Home LiteratureArticle Details
PMID: 19160396 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

A role for lipid droplets in inter-membrane lipid traffic.

Proteomics ·Vol. 9 ·No. 4 ·2009-02-00 ·Pages 914-21

Zehmer JK, Huang Y, Peng G, Pu J, Anderson RG, Liu P

Abstract

All cells have the capacity to accumulate neutral lipids and package them into lipid droplets. Recent proteomic analyses indicate that lipid droplets are not simple lipid storage depots, but rather complex organelles that have multiple cellular functions. One of these proposed functions is to distribute neutral lipids as well as phospholipids to various membrane-bound organelles within the cell. Here, we summarize the lipid droplet-associated membrane-trafficking proteins and review the evidence that lipid droplets interact with endoplasmic reticulum, endosomes, peroxisomes, and mitochondria. Based on this evidence, we present a model for how lipid droplets can distribute lipids to specific membrane compartments.

MeSH Terms
Animals Humans Lipids/physiology Membrane Proteins/metabolism Organelles/metabolism Phospholipids/metabolism Protein Transport/physiology Proteomics/methods Vesicular Transport Proteins/metabolism
Chemicals
Lipids Membrane Proteins Phospholipids Vesicular Transport Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zehmer John K
Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX, USA.
Huang Youguo
Peng Gong
Pu Jing
Anderson Richard G W
Liu Pingsheng
References (66)
66 references, click to expand
  1. Peroxisomes and intracellular cholesterol trafficking in adult rat Leydig cells following Luteinizing hormone stimulation.
    Tissue Cell. 2000 Feb;32(1):102-6 PMID: 10798324
  2. Cytosolic lipid droplets increase in size by microtubule-dependent complex formation.
    Arterioscler Thromb Vasc Biol. 2005 Sep;25(9):1945-51 PMID: 16051877
  3. SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity.
    Nat Cell Biol. 2007 Nov;9(11):1286-93 PMID: 17922004
  4. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation.
    Diabetes. 2004 May;53(5):1261-70 PMID: 15111495
  5. ADRP is dissociated from lipid droplets by ARF1-dependent mechanism.
    Biochem Biophys Res Commun. 2004 Sep 24;322(3):957-65 PMID: 15336557
  6. Proteomic analysis of proteins associated with lipid droplets of basal and lipolytically stimulated 3T3-L1 adipocytes.
    J Biol Chem. 2004 Nov 5;279(45):46835-42 PMID: 15337753
  7. Dynein-mediated cargo transport in vivo. A switch controls travel distance.
    J Cell Biol. 2000 Mar 6;148(5):945-56 PMID: 10704445
  8. The lipid-droplet proteome reveals that droplets are a protein-storage depot.
    Curr Biol. 2006 Sep 19;16(18):1783-95 PMID: 16979555
  9. Interorganelle transport of aminoglycerophospholipids.
    Biochim Biophys Acta. 2000 Jun 26;1486(1):97-107 PMID: 10856716
  10. Tubulo-reticular clusters of peroxisomes in living COS-7 cells: dynamic behavior and association with lipid droplets.
    J Histochem Cytochem. 2001 Nov;49(11):1421-29 PMID: 11668195
  11. Drosophila Perilipin/ADRP homologue Lsd2 regulates lipid metabolism.
    Mech Dev. 2003 Sep;120(9):1071-81 PMID: 14550535
  12. Intracellular lipid particles of eukaryotic cells.
    Biochim Biophys Acta. 2000 Sep 18;1469(2):101-20 PMID: 10998572
  13. Proteomic profiling of lipid droplet proteins in hepatoma cell lines expressing hepatitis C virus core protein.
    J Biochem. 2006 May;139(5):921-30 PMID: 16751600
  14. Network distribution of mitochondria and lipid droplets in human muscle fibres.
    Histochem Cell Biol. 2008 Jan;129(1):65-72 PMID: 17938948
  15. Proteomics reveal a link between the endoplasmic reticulum and lipid secretory mechanisms in mammary epithelial cells.
    Electrophoresis. 2000 Oct;21(16):3470-82 PMID: 11079566
  16. A class of amphipathic proteins associated with lipid storage bodies in plants. Possible similarities with animal serum apolipoproteins.
    Biochim Biophys Acta. 1991 Jan 17;1088(1):86-94 PMID: 1989697
  17. Morphometric evaluation of lipid droplet associations with secretory vesicles, mitochondria and other components in the lactating cell.
    Cell Tissue Res. 1984;236(2):471-5 PMID: 6733773
  18. Lipidomics reveals that adiposomes store ether lipids and mediate phospholipid traffic.
    J Lipid Res. 2007 Apr;48(4):837-47 PMID: 17210984
  19. Identification and characterization of associated with lipid droplet protein 1: A novel membrane-associated protein that resides on hepatic lipid droplets.
    Traffic. 2006 Sep;7(9):1254-69 PMID: 17004324
  20. Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots.
    J Bacteriol. 2005 Jun;187(11):3607-19 PMID: 15901682
  21. Multiple lipid transport pathways to the plasma membrane in yeast.
    Biochim Biophys Acta. 2005 Feb 21;1687(1-3):130-40 PMID: 15708361
  22. A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids.
    Eur J Biochem. 2001 Apr;268(8):2351-61 PMID: 11298754
  23. Association of stomatin with lipid bodies.
    J Biol Chem. 2004 May 28;279(22):23699-709 PMID: 15024010
  24. Quantitative proteomics analysis of the secretory pathway.
    Cell. 2006 Dec 15;127(6):1265-81 PMID: 17174899
  25. Functional genomic screen reveals genes involved in lipid-droplet formation and utilization.
    Nature. 2008 May 29;453(7195):657-61 PMID: 18408709
  26. 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
  27. Dynamic activity of lipid droplets: protein phosphorylation and GTP-mediated protein translocation.
    J Proteome Res. 2007 Aug;6(8):3256-65 PMID: 17608402
  28. Movement of lipolytic products to mitochondria in brown adipose tissue of young rats: an electron microscope study.
    J Lipid Res. 1983 Mar;24(3):229-44 PMID: 6842081
  29. A clean, more efficient method for in-solution digestion of protein mixtures without detergent or urea.
    J Proteome Res. 2006 Dec;5(12):3446-52 PMID: 17137347
  30. Lipid droplets: proteins floating on a pool of fat.
    Curr Biol. 2001 Jun 5;11(11):R446-9 PMID: 11516669
  31. Protein and lipid composition analysis of oil bodies from two Brassica napus cultivars.
    Proteomics. 2006 Aug;6(16):4586-98 PMID: 16847873
  32. Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics.
    Cell. 1998 Feb 20;92(4):547-57 PMID: 9491895
  33. Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells.
    J Cell Biol. 1983 Oct;97(4):1156-68 PMID: 6684660
  34. Lipid droplets: a classic organelle with new outfits.
    Histochem Cell Biol. 2008 Aug;130(2):263-79 PMID: 18546013
  35. Direct observation of rapid internalization and intracellular transport of sterol by macrophage foam cells.
    Traffic. 2005 May;6(5):396-412 PMID: 15813750
  36. Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7.
    Biochim Biophys Acta. 2004 Feb 2;1644(1):47-59 PMID: 14741744
  37. A proposed model of fat packaging by exchangeable lipid droplet proteins.
    FEBS Lett. 2006 Oct 9;580(23):5484-91 PMID: 16962104
  38. Live cell analysis and targeting of the lipid droplet-binding adipocyte differentiation-related protein.
    J Biol Chem. 2003 May 2;278(18):15998-6007 PMID: 12591929
  39. Lipid droplets: a unified view of a dynamic organelle.
    Nat Rev Mol Cell Biol. 2006 May;7(5):373-8 PMID: 16550215
  40. Visualization of double-stranded RNA in cells supporting hepatitis C virus RNA replication.
    J Virol. 2008 Mar;82(5):2182-95 PMID: 18094154
  41. Rab-regulated interaction of early endosomes with lipid droplets.
    Biochim Biophys Acta. 2007 Jun;1773(6):784-93 PMID: 17395284
  42. Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane.
    J Cell Sci. 2005 Jun 15;118(Pt 12):2601-11 PMID: 15914536
  43. [Ultrastructural study of liver cells from rooks living in ecologically unfavorable areas].
    Izv Akad Nauk Ser Biol. 2006 Mar-Apr;(2):133-41 PMID: 16634429
  44. PLD1 and ERK2 regulate cytosolic lipid droplet formation.
    J Cell Sci. 2006 Jun 1;119(Pt 11):2246-57 PMID: 16723731
  45. Molecular anatomy of a trafficking organelle.
    Cell. 2006 Nov 17;127(4):831-46 PMID: 17110340
  46. The murine perilipin gene: the lipid droplet-associated perilipins derive from tissue-specific, mRNA splice variants and define a gene family of ancient origin.
    Mamm Genome. 2001 Sep;12(9):741-9 PMID: 11641724
  47. High density lipoprotein-mediated cholesterol uptake and targeting to lipid droplets in intact L-cell fibroblasts. A single- and multiphoton fluorescence approach.
    J Biol Chem. 2000 Apr 28;275(17):12769-80 PMID: 10777574
  48. An intimate collaboration between peroxisomes and lipid bodies.
    J Cell Biol. 2006 Jun 5;173(5):719-31 PMID: 16735577
  49. The lipodystrophy protein seipin is found at endoplasmic reticulum lipid droplet junctions and is important for droplet morphology.
    Proc Natl Acad Sci U S A. 2007 Dec 26;104(52):20890-5 PMID: 18093937
  50. Identification and characterization of major lipid particle proteins of the yeast Saccharomyces cerevisiae.
    J Bacteriol. 1999 Oct;181(20):6441-8 PMID: 10515935
  51. Fluorescence resonance energy transfer analysis of mitochondrial:lipid association in the porcine oocyte.
    Reproduction. 2006 Dec;132(6):829-37 PMID: 17127743
  52. The surface of lipid droplets is a phospholipid monolayer with a unique Fatty Acid composition.
    J Biol Chem. 2002 Nov 15;277(46):44507-12 PMID: 12221100
  53. Regulated localization of Rab18 to lipid droplets: effects of lipolytic stimulation and inhibition of lipid droplet catabolism.
    J Biol Chem. 2005 Dec 23;280(51):42325-35 PMID: 16207721
  54. Regulation of lipid-droplet transport by the perilipin homolog LSD2.
    Curr Biol. 2005 Jul 26;15(14):1266-75 PMID: 16051169
  55. Organelle relationships in cultured 3T3-L1 preadipocytes.
    J Cell Biol. 1980 Oct;87(1):180-96 PMID: 7191426
  56. Interaction of high density lipoproteins with cholesteryl ester-laden macrophages: biochemical and morphological characterization of cell surface receptor binding, endocytosis and resecretion of high density lipoproteins by macrophages.
    EMBO J. 1985 Mar;4(3):613-22 PMID: 2988931
  57. Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity.
    Am J Physiol Regul Integr Comp Physiol. 2007 Mar;292(3):R1271-8 PMID: 17095651
  58. Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies.
    FASEB J. 2007 Jan;21(1):167-78 PMID: 17135363
  59. The biogenesis and functions of lipid bodies in animals, plants and microorganisms.
    Prog Lipid Res. 2001 Sep;40(5):325-438 PMID: 11470496
  60. Many roads lead to the lipid droplet.
    Cell Metab. 2008 Jun;7(6):472-3 PMID: 18522827
  61. Perilipins, ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells.
    Semin Cell Dev Biol. 1999 Feb;10(1):51-8 PMID: 10355028
  62. Arf1-dependent PLD1 is localized to oleic acid-induced lipid droplets in NIH3T3 cells.
    Biochem Biophys Res Commun. 2005 Sep 16;335(1):117-23 PMID: 16054594
  63. Leukocyte lipid bodies: inflammation-related organelles are rapidly detected by wet scanning electron microscopy.
    J Lipid Res. 2006 Nov;47(11):2589-94 PMID: 16940552
  64. Characterization of the Drosophila lipid droplet subproteome.
    Mol Cell Proteomics. 2006 Jun;5(6):1082-94 PMID: 16543254
  65. Lipid droplets in lipogenesis and lipolysis.
    Endocrinology. 2008 Mar;149(3):942-9 PMID: 18202123
  66. A phospholipase D-dependent process forms lipid droplets containing caveolin, adipocyte differentiation-related protein, and vimentin in a cell-free system.
    J Biol Chem. 2003 Jul 18;278(29):27293-300 PMID: 12730229
Article Info
Journal
Proteomics
Abbr.
Proteomics
ISSN
1615-9861
Published
2009-02-00
Pages
914-21
Language
English
Region
Germany
NLM ID
101092707
PMCID
PMC2676673
Subset
IM
Grants
NIGMS NIH HHS · P20 GM103476 · United States
NIGMS NIH HHS · GM 52016 · United States
NIGMS NIH HHS · R01 GM052016-14 · United States
NHLBI NIH HHS · HL 20948 · United States
NIGMS NIH HHS · R01 GM052016 · United States
NHLBI NIH HHS · P01 HL020948 · United States
NIGMS NIH HHS · GM 70117 · United States
NHLBI NIH HHS · P01 HL020948-260020 · United States
NIGMS NIH HHS · F32 GM070117 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]