TFE3 controls lipid metabolism in adipose tissue of male mice by suppressing lipolysis and thermogenesis

Endocrinology

Volumn 154, Issue 10, 2013, Pages 3577-3588

  Fujimoto, Yuri ^a   Nakagawa, Yoshimi ^a   Satoh, Aoi ^a   Okuda, Kanako ^a   Shingyouchi, Akiko ^a   Naka, Ayano ^a   Matsuzaka, Takashi ^a   Iwasaki, Hitoshi ^a   Kobayashi, Kazuto ^a   Yahagi, Naoya ^a   Shimada, Masako ^a   Yatoh, Shigeru ^a   Suzuki, Hiroaki ^a   Yogosawa, Satomi ^b   Izumi, Tetsuro ^b   Sone, Hirohito ^a   Urayama, Osamu ^a   Yamada, Nobuhiro ^a   Shimano, Hitoshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b GUNMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACID; G0 G1 SWITCH 2 PROTEIN; MESSENGER RNA; PERILIPIN; PERILIPIN 1; PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E3; TRANSCRIPTION FACTOR FKHR; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 1;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; DIET RESTRICTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REPRESSION; GENE EXPRESSION; HUMAN; HUMAN CELL; LIPID METABOLISM; LIPOLYSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; THERMOGENESIS; WEIGHT; WHITE ADIPOSE TISSUE; WILD TYPE;

3T3-L1 CELLS; ADIPOGENESIS; ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; DOWN-REGULATION; FATTY ACID-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; ION CHANNELS; LIPASE; LIPOLYSIS; MALE; MICE; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; OBESITY; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS; THERMOGENESIS;

EID: 84884686048     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1203     Document Type: Article

References (40)

1. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277-359. (Pubitemid 38054374)
2. Karlsson M, Contreras JA, Hellman U, Tornqvist H, Holm C. cDNA cloning, tissue distribution, and identification of the catalytic triad of monoglyceride lipase. Evolutionary relationship to esterases, lysophospholipases, and haloperoxidases. J Biol Chem. 1997;272:27218-27223. (Pubitemid 27452682)
3. Ahmadian M, Abbott MJ, Tang T, et al. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 2011;13:739-748.
4. Wei Wu J, Wang SP, Casavant S, Moreau A, Yang GS, Mitchell GA. Fasting energy homeostasis in mice with adipose deficiency of desnutrin/adipose triglyceride lipase. Endocrinology. 2012;153:2198-2207.
5. Haemmerle G, Lass A, Zimmermann R, et al. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science. 2006;312:734-737.
6. Beckmann H, Su LK, Kadesch T. TFE3: a helix-loop-helix protein that activates transcription through the immunoglobulin enhancer muE3 motif. Genes Dev. 1990;4:167-179.
7. Giangrande PH, Hallstrom TC, Tunyaplin C, Calame K, Nevins JR. Identification of E-box factor TFE3 as a functional partner for the E2F3 transcription factor. Mol Cell Biol. 2003;23:3707-3720. (Pubitemid 36597453)
8. Grinberg AV, Kerppola T. Both Max and TFE3 cooperate with Smad proteins to bind the plasminogen activator inhibitor-1 promoter, but they have opposite effects on transcriptional activity. J Biol Chem. 2003;278:11227-11236. (Pubitemid 36792679)
9. Feinman R, Qiu WQ, Pearse RN, et al. PU.1 and an HLH family member contribute to the myeloid-specific transcription of the Fc γ RIIIA promoter. EMBO J. 1994;13:3852-3860. (Pubitemid 24275031)
10. Armah HB, Parwani AV. Xp11.2 translocation renal cell carcinoma. Arch Pathol Lab Med. 2010;134:124-129.
11. Betschinger J, Nichols J, Dietmann S, Corrin PD, Paddison PJ, Smith A. Exit from pluripotency is gated by intracellular redistribution of the bHLH transcription factor Tfe3. Cell. 2013;153:335-347.
12. Huan C, Kelly ML, Steele R, Shapira I, Gottesman SR, Roman CA. Transcription factors TFE3 and TFEB are critical for CD40 ligand expression and thymus-dependent humoral immunity. Nat Immunol. 2006;7:1082-1091.
13. Nakagawa Y, Shimano H, Yoshikawa T, et al. TFE3 transcriptionally activates hepatic IRS-2, participates in insulin signaling and ameliorates diabetes. Nature Med. 2006;12:107-113. (Pubitemid 43050084)
14. Iwasaki H, Naka A, Iida KT, et al. TFE3 regulates muscle metabolic gene expression, increases glycogen stores, and enhances insulin sensitivity in mice. Am J Physiol Endocrinol Metab. 2012;302:E896-E902.
15. Nakanishi N, Nakagawa Y, Tokushige N, et al The up-regulation of microRNA-335 is associated with lipid metabolism in liver and white adipose tissue of genetically obese mice. Biochem Biophys Res Commun. 2009;385:492-496.
16. Fujimoto Y, Nakagawa Y, Shingyouchi A, et al. Dicer has a crucial role in the early stage of adipocyte differentiation, but not in lipid synthesis, in 3T3-L1 cells. Biochem Biophys Res Commun. 2012;420:931-936.
17. Yang XY, Lu X, Lombes M, et al. The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab. 2010;11:194-205.
18. Hirota K, Daitoku H, Matsuzaki H, et al. Hepatocyte nuclear factor-4 is a novel downstream target of insulin via FKHR as a signal-regulated transcriptional inhibitor. J Biol Chem. 2003;278:13056-13060. (Pubitemid 36800073)
19. Yogosawa S, Mizutani S, Ogawa Y, Izumi T. Activin receptor-like kinase 7 suppresses lipolysis to accumulate fat in obesity through downregulation of peroxisome proliferator-activated receptor γ and C/EBPα. Diabetes. 2013;62:115-123.
20. Elmasri H, Karaaslan C, Teper Y, et al. Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells. FASEB J. 2009;23:3865-3873.
21. Makowski L, Boord JB, Maeda K, et al. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis. Nat Med. 2001;7:699-705. (Pubitemid 32588026)
22. Ferrell RE, KimakMA,Lawrence EC, Finegold DN. Candidate gene analysis in primary lymphedema. Lymph Res Biol. 2008;6:69-76. (Pubitemid 351873442)
23. Urs S, Harrington A, Liaw L, Small D. Selective expression of an aP2/fatty acid binding protein 4-Cre transgene in non-adipogenic tissues during embryonic development. Transgen Res. 2006;15:647-653. (Pubitemid 44401444)
24. Cui X, Wang Y, Meng L, et al. Overexpression of a short human seipin/BSCL2 isoform in mouse adipose tissue results in mild lipodystrophy. AmJ Physiol Endocrinol Metab. 2012;302:E705-E713.
25. Kamei N, Tobe K, Suzuki R, et al. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem. 2006;281:26602-26614. (Pubitemid 44401869)
26. Ross SR, Graves RA, Greenstein A, et al. A fat-specific enhancer is the primary determinant of gene expression for adipocyte P2 in vivo. Proc Natl Acad Sci USA. 1990;87:9590-9594. (Pubitemid 120016489)
27. Wojciechowicz K, Gledhill K, Ambler CA, Manning CB, Jahoda CA. Development of the mouse dermal adipose layer occurs independently of subcutaneous adipose tissue and is marked by restricted early expression of FABP4. PloS One. 2013;8:e59811.
28. Eguchi J, Wang X, Yu S, et al. Transcriptional control of adipose lipid handling by IRF4. Cell Metab. 2011;13:249-259.
29. Chakrabarti P, Kandror KV. FoxO1 controls insulin-dependent adipose triglyceride lipase (ATGL) expression and lipolysis in adipocytes. J Biol Chem. 2009;284:13296-13300.
30. Fortier M, Wang SP, Mauriege P, et al. Hormone-sensitive lipase-independent adipocyte lipolysis during beta-adrenergic stimulation, fasting, and dietary fat loading. Am J Physiol Endocrinol Metab. 2004;287:E282-E288. (Pubitemid 38943894)
31. Osuga J, Ishibashi S, Oka T, et al. Targeted disruption of hormone-sensitive lipase results in male sterility and adipocyte hypertrophy, but not in obesity. Proc Natl Acad Sci USA. 2000;97:787-792. (Pubitemid 30070388)
32. Kershaw EE, Schupp M, Guan HP, Gardner NP, Lazar MA, Flier JS. PPARγ regulates adipose triglyceride lipase in adipocytes in vitro and in vivo. Am J Physiol Endocrinol Metab. 2007;293:E1736-E1745. (Pubitemid 350255127)
33. Lass A, Zimmermann R, Haemmerle G, Riederer M, Schoiswohl G, Schweiger M, Kienesberger P, Strauss JG, Gorkiewicz G, Zechner R. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman Syndrome. Cell Metab. 2006;3:309-319.
34. Miyoshi H, Souza SC, Endo M, et al. Perilipin overexpression in mice protects against diet-induced obesity. J Lipid Res. 2010;51:975-982.
35. Liew CW, Boucher J, Cheong JK, Vernochet C, et al. Ablation of TRIP-Br2, a regulator of fat lipolysis, thermogenesis and oxidative metabolism, prevents diet-induced obesity and insulin resistance. Nat Med. 2013;19:217-226.
36. Ahmadian M, Duncan RE, Varady KA, et al. Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes. 2009;58:855-866.
37. Haemmerle G, Moustafa T, Woelkart G, et al. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-α and PGC-1. Nat Med. 2011;17:1076-1085.
38. Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F, Giralt M. Peroxisome proliferator-activated receptor α activates transcription of the brown fat uncoupling protein-1 gene. A link between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J Biol Chem. 2001;276:1486-1493. (Pubitemid 32096582)
39. Kienesberger PC, Pulinilkunnil T, Sung MM, et al. Myocardial ATGL overexpression decreases the reliance on fatty acid oxidation and protects against pressure overload-induced cardiac dysfunction. Mol Cell Biol. 2012;32:740-750.
40. Nielsen TS, Kampmann U, Nielsen RR, et al. Reduced mRNA and protein expression of perilipin A and G0/G1 switch gene 2 (G0S2) in human adipose tissue in poorly controlled type 2 diabetes. J Clin Endocrinol Metab. 2012;97:E1348-E1352.