Ablation of TRIP-Br2, a regulator of fat lipolysis, thermogenesis and oxidative metabolism, prevents diet-induced obesity and insulin resistance

Nature Medicine

Volumn 19, Issue 2, 2013, Pages 217-226

  Liew, Chong Wee ^a,i   Boucher, Jeremie ^a   Cheong, Jit Kong ^b   Vernochet, Cecile ^a,c   Koh, Ho Jin ^a   Mallol, Cristina ^d   Townsend, Kristy ^a   Langin, Dominique ^e   Kawamori, Dan ^a   Hu, Jiang ⁱ   Tseng, Yu Hua ^a   Hellerstein, Marc K ^f   Farmer, Stephen R ^c   Goodyear, Laurie ^a   Doria, Alessandro ^a   Blüher, Matthias ^g   Hsu, Stephen I Hong ^h   Kulkarni, Rohit N ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^e INSERM   (France)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF LEIPZIG   (Germany)

^h UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

ⁱ UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 3 ADRENERGIC RECEPTOR; HORMONE SENSITIVE LIPASE; REGULATOR PROTEIN; TRIP BR2 PROTEIN; UNCLASSIFIED DRUG;

ADIPOCYTE; AEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENERGY EXPENDITURE; ENZYME INDUCTION; INSULIN RESISTANCE; LIPID STORAGE; LIPOLYSIS; METABOLISM; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERMOGENESIS;

3T3-L1 CELLS; ADIPOCYTES; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; DIETARY FATS; FEMALE; HUMANS; INSULIN RESISTANCE; LIPOLYSIS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; OBESITY; OXIDATION-REDUCTION; RECEPTORS, ADRENERGIC, BETA-3; STEROL ESTERASE; THERMOGENESIS; TRANSCRIPTION FACTORS;

MUS;

EID: 84873570184     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3056     Document Type: Article

References (62)

1. Kahn, B.B. & Flier, J.S. Obesity and insulin resistance. J. Clin. Invest. 106, 473-481 (2000 (Pubitemid 30666380)
2. Friedman, J.M. A war on obesity, not the obese. Science 299, 856-858 (2003 (Pubitemid 36182435)
3. Rosen, E.D. & Spiegelman, B.M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444, 847-853 (2006 (Pubitemid 46024991)
4. Duncan, R.E., Ahmadian, M., Jaworski, K., Sarkadi-Nagy, E. & Sul, H.S. Regulation of lipolysis in adipocytes. Annu. Rev. Nutr. 27, 79-101 (2007 (Pubitemid 351373349)
5. Lafontan, M. & Langin, D. Lipolysis and lipid mobilization in human adipose tissue. Prog. Lipid Res. 48, 275-297 (2009
6. Hamann, A., Flier, J.S. & Lowell, B.B. Decreased brown fat markedly enhances susceptibility to diet-induced obesity, diabetes, and hyperlipidemia. Endocrinology 137, 21-29 (1996 (Pubitemid 26004968)
7. Desvergne, B., Michalik, L. & Wahli, W. Transcriptional regulation of metabolism. Physiol. Rev. 86, 465-514 (2006
8. Feige, J.N. & Auwerx, J. Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 17, 292-301 (2007 (Pubitemid 46829846)
9. Rosenfeld, M.G., Lunyak, V.V. & Glass, C.K. Sensors and signals: A coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 20, 1405-1428 (2006 (Pubitemid 43830648)
10. Spiegelman, B.M. & Heinrich, R. Biological control through regulated transcriptional coactivators. Cell 119, 157-167 (2004 (Pubitemid 39360899)
11. Lehrke, M. & Lazar, M.A. The many faces of PPARγ. Cell 123, 993-999 (2005
12. Hsu, S.I. et al. TRIP-Br: A novel family of PHD zinc finger- and bromodomain-interacting proteins that regulate the transcriptional activity of E2F-1/DP-1. EMBO J. 20, 2273-2285 (2001 (Pubitemid 32410596)
13. Cheong, J.K. et al. TRIP-Br2 promotes oncogenesis in nude mice and is frequently overexpressed in multiple human tumors. J. Transl. Med. 7, 8 (2009
14. Darwish, H., Cho, J.M., Loignon, M. & Alaoui-Jamali, M.A. Overexpression of SERTAD3, a putative oncogene located within the 19q13 amplicon, induces E2F activity and promotes tumor growth. Oncogene 26, 4319-4328 (2007 (Pubitemid 46975794)
15. Hayashi, R., Goto, Y., Ikeda, R., Yokoyama, K.K. & Yoshida, K. CDCA4 is an E2F transcription factor family-induced nuclear factor that regulates E2F-dependent transcriptional activation and cell proliferation. J. Biol. Chem. 281, 35633-35648 (2006 (Pubitemid 46041294)
16. Lai, I.L., Wang, S.Y., Yao, Y.L. & Yang, W.M. Transcriptional and subcellular regulation of the TRIP-Br family. Gene 388, 102-109 (2007
17. Hirose, T. et al. Regulation of CREB-mediated transcription by association of CDK4 binding protein p34SEI-1 with CBP. Int. J. Mol. Med. 2003 11, 705-712 (2003
18. Kim, S.S., Chen, Y.M., O'Leary, E., Witzgall, R., Vidal, M. & Bonventre, J.V. A novel member of the RING finger family, KRIP-1, associates with the KRAB-A transcriptional repressor domain of zinc finger proteins. Proc. Natl. Acad. Sci. USA. 93, 15299-15304 (1996 (Pubitemid 27009595)
19. Fajas, L. et al. E2Fs regulate adipocyte differentiation. Dev. Cell 3, 39-49 (2002 (Pubitemid 34778394)
20. Tseng, Y.H. et al. Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin. Nat. Cell Biol. 7, 601-611 (2005
21. Sim, K.G., Cheong, J.K. & Hsu, S.I. The TRIP-Br family of transcriptional regulators is essential for the execution of cyclin E-mediated cell cycle progression. Cell Cycle 5, 1111-1115 (2006 (Pubitemid 43765308)
22. Almind, K. & Kahn, C.R. Genetic determinants of energy expenditure and insulin resistance in diet-induced obesity in mice. Diabetes 53, 3274-3285 (2004 (Pubitemid 39571714)
23. Jandacek, R.J., Heubi, J.E. & Tso, P. A novel, noninvasive method for the measurement of intestinal fat absorption. Gastroenterology 127, 139-144 (2004 (Pubitemid 38962282)
24. Hotta, K. et al. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler. Thromb. Vasc. Biol. 20, 1595-1599 (2000 (Pubitemid 30353893)
25. Rosenbaum, M. & Leibel, R.L. The role of leptin in human physiology. N. Engl. J. Med. 341, 913-915 (1999 (Pubitemid 29427057)
26. Postic, C. & Girard, J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: Lessons from genetically engineered mice. J. Clin. Invest. 118, 829-838 (2008 (Pubitemid 351364588)
27. Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 444, 860-867 (2006
28. Schenk, S., Saberi, M. & Olefsky, J.M. Insulin sensitivity: Modulation by nutrients and inflammation. J. Clin. Invest. 118, 2992-3002 (2008
29. Gregoire, F.M., Smas, C.M. & Sul, H.S. Understanding adipocyte differentiation. Physiol. Rev. 78, 783-809 (1998 (Pubitemid 28340604)
30. Rosen, E.D. & MacDougald, O.A. Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7, 885-896 (2006 (Pubitemid 44871415)
31. Kersten, S. Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep. 2, 282-286 (2001 (Pubitemid 32401521)
32. Uysal, K.T., Scheja, L., Wiesbrock, S.M., Bonner-Weir, S. & Hotamisligil, G.S. Improved glucose and lipid metabolism in genetically obese mice lacking aP2. Endocrinology 141, 3388-3396 (2000 (Pubitemid 32269028)
33. Turner, S.M. et al. Measurement of TG synthesis and turnover in vivo by 2H2O incorporation into the glycerol moiety and application of MIDA. Am. J. Physiol. Endocrinol. Metab. 285, E790-E803 (2003 (Pubitemid 37176430)
34. Ahmadian, M. et al. Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes 58, 855-866 (2009
35. Zimmermann, R. et al. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306, 1383-1386 (2004 (Pubitemid 39532517)
36. Holm, C., Osterlund, T., Laurell, H. & Contreras, J.A. Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Annu. Rev. Nutr. 20, 365-393 (2000
37. Mottillo, E.P., Shen, X.J. & Granneman, J.G. Role of hormone-sensitive lipase in β-adrenergic remodeling of white adipose tissue. Am. J. Physiol. Endocrinol. Metab. 293, E1188-E1197 (2007 (Pubitemid 350106584)
38. Langin, D. et al. Adipocyte lipases and defect of lipolysis in human obesity. Diabetes 54, 3190-3197 (2005 (Pubitemid 43334374)
39. Lowell, B.B. & Bachman, E.S. β-adrenergic receptors, diet-induced thermogenesis, and obesity. J. Biol. Chem. 278, 29385-29388 (2003 (Pubitemid 36962316)
40. Cermak, T. et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res. 39, e82 (2011
41. Lonard, D.M., Lanz, R.B. & O'Malley, B.W. Nuclear receptor coregulators and human disease. Endocr. Rev. 28, 575-587 (2007 (Pubitemid 47236337)
42. Jaworski, K. et al. AdPLA ablation increases lipolysis and prevents obesity induced by high-fat feeding or leptin deficiency. Nat. Med. 15, 159-168 (2009
43. Lucas, S., Tavernier, G., Tiraby, C., Mairal, A. & Langin, D. Expression of human hormone-sensitive lipase in white adipose tissue of transgenic mice increases lipase activity but does not enhance in vitro lipolysis. J. Lipid Res. 44, 154-163 (2003 (Pubitemid 36114781)
44. Kopecky, J. et al. Reduction of dietary obesity in aP2-Ucp transgenic mice: Mechanism and adipose tissue morphology. Am. J. Physiol. 270, E776-E786 (1996
45. Wang, Y.X. et al. Peroxisome-proliferator-activated receptor δ activates fat metabolism to prevent obesity. Cell 113, 159-170 (2003
46. Puigserver, P. et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839 (1998 (Pubitemid 28155321)
47. Leone, T.C. et al. PGC-1α deficiency causes multi-system energy metabolic derangements: Muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3, e101 (2005
48. Kosteli, A. et al. Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J. Clin. Invest. 120, 3466-3479 (2010
49. Blanchet, E., Annicotte, J.S. & Fajas, L. Cell cycle regulators in the control of metabolism. Cell Cycle 8, 4029-4031 (2009
50. Berndt, J. et al. Plasma visfatin concentrations and fat depot-specific mRNA expression in humans. Diabetes 54, 2911-2916 (2005 (Pubitemid 41401086)
51. Blüher, M., Unger, R., Rassoul, F., Richter, V. & Paschke, R. Relation between glycaemic control, hyperinsulinaemia and plasma concentrations of soluble adhesion molecules in patients with impaired glucose tolerance or Type II diabetes. Diabetologia 45, 210-216 (2002 (Pubitemid 34208383)
52. Carpenter, A.E. et al. CellProfiler: Image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100 (2006
53. Chiang, S.H. et al. The protein kinase IKKε regulates energy balance in obese mice. Cell 138, 961-975 (2009
54. Ahmadian, M. et al. Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab. 13, 739-748 (2011
55. Yehuda-Shnaidman, E., Buehrer, B., Pi, J., Kumar, N. & Collins, S. Acute stimulation of white adipocyte respiration by PKA-induced lipolysis. Diabetes 59, 2474-2483 (2010
56. Wu, M. et al. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292, C125-C136 (2007 (Pubitemid 46115126)
57. Boucher, J. et al. Human α2A-adrenergic receptor gene expressed in transgenic mouse adipose tissue under the control of its regulatory elements. J. Mol. Endocrinol. 29, 251-264 (2002 (Pubitemid 35276613)
58. Macotela, Y., Boucher, J., Tran, T.T. & Kahn, C.R. Sex and depot differences in adipocyte insulin sensitivity and glucose metabolism. Diabetes 58, 803-812 (2009
59. Folch, J., Lees, M. & Sloane Stanley, G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509 (1957
60. Morgenstern, J.P. & Land, H. Advanced mammalian gene transfer: High titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596 (1990
61. Kulkarni, R.N. et al. Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 96, 329-339 (1999 (Pubitemid 29077587)
62. Lu, Y.C. et al. Cyclophilin a protects Peg3 from hypermethylation and inactive histone modification. J. Biol. Chem. 281, 39081-39087 (2006