Adipophilin-enriched domains in the ER membrane are sites of lipid droplet biogenesis

Journal of Cell Science

Volumn 119, Issue 20, 2006, Pages 4215-4224

  Robenek, Horst ^a   Hofnagel, Oliver ^a   Buers, Insa ^a   Robenek, Mirko J ^b   Troyer, David ^a   Severs, Nicholas J ^c  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Freeze fracture immunocytochemistry; Lipid droplet formation and growth; PAT proteins

Indexed keywords

ADIPOPHILIN; FAT DROPLET; MEMBRANE PROTEIN;

ANTIBODY LABELING; ARTICLE; CELL CULTURE; CONFOCAL MICROSCOPY; CYTOCHEMISTRY; ELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; FREEZE FRACTURE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; LIPOGENESIS; MONOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELLS, CULTURED; CRYOELECTRON MICROSCOPY; ENDOPLASMIC RETICULUM; FREEZE FRACTURING; HUMANS; LIPIDS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; PEPTIDES;

EID: 33751161853     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03191     Document Type: Article

References (40)

1. 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.
2. Branton, D., Bullivant, S., Gilula, N. B., Karnovsky, M. J., Moor, H., Mühletahler, K., Northeote, D. H., Packer, L., Satir, B., Satir, P. et al. (1975). Freeze-etching nomenclature. Science 190, 54-56.
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. Brown, D. A. (2001). Lipid droplets: proteins floating on a pool of fat. Curr. Biol. 11, R446-R449.
5. Chang, T. Y., Chang, C. C. Y., Lu, X. and Lin, S. (2001). Catalysis of ACAT may be completed within the plane of the membrane: a working hypothesis. J. Lipid Res. 42, 1933-1938.
6. Cole, N. B., Murphy, D. D., Grider, T., Rueter, S., Brasaemle, D. and Nussbaum, R. L. (2002). Lipid droplet binding and oligomerization properties of the Parkinson's disease protein α-synuclein. J. Biol. Chem. 277, 6344-6352.
7. Diaz, E. and Pfeffer, S. R. (1998). TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell 93, 433-443.
8. Fujimoto, K. (1995). Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J. Cell Sci. 108, 3443-3449.
9. Fujimoto, T., Kogo, H., Ishiguro, K., Tauchi, K. and Nomura, R. (2001). Caveolin-2 is targeted to lipid droplets, a new "membrane domam" in the cell. J. Cell Biol. 152, 1079-1085.
10. Fujimoto, Y., Itabe, H., Sakai, J., Makita, M., Noda, J., Mori, M., Higashi, Y., Kojima, S. and Takano, T. (2004). Identification of major proteins in the lipid droplet-enriched fraction isolated from the human hepatocyte cell line HuH7. Biochim. Biophys. Acta 1644, 47-59.
11. 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.
12. Gaus, K., Kritharides, L., Schmitz, G., Boettcher, A., Drobnik, W., Langmann, T., Quinn, C. M., Death, A., Dean, R. T. and Jessup, W. (2004). Apolipoprotein A-1 interaction with plasma membrane lipid rafts controls cholesterol export from macrophages, FASEB J. 18, 574-576.
13. Gocze, P. M. and Freeman, D. A. (1994). Factors underlying the variability of lipid droplet fluorescence in MA-10 Leydig tumor cells. Cytometry 17, 151-158.
14. Hara, H., Tanishita, H., Yokoyama, S., Tajima, S. and Yamamoto, A. (1987). Induction of acetylated low density lipoprotein receptor and suppression of low density lipoprotein receptor on the cells of human monocytic leukemia cell line (THP-1 cell). Biochem. Biophys. Res. Commun. 146, 802-808.
15. 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.
16. Iwashima, Y., Eto, M., Hata, A., Kaku, K., Horiuchi, S., Ushikubi, F. and Sano, H. (2000). Advanced glycation end products-induced gene expression of scavenger receptors in cultured human monocyte-derived macrophages. Biochem. Biophys. Res. Commun. 277, 368-380.
17. 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.
18. Liu, P., Ying, Y., Zaho, Y., Mundy, D. L, 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.
19. Londos, C., Brasaemle, D. L., Schultz, C. J., Segrest, J. P. and Kimmel, A. R. (1999). Perilipins, ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells. Semin. Cell Dev. Biol. 10, 51-58.
20. Martinez-Botas, J., Anderson, J. B., Tessier, D., Laipillone, A., Chang, B. H., Quast, M. J., Gorenstein, D., Chen, K. H. and Chan, L, (2000). Absence of perilipin results in leanness and reverses obesity in Lep(db/ db) mice. Nat. Genet. 26, 476-479,
21. McManaman, J. L., Zabaronick, W., Schaack, J. and Orlicky, D. J. (2003). Lipid droplet targeting domains of adipophilin. J. Lipid Res. 44, 668-673.
22. Mishra, R, Eminacipator, S. N., Miller, C., Kern, T. and Simonson, M. S. (2004). Adipose differentiation related protein and regulators of lipid homeostasis identified by gene expression profiling in murine db/db diabetic kidney. Am. J. Physiol. Renal Physiol. 286, F913-F921.
23. Miura, S., Gan, J. W., Brzostowski, J., Parisi, M. J., Schultz, C. J., Londos, C., Oliver, B. and Kimmel, A. R. (2002). Functional conservation for lipid storage droplet association among perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J. Biol. Chem. 277, 32253-32257.
24. Murphy, D. J. (2001) The biogenesis and function of lipid bodies in animals, plants and microorganisms. Prog. Lipid Res. 40, 325-438.
25. Ohashi, M., Mizushima, N., Kabeya, Y. and Yoshimori, T. (2003). Localization of mammalian NAD(P)H steroid dehydrogenase-like protein on lipid droplets. J. Biol. Chem. 278, 36819-36929.
26. Ostermeyer, A. G., Ramehasan, L. T., Zeug, Y., Lublin, D. M. and Brown, D. A. (2004). Role of the hydrophobic domain in targeting caveolin-1 to lipid droplets. J. Cell Biol. 164, 69-78.
27. 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.
28. Pol, A., Martin, S., Fernandez, M. A., Ferguson, C., Carozzi, A., Luetterforst, R., Enrich, C. and Parton, R. G. (2004). Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol. Biol. Cell 15, 99-110.
29. Robenek, M. J., Schlattmann, K., Zimmer, K.-P., Plenz, G., Troyer, D. and Robenek, H. (2003). Cholesterol transporter caveolin-1 transits the lipid bilayer during intracellular cycling. FASEB J. 17, 1940-1942.
30. Robenek, M. J., Schlattmanu, K., Zimmer, K.-P., Plenz, G., 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.
31. Robenek, H., Robenek, M. J. and Troyer, D. (2005a). PAT family proteins pervade lipid droplet cores. J. Lipid Res. 46, 1331-1338.
32. Robenek, H., Lorkowski, S., Schnoor, M. and Troyer, D. (2005b). Spatial integration of TIP47 and adipophilin in macrophage lipid bodies. J. Biol. Chem. 280, 5789-5794.
33. Robenek, H., Robenek, M. J., Buers, I, Lorkowski, S., Hofnagel, O., Troyer, D. and Severs, N. J. (2005c). Lipid droplets gain their PATs by interaction with specialized plasma membrane domains. J. Biol. Chem. 280, 26330-26338.
34. Robenek, H., Hofnagel, O., Buers, I., Lorkowski, S., Schnoor, M., Robenek, M. J., Heid, H., Troyer, D. and Severs, N. J. (2006). Butyrophilin controls milk fat globule secretion. Proc. Natl. Acad. Sci. USA 103, 10385-10390.
35. Serrero, G., Frolov, R., Schroeder, F., Tanaka, K. and Gehlaar, 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.
36. 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.
37. Tokuyasu, K. T. (1980). Immunocytochemistry on ultrathin frozen sections. Histochem. J. 12, 381-403.
38. 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.
39. 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,
40. Wolins, N. E., Rubin, B. and Brasaemle, D. L. (2001). TIP47 associates with lipid droplets. J. Biol. Chem. 276, 5101-5108.