DOI: 10.1242/jcs.113.17.2977. Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures

Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures

10.1242/jcs.113.17.2977

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

ABSTRACT In addition to their central role in triglyceride storage, fat cells are a primary depot of unesterified cholesterol (FC) in the body. In comparison, peripheral cells contain very little FC. This difference in adipocytes versus peripheral tissues is inconsistent with the current theory of cholesterol homeostasis. Attempting to resolve this discrepancy, we examined intracellular storage sites of FC in murine 3T3-F442A adipocytes. Using the cholesterol-binding antibiotic, filipin, in combination with high resolution fluorescence microscopy, intense fluorescent staining characteristically decorated the periphery of triglyceride droplets (TGD) as well as the plasma membrane (PM) of fat cells. Filipin-staining was not visible inside the lipid droplets. Purification of TGD by subcellular fractionation demonstrated that the rise in total FC content of adipocytes upon differentiation was attributable to an increase in TGD-FC, which contributed up to one third of the total cellular FC. The protein component of purified TGD from cultured adipocytes as well as from murine adipocytes obtained from fresh tissues contained the lumenal endoplasmic reticulum (ER) immunoglobulin binding protein (BiP) and the integral ER membrane protein calnexin. Efflux experiments using the extracellular FC acceptors β-cyclodextrin or apolipoprotein A-I demonstrated that TGD-associated FC was releasable from TGD. Whereas FC efflux from adipocytes was unaffected in the presence of brefeldin A or monensin, the secretion of a control protein, lipoprotein lipase, was effectively reduced. In summary, our findings identify the TGD surface layer as primary intracellular storage site for FC within adipocytes. We suggest that the structural role of ER-resident proteins in this adipocyte TGD envelope has been previously neglected. Our findings support the suggestion that an ER-like structure, albeit of modified lipid composition, constitutes the lipid droplets’ surface layer. Finally, the efflux process of FC from adipocytes upon extracellular stimulation with β-cyclodextrin provides evidence for an energy-dependent intracellular trafficking route between the TGD-FC pool and the PM-FC sites which is distinct from the secretory pathway of proteins.

Bibliography

Prattes, S., HÃ¶rl, G., Hammer, A., Blaschitz, A., Graier, W. F., Sattler, W., Zechner, R., & Steyrer, E. (2000). Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures. Journal of Cell Science, 113(17), 2977â2989.

Authors 8

Susanne Prattes (first)
Gerd Hörl (additional)
Astrid Hammer (additional)
Astrid Blaschitz (additional)
Wolfgang F. Graier (additional)
Wolfgang Sattler (additional)
Rudolf Zechner (additional)
Ernst Steyrer (additional)

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Dates

Type	When
Created	4 years, 4 months ago (April 23, 2021, 11:07 p.m.)
Deposited	1 year, 4 months ago (April 15, 2024, 7:36 p.m.)
Indexed	1 month, 2 weeks ago (July 14, 2025, 11:36 p.m.)
Issued	25 years ago (Sept. 1, 2000)
Published	25 years ago (Sept. 1, 2000)
Published Online	25 years ago (Sept. 1, 2000)
Published Print	25 years ago (Sept. 1, 2000)

Funders 0

None

BibTeX

@article{Prattes_2000, title={Intracellular distribution and mobilization of unesterified cholesterol in adipocytes: triglyceride droplets are surrounded by cholesterol-rich ER-like surface layer structures}, volume={113}, ISSN={1477-9137}, url={http://dx.doi.org/10.1242/jcs.113.17.2977}, DOI={10.1242/jcs.113.17.2977}, number={17}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Prattes, Susanne and Hörl, Gerd and Hammer, Astrid and Blaschitz, Astrid and Graier, Wolfgang F. and Sattler, Wolfgang and Zechner, Rudolf and Steyrer, Ernst}, year={2000}, month=sep, pages={2977–2989} }

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  "abstract": "<jats:title>ABSTRACT</jats:title>\n               <jats:p>In addition to their central role in triglyceride storage, fat cells are a primary depot of unesterified cholesterol (FC) in the body. In comparison, peripheral cells contain very little FC. This difference in adipocytes versus peripheral tissues is inconsistent with the current theory of cholesterol homeostasis. Attempting to resolve this discrepancy, we examined intracellular storage sites of FC in murine 3T3-F442A adipocytes. Using the cholesterol-binding antibiotic, filipin, in combination with high resolution fluorescence microscopy, intense fluorescent staining characteristically decorated the periphery of triglyceride droplets (TGD) as well as the plasma membrane (PM) of fat cells. Filipin-staining was not visible inside the lipid droplets. Purification of TGD by subcellular fractionation demonstrated that the rise in total FC content of adipocytes upon differentiation was attributable to an increase in TGD-FC, which contributed up to one third of the total cellular FC. The protein component of purified TGD from cultured adipocytes as well as from murine adipocytes obtained from fresh tissues contained the lumenal endoplasmic reticulum (ER) immunoglobulin binding protein (BiP) and the integral ER membrane protein calnexin. Efflux experiments using the extracellular FC acceptors \u03b2-cyclodextrin or apolipoprotein A-I demonstrated that TGD-associated FC was releasable from TGD. Whereas FC efflux from adipocytes was unaffected in the presence of brefeldin A or monensin, the secretion of a control protein, lipoprotein lipase, was effectively reduced.</jats:p>\n               <jats:p>In summary, our findings identify the TGD surface layer as primary intracellular storage site for FC within adipocytes. We suggest that the structural role of ER-resident proteins in this adipocyte TGD envelope has been previously neglected. Our findings support the suggestion that an ER-like structure, albeit of modified lipid composition, constitutes the lipid droplets\u2019 surface layer. Finally, the efflux process of FC from adipocytes upon extracellular stimulation with \u03b2-cyclodextrin provides evidence for an energy-dependent intracellular trafficking route between the TGD-FC pool and the PM-FC sites which is distinct from the secretory pathway of proteins.</jats:p>",
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