Apolipoprotein E promotes lipid accumulation and differentiation in human adipocytes

Experimental Cell Research

Volumn 337, Issue 1, 2015, Pages 94-102

  Lasrich, Dorothee ^a   Bartelt, Alexander ^a   Grewal, Thomas ^b   Heeren, Joerg ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Adipocyte differentiation; Adipocytes; Apolipoprotein E; Lipoproteins; Peroxisome proliferator activated receptor gamma; Triglycerides

Indexed keywords

ADIPONECTIN; APOLIPOPROTEIN E; FATTY ACID BINDING PROTEIN 4; GLUCOSE TRANSPORTER 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN; APOLIPOPROTEIN E3;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; GENE EXPRESSION; GENE INDUCTION; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; INSULIN SENSITIVITY; LIPID STORAGE; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPPLEMENTATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; LIPID METABOLISM; PHYSIOLOGY;

MURINAE; MUS;

ADIPOCYTES; ANIMALS; APOLIPOPROTEIN E3; CELL DIFFERENTIATION; GENE EXPRESSION; HUMANS; LIPID METABOLISM; MICE; MICE, INBRED C57BL;

EID: 84939569516     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.07.015     Document Type: Article

References (37)

1. Kahn S.E., Hull R.L., Utzschneider K.M. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006, 444:840-846.
2. Rosen E.D., Spiegelman B.M. Molecular regulation of adipogenesis. Annu. Rev. Cell Dev. Biol. 2000, 16:145-171.
3. Maeda N., Takahashi M., Funahashi T., Kihara S., Nishizawa H., Kishida K., Nagaretani H., Matsuda M., Komuro R., Ouchi N., Kuriyama H., Hotta K., Nakamura T., Shimomura I., Matsuzawa Y. PPARgamma ligands increase expression and plasma concentrations of adiponectin, an adipose-derived protein. Diabetes 2001, 50:2094-2099.
4. Tontonoz P., Hu E., Graves R.A., Budavari A.I., Spiegelman B.M. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 1994, 8:1224-1234.
5. Lee C.H., Olson P., Evans R.M. Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 2003, 144:2201-2207.
6. Tontonoz P., Spiegelman B.M. Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 2008, 77:289-312.
7. Yue L., Mazzone T. Peroxisome proliferator-activated receptor {gamma} stimulation of adipocyte ApoE gene transcription mediated by the liver receptor X pathway. J. Biol. Chem. 2009, 284:10453-10461.
8. Beisiegel U., Weber W., Ihrke G., Herz J., Stanley K.K. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 1989, 341:162-164.
9. Ishibashi S., Herz J., Maeda N., Goldstein J.L., Brown M.S. The two-receptor model of lipoprotein clearance: tests of the hypothesis in "knockout" mice lacking the low density lipoprotein receptor, apolipoprotein E, or both proteins. Proc. Natl. Acad. Sci. USA 1994, 91:4431-4435.
10. Rohlmann A., Gotthardt M., Hammer R.E., Herz J. Inducible inactivation of hepatic LRP gene by cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J. Clin. Investig. 1998, 101:689-695.
11. Yue L., Rasouli N., Ranganathan G., Kern P.A., Mazzone T. Divergent effects of peroxisome proliferator-activated receptor gamma agonists and tumor necrosis factor alpha on adipocyte ApoE expression. J. Biol. Chem. 2004, 279:47626-47632.
12. Huang Z.H., Reardon C.A., Mazzone T. Endogenous ApoE expression modulates adipocyte triglyceride content and turnover. Diabetes 2006, 55:3394-3402.
13. Hofmann S.M., Perez-Tilve D., Greer T.M., Coburn B.A., Grant E., Basford J.E., Tschop M.H., Hui D.Y. Defective lipid delivery modulates glucose tolerance and metabolic response to diet in apolipoprotein E-deficient mice. Diabetes 2008, 57:5-12.
14. Schreyer S.A., Vick C., Lystig T.C., Mystkowski P., LeBoeuf R.C. LDL receptor but not apolipoprotein E deficiency increases diet-induced obesity and diabetes in mice. Am. J. Physiol. Endocrinol. Metab. 2002, 282:E207-E214.
15. (-/-) mice: relevance to adipose tissue inflammation, hepatic steatosis and insulin resistance. Diabetologia 2011, 54:2900-2910.
16. Gao J., Katagiri H., Ishigaki Y., Yamada T., Ogihara T., Imai J., Uno K., Hasegawa Y., Kanzaki M., Yamamoto T.T., Ishibashi S., Oka Y. Involvement of apolipoprotein E in excess fat accumulation and insulin resistance. Diabetes 2007, 56:24-33.
17. Karagiannides I., Abdou R., Tzortzopoulou A., Voshol P.J., Kypreos K.E. Apolipoprotein E predisposes to obesity and related metabolic dysfunctions in mice. FEBS J. 2008, 275:4796-4809.
18. Takahashi S., Sakai J., Fujino T., Hattori H., Zenimaru Y., Suzuki J., Miyamori I., Yamamoto T.T. The very low-density lipoprotein (VLDL) receptor: characterization and functions as a peripheral lipoprotein receptor. J. Atheroscler. Thromb. 2004, 11:200-208.
19. Huang Z.H., Minshall R.D., Mazzone T. Mechanism for endogenously expressed APOE modulation of adipocyte VLDL metabolism: role in endocytic and lipase-mediated metabolic pathways. J. Biol. Chem. 2009.
20. Chiba T., Nakazawa T., Yui K., Kaneko E., Shimokado K. VLDL induces adipocyte differentiation in ApoE-dependent manner. Arterioscler. Thromb. Vasc. Biol. 2003, 23:1423-1429.
21. Prawitt J., Niemeier A., Kassem M., Beisiegel U., Heeren J. Characterization of lipid metabolism in insulin-sensitive adipocytes differentiated from immortalized human mesenchymal stem cells. Exp. Cell Res. 2008, 314:814-824.
22. Simonsen J.L., Rosada C., Serakinci N., Justesen J., Stenderup K., Rattan S.I., Jensen T.G., Kassem M. Telomerase expression extends the proliferative life-span and maintains the osteogenic potential of human bone marrow stromal cells. Nat. Biotechnol. 2002, 20:592-596.
23. Huang Z.H., Reardon C.A., Mazzone T. Endogenous ApoE expression modulates adipocyte triglyceride content and turnover. Diabetes 2006, 55:3394-3402.
24. Huang Z.H., Gu D., Mazzone T. Role of adipocyte-derived apoE in modulating adipocyte size, lipid metabolism, and gene expression in vivo. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E1110-E1119.
25. Zechner R., Moser R., Newman T.C., Fried S.K., Breslow J.L. Apolipoprotein E gene expression in mouse 3T3-L1 adipocytes and human adipose tissue and its regulation by differentiation and lipid content. J. Biol. Chem. 1991, 266:10583-10588.
26. Huang Z.H., Reardon C.A., Mazzone T. Endogenous ApoE expression modulates adipocyte triglyceride content and turnover. Diabetes 2006, 55:3394-3402.
27. Huang Z.H., Reardon C.A., Subbaiah P.V., Getz G.S., Mazzone T. ApoE derived from adipose tissue does not suppress atherosclerosis or correct hyperlipidemia in apoE knockout mice. J. Lipid Res. 2013, 54:202-213.
28. Rosen E.D. The molecular control of adipogenesis, with special reference to lymphatic pathology. Ann. N.Y. Acad. Sci. 2002, 979:143-158.
29. Spiegelman B.M., Puigserver P., Wu Z. Regulation of adipogenesis and energy balance by PPARgamma and PGC-1. Int. J. Obes. Relat. Metab. Disord. 2000, 24(Suppl 4):S8-S10.
30. Tontonoz P., Hu E., Spiegelman B.M. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994, 79:1147-1156.
31. Ren D., Collingwood T.N., Rebar E.J., Wolffe A.P., Camp H.S. PPARgamma knockdown by engineered transcription factors: exogenous PPARgamma2 but not PPARgamma1 reactivates adipogenesis. Genes Dev. 2002, 16:27-32.
32. Mueller E., Drori S., Aiyer A., Yie J., Sarraf P., Chen H., Hauser S., Rosen E.D., Ge K., Roeder R.G., Spiegelman B.M. Genetic analysis of adipogenesis through peroxisome proliferator-activated receptor gamma isoforms. J. Biol. Chem. 2002, 277:41925-41930.
33. Niemeier A., Schinke T., Heeren J., Amling M. The role of apolipoprotein E in bone metabolism. Bone 2012, 50:518-524.
34. Bartelt A., Beil F.T., Schinke T., Roeser K., Ruether W., Heeren J., Niemeier A. Apolipoprotein E-dependent inverse regulation of vertebral bone and adipose tissue mass in C57Bl/6 mice: modulation by diet-induced obesity. Bone 2010, 47:736-745.
35. Kang K.S., Robling A.G. New Insights into Wnt-Lrp5/6-β-Catenin Signaling in mechanotransduction. Front Endocrinol. (Lausanne) 2015, 5:246.
36. Laatsch A., Merkel M., Talmud P.J., Grewal T., Beisiegel U., Heeren J. Insulin stimulates hepatic low density lipoprotein receptor-related protein 1 (LRP1) to increase postprandial lipoprotein clearance. Atherosclerosis 2009, 204:105-111.
37. Hofmann S.M., Zhou L., Perez-Tilve D., Greer T., Grant E., Wancata L., Thomas A., Pfluger P.T., Basford J.E., Gilham D., Herz J., Tschöp M.H., Hui D.Y. Adipocyte LDL receptor-related protein-1 expression modulates postprandial lipid transport and glucose homeostasis in mice. J. Clin. Invest. 2007, 117:3271-3282.