Lipid droplet associated proteins: An emerging role in atherogenesis

Histology and Histopathology

Volumn 26, Issue 5, 2011, Pages 631-642

  Buers, Insa ^a   Hofnagel, Oliver ^a   Ruebel, Anneke ^a   Severs, Nicholas J ^b   Robenek, Horst ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Atherosclerosis; Lipid droplets; PAT proteins

Indexed keywords

ADFP PROTEIN, HUMAN; ADFP PROTEIN, MOUSE; CARRIER PROTEIN; DNA BINDING PROTEIN; LIPID; MEMBRANE PROTEIN; MUSCLE PROTEIN; OXPAT PROTEIN, HUMAN; OXPAT PROTEIN, MOUSE; PERILIPIN; PHOSPHOPROTEIN; PLACENTA PROTEIN; PLIN3 PROTEIN, HUMAN; S3 12 PROTEIN, MOUSE; S3-12 PROTEIN, MOUSE; SIGNAL PEPTIDE; TIP47 PROTEIN, MOUSE;

ANIMAL; ATHEROSCLEROSIS; BIOSYNTHESIS; CHEMISTRY; HUMAN; METABOLISM; MOUSE; REVIEW; TRANSGENIC MOUSE;

ANIMALS; ATHEROSCLEROSIS; CARRIER PROTEINS; DNA-BINDING PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPIDS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MUSCLE PROTEINS; PHOSPHOPROTEINS; PREGNANCY PROTEINS;

EID: 79960647777     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (71)

1. Aboulaich N., Vener A.V. and Stralfors P. (2006). Hormonal control of reversible translocation of perilipin B to the plasma membrane in primary human adipocytes. J. Biol. Chem. 281, 11446-11449.
2. Atshaves B.P., Storey S.M., McIntosh A.L., Petrescu A.D., Lyuksyutova O.I., Greenberg A.S. and Schroeder F. (2001). Sterol carrier protein-2 expression modulates protein and lipid composition of lipid droplets. J. Biol. Chem. 276, 25324-25335.
3. Brasaemle D.L., Barber T., Wolins N.E., Serrero G., Blanchette-Mackie E.J. and Londos C. (1997). Adipose differentiation-related protein is an ubiquitously expressed lipid storage droplet-associated protein. J. Lipid Res. 38, 2249-2263.
4. Brasaemle D.L., Rubin B., Harten J.A., Gruia-Gray J., Kimmel A.R. and Londos C. (2000). Perilipin A increases triacylglycerol storage by decreasing the rate of triacylglycerol hydrolysis. J. Biol. Chem. 275, 38486-38493.
5. Brown D.A. (2001). Lipid droplets: proteins floating on a pool of fat. Curr. Biol. 11, R446-R449.
6. Brown M.S. and Goldstein J.L. (1999). A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. USA 96, 11041-11048.
7. Buechler C., Ritter M., Duong C.Q., Orso E., Kapinsky M. and Schmitz G. (2001). Adipophilin is a sensitive marker for lipid loading in human blood monocytes. Biochim. Biophys. Acta 1532, 97-104.
8. Buers I., Robenek H., Lorkowski S., Nitschke Y., Severs N.J. and Hofnagel O. (2009). TIP47, a lipid cargo protein involved in macrophage triglyceride metabolism. Arterioscler. Thromb. Vasc. Biol. 29, 767-773.
9. Chen F.L., Yang Z.H., Wang X.C., Liu Y., Yang Y.H., Li L.X., Liang W.C., Zhou W.B. and Hu R.M. (2009). Adipophilin affects the expression of TNF-alpha, MCP-1, and IL-6 in THP-1 macrophages. Mol. Cell. Biochem. 337, 193-199.
10. Chen J.S., Greenberg A.S., Tseng Y.Z. and Wang S.M. (2001). Possible involvement of protein kinase C in the induction of adipose differentiation-related protein by Sterol ester in RAW 264.7 macrophages. J. Cell. Biochem. 83, 187-199.
11. Dalen K.T., Dahl T., Holter E., Arntsen B., Londos C., Sztalryd C. and Nebb H.I. (2007). LSDP5 is a PAT protein specially expressed in fatty acid oxidizing tissues. Biochim. Biophys. Acta 1771, 210-227.
12. Diaz E. and Pfeffer S.R. (1998). TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93, 433-443.
13. Doege H. and Stahl A. (2006). Protein-Mediated fatty acid uptake: Novel insights from in vivo models. Physiology 21, 259-268.
14. Dong Z.M., Chapman S.M., Brown A.A., Frenette P.S., Hynes R.O. and Wagner D.D. (1998). The combined role of P- and E-selectins in atherosclerosis. J. Clin. Invest. 102, 145-152.
15. Faber B.C., Cleutjens K.B., Niessen R.L., Aarts P.L., Boon W., Greenberg A.S., Kitslaar P.J., Tordoir J.H. and Daemen M.J. (2001). Identification of genes potentially involved in rupture of human atherosclerotic plaques. Circ. Res. 89, 547-555.
16. Febbraio M., Podrez E.A., Smith J.D., Hajjar D.P., Hazen S.L., Hoff H.F., Sharma K. and Silverstein R.L. (2000). Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J. Clin. Invest. 105, 1049-1056.
17. Forcheron F., Legedz L., Chinetti G., Feugier P., Letexier D., Bricca G. and Beylot M. (2005). Genes of cholesterol metabolism in human atheroma: overexpression of perilipin and repression of ABCA1 expression. Arterioscler. Thromb. Vasc. Biol. 25, 1711-1717.
18. Galis Z.S., Muszynski M., Sukhova G.K., Simon-Morrissey E. and Libby P. (1995). Enhanced expression of vascular matrix metalloproteinases induced in vitro by cytokines and in regions of human atherosclerotic lesions. Ann. NY Acad. Sci. 748, 501-507.
19. Gao J. and Serrero G. (1999). Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty acid uptake. J. Biol. Chem. 274, 16825-16830.
20. Greenberg A.S., Egan J.J., Wek S.A., Garty N.B., Blanchette-Mackie E.J. and Londos C. (1991). Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J. Biol. Chem. 266, 11341-11346.
21. Greenberg A.S., Egan J.J, Wek S.A., Moos Jr. M.C., Londos C. and Kimmel A.R. (1993). Isolation of cDNAs for perilipin A and B: sequence and expression of lipid droplet-associated proteins of adipocytes. Proc. Natl. Acad. Sci. USA 90, 12035-12039.
22. Heid H.W., Schnölzer M. and Keenan T.W. (1996). Adipocyte differentiation-related protein is secreted into milk as a constituent of milk lipid globule membrane. Biochem. J. 320, 1025-1030.
23. Heid H.W., Moll R., Schwetlick I., Rackwitz H.R. and Keenan T.W. (1998). Adipophilin is a specific marker of lipid accumulation in diverse cell types and diseases. Cell Tissue Res. 294, 309-321.
24. Hickenbottom S.J., Kimmel A.R., Londos C. and Hurley J.H. (2004). Structure of a lipid droplet protein; the PAT family member TIP47. Structure 12, 1199-1207.
25. Hofnagel O., Buers I., Schnoor M., Lorkowski S. and Robenek H. (2007). Expression of perilipin isoforms in cell types involved in atherogenesis. Atherosclerosis 190, 14-15.
26. Jiang H.P., Harris S.E. and Serrero G. (1992). Molecular cloning of a differentiation-related mRNA in the adipogenic cell line 1246. Cell Growth Differ. 3, 21-30.
27. Koyama N., Morisaki N., Saito Y. and Yoshida S. (1992). Regulatory effects of platelet-derived growth factor-AA homodimer on migration of vascular smooth muscle cells. J. Biol. Chem. 267, 22806-22812.
28. Kruth H.S., Ifrim I., Chang J., Addadi L., Perl-Treves D. and Zhang W.Y. (2001). Monoclonal antibody detection of plasma membrane cholesterol microdomains responsive to cholesterol trafficking. J. Lipid Res. 42, 1492-1500.
29. Larigauderie G., Furman C., Jaye M., Lasselin C., Copin C., Fruchart J.C., Castro G. and Rouis M. (2004). Adipophilin enhances lipid accumulation and prevents lipid efflux from THP-1 macrophages: potential role in atherogenesis. Arterioscler. Thromb. Vasc. Biol. 24, 504-510.
30. Larigauderie G., Cuaz-Pérolin C., Younes A.B., Furman C., Lasselin C., Copin C., Jaye M., Fruchart J.C. and Rouis M. (2006a). Adipophilin increases triglyceride storage in human macrophages by stimulation of biosynthesis and inhibition of beta-oxidation. FEBS J. 273, 3498-3510.
31. Larigauderie G., Bouhlel M.A., Furman C., Jaye M., Fruchart J.C. and Rouis M. (2006b). Perilipin, a potential substitute for adipophilin in triglyceride storage in human macrophages. Atherosclerosis 189, 142-148.
32. Lass A., Zimmermann R., Haemmerle G., Riederer M., Schoiswohl G., Schweiger M., Kienesberger P., Strauss J.G., Gorkiewicz G. and Zechner R. (2006). Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman syndrome. Cell. Metab. 3, 309-319.
33. Liken J.J., Schaap F.G., van Nieuwenhoven F.A., van der Vusse G.J., Bonen A. and Glatz J.F. (1999). Cellular fatty acid transport in heart and skeletal muscle as facilitated by proteins. Lipids 34, 169-175.
34. Lindstedt K.A., Kokkonen J.O. and Kovanen P.T. (1992). Soluble heparin proteoglycans released from stimulated mast cells induce uptake of low density lipoproteins by macrophages via scavenger receptor-mediated phagocytosis. J. Lipid Res. 33, 65-75.
35. Liu P., Ying Y., Zaho Y., Mundy D.I., Zhu M. and Anderson R.G.W. (2003). CHO K2 cell lipid droplets appear to be metabolic organelles involved in membrane traffic. J. Biol. Chem. 279, 3787-3792.
36. Lu X., Gruia-Gray J., Copeland N.G., Gilbert D.J., Jenkins N.A., Londos C. and Kimmel A.R. (2001). The murine perilipin gene: the lipid droplet-associated proteins derive from tissue-specific, mRNA splice variants and define a gene family of ancient origen. Mamm. Genome 12, 741-749.
37. Murphy D.J. (2001). The biogenesis and function of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40, 325-438.
38. Nuotio K., Isoviita P.M., Saksi J., Ijäs P., Pitkäniemi J., Sonninen R., Soinne L., Saimanen E., Salonen O., Kovanen P.T., Kaste M. and Lindsberg P.J. (2007). Adipophilin expression is increased in symptomatic carotid atherosclerosis: correlation with red blood cells and cholesterol crystals. Stroke 38, 1791-1798.
39. Ohsaki Y., Maeda T., Maeda M., Tauchi-Sato K. and Fujimoto T. (2006). Recruitment of TIP47 to lipid droplets is controlled by the putative hydrophobic cleft. Biochem. Biophys. Res. Commun. 347, 279-287.
40. Ozeki S., Cheng J., Tauchi-Sato K., Hatano N., Taniguchi H. and Fujimoto T. (2005). Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane. J. Cell Sci. 118, 2601-2611.
41. Paul A., Chang B.H., Li L., Yechoor V.K. and Chan L. (2008). Deficiency of adipose differentiation-related protein impairs foam cell formation and protects against atherosclerosis. Circ. Res. 102, 1492-1501.
42. Persson J., Degerman E., Nilsson J. and Lindholm M.W. (2007). Perilipin and adipophilin expression in lipid loaded macrophages. Biochem. Biophys. Res. Commun. 363, 1020-1026.
43. Ploegh H.L. (2007). A lipid-based model for the creation of an escape hatch from the endoplasmic reticulum. Nature 448, 435-438.
44. Robenek H. and Severs N.J. (1992). Cell interactions in atherosclerosis. CRC Press. Boca Raton.
45. Robenek M.J., Severs N.J., Schlattmann K., Plenz G., Zimmer K.P., Troyer D. and Robenek H. (2004). Lipids partition caveolin-1 from ER membranes into lipid droplets: updating the model of lipid droplet biogenesis. FASEB J. 18, 866-868.
46. Robenek H., Lorkowski S., Schnoor M. and Troyer D. (2005a). Spatial integration of TIP47 and adipophilin in macrophage lipid bodies. J. Biol. Chem. 280, 5789-5794.
47. Robenek H., Robenek M.J. and Troyer D. (2005b). PAT family proteins pervade lipid droplet cores. J. Lipid Res. 46, 1331-1338.
48. Robenek H., Robenek M.J., Buers I., Lorkowski S., Hofnagel O., Troyer D. and Severs N.J. (2005c). Lipid droplets gain PAT family proteins by interaction with specialized plasma membrane domains. J. Biol. Chem. 280, 26330-26338.
49. Robenek H., Hofnagel O., Buers I., Robenek M.J., Troyer D. and Severs N.J. (2006). Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis. J. Cell Sci. 119, 4215-4224.
50. Robenek H., Buers I., Hofnagel O., Robenek M.J., Troyer D. and Severs N.J. (2009). Compartmentalization of proteins in lipid droplet biogenesis. Biochim. Biophys. Acta 1791, 408-418.
51. Ross R. (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801-809.
52. Ross R. (1999). Atherosclerosis-an inflammatory disease. N. Engl. J. Med. 340, 115-126.
53. Scherer P.E., Bickel P.E., Kotler M. and Lodish H.F. (1998). Cloning of cell-specific secreted and surface proteins by subtractive antibody screening. Nat. Biotechnol. 16, 581-586.
54. Schweiger M., Schreiber R., Haemmerle G., Lass A., Fledelius C., Jacobsen P., Tornqvist H., Zechner R. and Zimmermann R. (2006). Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism. J. Biol. Chem. 281, 40236-40241.
55. Schwenke D.C. and Carew T.E. (1989). Initiation of atherosclerotic lesions in cholesterol-fed rabbits. II. Selective retention of LDL vs. selective increases in LDL permeability in susceptible sites of arteries. Arteriosclerosis 9, 908-918.
56. Serrero G., Frolov A., Schroeder F., Tanaka K. and Gelhaar L. (2000). Adipose differentiation related protein: expression, purification of recombinant protein in Escherichia coli and characterization of its fatty acid binding properties. Biochim. Biophys. Acta 1488, 245-254.
57. Soccio R.M. and Breslow J.L. (2004). Intracellular cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 24, 1150-1160.
58. Stremmel W., Pohl L., Ring A. and Herrmann T. (2001). A new concept of cellular uptake and intracellular trafficking of long-chain fatty acids. Lipids 36, 981-989.
59. Suzuki H., Kurihara Y., Takeya M., Kamada N., Kataoka M., Jishage K., Ueda O., Sakaguchi H., Higashi T., Suzuki T., Takashima Y., Kawabe Y., Cynshi O., Wada Y., Honda M., Kurihara H., Aburatani H., Doi T., Matsumoto A., Azuma S., Noda T., Toyoda Y., Itakura H., Yazaki Y. and Kodama T. (1997). A role for macrophage scavenger receptors in atherosclerosis and susceptibility to infection. Nature 386, 292-296.
60. Tansey J.T., Huml A.M., Vogt R., Davis K.E., Jones J.M., Fraser K.A., Brasaemle D.L., Kimmel A.R. and Londos C. (2003). Functional studies on native and mutated forms of perilipins. A role in protein kinase A-mediated lipolysis of triacylglycerols. J. Biol. Chem. 278, 8401-8406.
61. Tauchi-Sato K., Ozeki S., Houjou T., Taguchi R. and Fujimoto T. (2002). The surface of lipid droplets is a phospholipid monolayer with a unique fatty acid composition. J. Biol. Chem. 277, 44507-44512.
62. Umlauf E., Csaszar E., Moertelmaier M., Schuetz G., Parton R.G. and Prohaska R. (2004). Association of stomatin with lipid droplets. J. Biol. Chem. 279, 23699-23709.
63. Wang X., Reape T.J., Li X., Rayner K., Webb C.L., Burnand K.G. and Lyso P.G. (1999). Induced expression of adipophilin mRNA in human macrophages stimulated with oxidized low-density lipoprotein in atherosclerotic lesions. FEBS Lett. 462, 445-450.
64. Wei P., Taniguchi S., Sakai Y., Imamura M., Inoguchi T., Nawata H., Oda S., Nakabeppu Y., Nishimura J. and Ikuyama S. (2005). Expression of adipose differentiation-related protein (ADRP) is conjointly regulated by PU.1 and AP-1 in macrophages. J. Biochem. 138, 399-412.
65. Wolins N.E., Rubin B. and Brasaemle D.L. (2001). TIP47 associates with lipid droplets. J. Biol. Chem. 276, 5101-5108.
66. Wolins N.E., Skinner J.R., Schoenfish M.J., Tzekov A., Bensch K.G. and Bickel P.E. (2003). Adipocyte protein S3-12 coats nascent lipid droplets. J. Biol. Chem. 278, 37713-37721.
67. Wolins N.E., Brasaemle D.L. and Bickel P.E. (2006a). A proposed model of fat packaging by exchangeable lipid droplet proteins. FEBS Lett. 580, 5484-5491.
68. Wolins N.E., Quaynor B.K., Skinner J.R., Tzekov A., Croce M.A., Gropler M.C., Varma V., Yao-Borengasser A., Rasouli N., Kern P.A., Finck B.N. and Bickel P.E. (2006b). OXPAT/PAT-1 is a PPARinduced lipid droplet protein that promotes fatty acid utilization. Diabetes 55, 3418-3428.
69. Yamaguchi T., Matsushita S., Motojima K., Hirose F. and Osumi T. (2006). MLDP, a novel PAT family protein localized to lipid droplets and enriched in the heart, is regulated by peroxisome proliferatoractivated receptor alpha. J. Biol. Chem. 281, 14232-14240.
70. Zhao B., Fisher B.J., Clair R.W., Rudel L.L. and Ghosh S. (2005). Redistribution of macrophage cholesteryl ester hydrolase from cytoplasm to lipid droplets upon lipid loading. J. Lipid Res. 46, 2114-2121.
71. Zimmermann R., Strauss J.G., Haemmerle G., Schoiswohl G., Birner-Gruenberger R., Riederer M., Lass A., Neuberger G., Eisenhaber F., Hermetter A. and Zechner R. (2004). Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306, 1383-1386.