the acquisition of mitochondria and simple plastids from Gram-positive bacteria by primary endosymbiosis events and the emergence of extremely complex plastids, collectively called secondary plastids, bounded by three to four membranes, following multiple and independent secondary endosymbiosis events. There is currently no consensus view of the evolution of LDs in the Tree of Life. Some features are conserved; others show Josselin Lupette and Eric Maréchal contributed equally with all other contributors.

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Perilipin-related protein regulates lipid metabolism in C. elegans

Cited by 4 publications

References 3 publications

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Imaging cytoplasmic lipid dropletsin vivowith fluorescent perilipin 2 and perilipin 3 knockin zebrafish

The Puzzling Conservation and Diversification of Lipid Droplets from Bacteria to Eukaryotes

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