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Originally published In Press as doi:10.1074/jbc.M409340200 on August 27, 2004

J. Biol. Chem., Vol. 279, Issue 45, 46835-46842, November 5, 2004
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Proteomic Analysis of Proteins Associated with Lipid Droplets of Basal and Lipolytically Stimulated 3T3-L1 Adipocytes*

Dawn L. Brasaemle{ddagger}§, Georgia Dolios¶, Lawrence Shapiro||, and Rong Wang¶**

From the {ddagger}Department of Nutritional Sciences, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901, the ||Department of Biochemistry and Molecular Biophysics, Columbia University College of Physicians and Surgeons, and Department of Human Genetics, Mount Sinai School of Medicine, New York, New York 10029

Adipocytes hold the body's major energy reserve as triacylglycerols packaged in large lipid droplets. Perilipins, the most abundant proteins on these lipid droplets, play a critical role in facilitating both triacylglycerol storage and hydrolysis. The stimulation of lipolysis by {beta}-adrenergic agonists triggers rapid phosphorylation of perilipin and translocation of hormone-sensitive lipase to the surfaces of lipid droplets and more gradual fragmentation and dispersion of micro-lipid droplets. Because few lipid droplet-associated proteins have been identified in adipocytes, we isolated lipid droplets from basal and lipolytically stimulated 3T3-L1 adipocytes and identified the component proteins by mass spectrometry. Structural proteins identified in both preparations include perilipin, S3-12, vimentin, and TIP47; in contrast, adipophilin, caveolin-1, and tubulin selectively localized to droplets in lipolytically stimulated cells. Lipid metabolic enzymes identified in both preparations include hormone-sensitive lipase, lanosterol synthase, NAD(P)-dependent steroid dehydrogenase-like protein, acyl-CoA synthetase, long chain family member (ACSL) 1, and CGI-58. 17-{beta}-Hydroxysteroid dehydrogenase, type 7, was identified only in basal preparations, whereas ACSL3 and 4 and two short-chain reductase/dehydrogenases were identified on droplets from lipolytically stimulated cells. Additionally, both preparations contained FSP27, ribophorin I, EHD2, diaphorase I, and ancient ubiquitous protein. Basal preparations contained CGI-49, whereas lipid droplets from lipolytically stimulated cells contained several Rab GTPases and tumor protein D54. A close association of mitochondria with lipid droplets was suggested by the identification of pyruvate carboxylase, prohibitin, and a subunit of ATP synthase in the preparations. Thus, adipocyte lipid droplets contain specific structural proteins as well as lipid metabolic enzymes; the structural reorganization of lipid droplets in response to the hormonal stimulation of lipolysis is accompanied by increases in the relative mass of several proteins and the recruitment of additional proteins.

Received for publication, August 16, 2004 , and in revised form, August 26, 2004.

* This work was supported by National Institutes of Health Grants DK54797 (to D. L. B.) and CA88325 (to R. W.), an Established Investigator Award from the American Heart Association (to D. L. B.), and a Johnson & Johnson Discovery Award (to D. L. B.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ To whom correspondence may be addressed: Dept. of Nutritional Sciences, 96 Lipman Dr., Rutgers, The State University of New Jersey, New Brunswick, NJ 08901. Tel.: 732-932-6524; Fax: 732-932-6837; E-mail: Brasaemle{at}AESOP.Rutgers.edu. ** To whom correspondence may be addressed: Dept. of Human Genetics, Mount Sinai School of Medicine, 1425 Madison Ave., New York, NY 10029. Tel.: 212-659-6759; Fax: 212-828-5515; E-mail: Rong.Wang{at}mssm.edu.


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D. Binns, T. Januszewski, Y. Chen, J. Hill, V. S. Markin, Y. Zhao, C. Gilpin, K. D. Chapman, R. G.W. Anderson, and J. M. Goodman
An intimate collaboration between peroxisomes and lipid bodies
J. Cell Biol., June 5, 2006; 173(5): 719 - 731.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
M. Beller, D. Riedel, L. Jansch, G. Dieterich, J. Wehland, H. Jackle, and R. P. Kuhnlein
Characterization of the Drosophila Lipid Droplet Subproteome
Mol. Cell. Proteomics, June 1, 2006; 5(6): 1082 - 1094.
[Abstract] [Full Text] [PDF]

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 Mol. Biol. CellHome page
Y. Ohsaki, J. Cheng, A. Fujita, T. Tokumoto, and T. Fujimoto
Cytoplasmic Lipid Droplets Are Sites of Convergence of Proteasomal and Autophagic Degradation of Apolipoprotein B
Mol. Biol. Cell, June 1, 2006; 17(6): 2674 - 2683.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Yamaguchi, S. Matsushita, K. Motojima, F. Hirose, and T. Osumi
MLDP, a Novel PAT Family Protein Localized to Lipid Droplets and Enriched in the Heart, Is Regulated by Peroxisome Proliferator-activated Receptor {alpha}
J. Biol. Chem., May 19, 2006; 281(20): 14232 - 14240.
[Abstract] [Full Text] [PDF]

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 J BiochemHome page
S. Sato, M. Fukasawa, Y. Yamakawa, T. Natsume, T. Suzuki, I. Shoji, H. Aizaki, T. Miyamura, and M. Nishijima
Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein.
J. Biochem., May 1, 2006; 139(5): 921 - 930.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Marcinkiewicz, D. Gauthier, A. Garcia, and D. L. Brasaemle
The Phosphorylation of Serine 492 of Perilipin A Directs Lipid Droplet Fragmentation and Dispersion
J. Biol. Chem., April 28, 2006; 281(17): 11901 - 11909.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
H. D'Avila, R. C. N. Melo, G. G. Parreira, E. Werneck-Barroso, H. C. Castro-Faria-Neto, and P. T. Bozza
Mycobacterium bovis Bacillus Calmette-Guerin Induces TLR2-Mediated Formation of Lipid Bodies: Intracellular Domains for Eicosanoid Synthesis In Vivo.
J. Immunol., March 1, 2006; 176(5): 3087 - 3097.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
B. H.-J. Chang, L. Li, A. Paul, S. Taniguchi, V. Nannegari, W. C. Heird, and L. Chan
Protection against Fatty Liver but Normal Adipogenesis in Mice Lacking Adipose Differentiation-Related Protein
Mol. Cell. Biol., February 1, 2006; 26(3): 1063 - 1076.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
N. E. Wolins, B. K. Quaynor, J. R. Skinner, A. Tzekov, C. Park, K. Choi, and P. E. Bickel
OP9 mouse stromal cells rapidly differentiate into adipocytes: characterization of a useful new model of adipogenesis
J. Lipid Res., February 1, 2006; 47(2): 450 - 460.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. N. Gross, H. Miyoshi, T. Hosaka, H.-H. Zhang, E. C. Pino, S. Souza, M. Obin, A. S. Greenberg, and P. F. Pilch
Dynamics of Lipid Droplet-Associated Proteins during Hormonally Stimulated Lipolysis in Engineered Adipocytes: Stabilization and Lipid Droplet Binding of Adipocyte Differentiation-Related Protein/Adipophilin
Mol. Endocrinol., February 1, 2006; 20(2): 459 - 466.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H.-P. H. Moore, R. B. Silver, E. P. Mottillo, D. A. Bernlohr, and J. G. Granneman
Perilipin Targets a Novel Pool of Lipid Droplets for Lipolytic Attack by Hormone-sensitive Lipase
J. Biol. Chem., December 30, 2005; 280(52): 43109 - 43120.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Martin, K. Driessen, S. J. Nixon, M. Zerial, and R. G. Parton
Regulated Localization of Rab18 to Lipid Droplets: EFFECTS OF LIPOLYTIC STIMULATION AND INHIBITION OF LIPID DROPLET CATABOLISM
J. Biol. Chem., December 23, 2005; 280(51): 42325 - 42335.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
D. Langin, A. Dicker, G. Tavernier, J. Hoffstedt, A. Mairal, M. Ryden, E. Arner, A. Sicard, C. M. Jenkins, N. Viguerie, et al.
Adipocyte Lipases and Defect of Lipolysis in Human Obesity
Diabetes, November 1, 2005; 54(11): 3190 - 3197.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
M. Fortier, K. Soni, N. Laurin, S. P. Wang, P. Mauriege, F. R. Jirik, and G. A. Mitchell
Human hormone-sensitive lipase (HSL): expression in white fat corrects the white adipose phenotype of HSL-deficient mice
J. Lipid Res., September 1, 2005; 46(9): 1860 - 1867.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
P. Bostrom, M. Rutberg, J. Ericsson, P. Holmdahl, L. Andersson, M. A. Frohman, J. Boren, and S.-O. Olofsson
Cytosolic Lipid Droplets Increase in Size by Microtubule-Dependent Complex Formation
Arterioscler. Thromb. Vasc. Biol., September 1, 2005; 25(9): 1945 - 1951.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. T. Patel, J. L. Soulages, B. Hariharasundaram, and E. L. Arrese
Activation of the Lipid Droplet Controls the Rate of Lipolysis of Triglycerides in the Insect Fat Body
J. Biol. Chem., June 17, 2005; 280(24): 22624 - 22631.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. P. DeLany, Z. E. Floyd, S. Zvonic, A. Smith, A. Gravois, E. Reiners, X. Wu, G. Kilroy, M. Lefevre, and J. M. Gimble
Proteomic Analysis of Primary Cultures of Human Adipose-derived Stem Cells: Modulation by Adipogenesis
Mol. Cell. Proteomics, June 1, 2005; 4(6): 731 - 740.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
N. E. Wolins, B. K. Quaynor, J. R. Skinner, M. J. Schoenfish, A. Tzekov, and P. E. Bickel
S3-12, Adipophilin, and TIP47 Package Lipid in Adipocytes
J. Biol. Chem., May 13, 2005; 280(19): 19146 - 19155.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. ProteomicsHome page
J. E. Celis, J. M. A. Moreira, T. Cabezon, P. Gromov, E. Friis, F. Rank, and I. Gromova
Identification of Extracellular and Intracellular Signaling Components of the Mammary Adipose Tissue and Its Interstitial Fluid in High Risk Breast Cancer Patients: Toward Dissecting The Molecular Circuitry of Epithelial-Adipocyte Stromal Cell Interactions
Mol. Cell. Proteomics, April 1, 2005; 4(4): 492 - 522.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Ost, U. Ortegren, J. Gustavsson, F. H. Nystrom, and P. Stralfors
Triacylglycerol Is Synthesized in a Specific Subclass of Caveolae in Primary Adipocytes
J. Biol. Chem., January 7, 2005; 280(1): 5 - 8.
[Abstract] [Full Text] [PDF]


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