Abstract
Despite the critical roles of intracellular lipid droplets (LDs) in lipid storage and metabolism, little is known about the molecular mechanisms of their functions. Several protein components associated with the surface of LDs have been identified. A major one is perilipin in adipocytes and steroidogenic cells, whereas ADRP in most other cell types. They are loosely grouped as a small protein family sharing a common N-terminal motif, called the PAT domain. Perilipin regulates the breakdown of triacylglycerol in LDs via its phosphorylation. ADRP is characterized as a fatty acid binding protein and involved in lipid uptake and LD formation. For examining the functions of perilipin and ADRP at the molecular level, we performed yeast two-hybrid screening in this study, to find their functional partners. We identified CGI-58, a product of the causal gene of Chanarin-Dorfman syndrome (CDS), as an interactor for both perilipin and ADRP. Specific interaction between CGI-58 and perilipin was confirmed in a GST-pulldown assay and supported by fluorescence microscopic analyses. We further demonstrated that CGI-58 is principally located at the surface of LDs in 3T3-L1 cells, together with perilipin, and its expression is upregulated upon stimulation for adipocyte differentiation. Other than CGI-58, we also identified in yeast two-hybrid screening HSP86 and D52 tumor proteins as binding partners of perilipin, and IRG-47 of ADRP. These factors might be cooperated with perilipin and ADRP, and hence involved in membrane dynamics of LDs as well as the regulation of lipolysis on the surface of LDs.
MeSH Terms
1-Acylglycerol-3-Phosphate O-Acyltransferase
3T3-L1 Cells
Adipocytes/physiology
Animals
Carrier Proteins
Cell Differentiation
Esterases/metabolism
Fluorescent Antibody Technique
HSP90 Heat-Shock Proteins/metabolism
Lipid Metabolism
Lipolysis
Membrane Proteins/biosynthesis,metabolism
Mice
Neoplasm Proteins/metabolism
Perilipin-1
Perilipin-2
Phosphoproteins/biosynthesis,metabolism
Rats
Two-Hybrid System Techniques
Yeasts/genetics
Chemicals
Carrier Proteins
HSP90 Heat-Shock Proteins
Hspca protein, mouse
Membrane Proteins
Neoplasm Proteins
Perilipin-1
Perilipin-2
Phosphoproteins
Plin2 protein, mouse
Plin2 protein, rat
1-Acylglycerol-3-Phosphate O-Acyltransferase
Abhd5 protein, mouse
Esterases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yamaguchi Tomohiro
Graduate School of Life Science, Himeji Institute of Technology, University of Hyogo, Kamigori, Hyogo 678-1297, Japan.
Omatsu Naoto
Omukae Asami
Osumi Takashi
References (23)
23 references, click to expand
-
Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome.
Am J Hum Genet. 2001 Nov;69(5):1002-12
PMID: 11590543
-
Hsp90: a specialized but essential protein-folding tool.
J Cell Biol. 2001 Jul 23;154(2):267-73
PMID: 11470816
-
Hsp90: chaperoning signal transduction.
J Cell Physiol. 2001 Sep;188(3):281-90
PMID: 11473354
-
The IRG-47 gene is IFN-gamma induced in B cells and encodes a protein with GTP-binding motifs.
J Immunol. 1992 May 15;148(10):3275-81
PMID: 1578148
-
Isolation and characterization of a full-length cDNA coding for an adipose differentiation-related protein.
Proc Natl Acad Sci U S A. 1992 Sep 1;89(17 ):7856-60
PMID: 1518805
-
CGI-58 interacts with perilipin and is localized to lipid droplets. Possible involvement of CGI-58 mislocalization in Chanarin-Dorfman syndrome.
J Biol Chem. 2004 Jul 16;279(29):30490-7
PMID: 15136565
-
Growth hormone has dual stage-specific effects on the differentiation of 3T3-L1 preadipocytes.
J Biochem. 2002 Dec;132(6):881-9
PMID: 12473190
-
Identification of homo- and heteromeric interactions between members of the breast carcinoma-associated D52 protein family using the yeast two-hybrid system.
Oncogene. 1998 Feb 19;16(7):873-81
PMID: 9484778
-
Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein.
J Lipid Res. 1997 Nov;38(11):2249-63
PMID: 9392423
-
Identification of MAL2, a novel member of the mal proteolipid family, though interactions with TPD52-like proteins in the yeast two-hybrid system.
Genomics. 2001 Aug;76(1-3):81-8
PMID: 11549320
-
Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty acid uptake.
J Biol Chem. 1999 Jun 11;274(24):16825-30
PMID: 10358026
-
A promoter ISRE and dual 5' YY1 motifs control IFN-gamma induction of the IRG-47 G-protein gene.
Gene. 1996 Nov 14;179(2):237-44
PMID: 8972906
-
Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium.
J Biol Chem. 2002 Aug 30;277(35):32253-7
PMID: 12077142
-
Formation of peroxisomes from peroxisomal ghosts in a peroxisome-deficient mammalian cell mutant upon complementation by protein microinjection.
J Biol Chem. 1999 Dec 10;274(50):35293-6
PMID: 10585391
-
Association of stomatin with lipid bodies.
J Biol Chem. 2004 May 28;279(22):23699-709
PMID: 15024010
-
Definition of the tumor protein D52 (TPD52) gene family through cloning of D52 homologues in human (hD53) and mouse (mD52).
Genomics. 1996 Aug 1;35(3):523-32
PMID: 8812487
-
Chinese hamster ovary K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic.
J Biol Chem. 2004 Jan 30;279(5):3787-92
PMID: 14597625
-
Perilipin A is essential for the translocation of hormone-sensitive lipase during lipolytic activation.
J Cell Biol. 2003 Jun 23;161(6):1093-103
PMID: 12810697
-
Isolation of cDNAs for perilipins A and B: sequence and expression of lipid droplet-associated proteins of adipocytes.
Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):12035-9
PMID: 7505452
-
The biogenesis and functions of lipid bodies in animals, plants and microorganisms.
Prog Lipid Res. 2001 Sep;40(5):325-438
PMID: 11470496
-
A screening method to identify genes commonly overexpressed in carcinomas and the identification of a novel complementary DNA sequence.
Cancer Res. 1995 Jul 1;55(13):2896-903
PMID: 7796418
-
Inactivation of LRG-47 and IRG-47 reveals a family of interferon gamma-inducible genes with essential, pathogen-specific roles in resistance to infection.
J Exp Med. 2001 Jul 16;194(2):181-8
PMID: 11457893
-
Lipase-selective functional domains of perilipin A differentially regulate constitutive and protein kinase A-stimulated lipolysis.
J Biol Chem. 2003 Dec 19;278(51):51535-42
PMID: 14527948