Brain insulin controls adipose tissue lipolysis and lipogenesis

Cell Metabolism

Volumn 13, Issue 2, 2011, Pages 183-194

  Scherer, Thomas ^a   OHare, James ^a   Diggs Andrews, Kelly ^b   Schweiger, Martina ^c   Cheng, Bob ^a   Lindtner, Claudia ^a   Zielinski, Elizabeth ^a   Vempati, Prashant ^a   Su, Kai ^a   Dighe, Shveta ^a   Milsom, Thomas ^a   Puchowicz, Michelle ^d   Scheja, Ludger ^e   Zechner, Rudolf ^c   Fisher, Simon J ^b   Previs, Stephen F ^d   Buettner, Christoph ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GRAZ   (Austria)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE SENSITIVE LIPASE; INSULIN; INSULIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE DELETION; LIPOGENESIS; LIPOLYSIS; MALE; MEDIOBASAL HYPOTHALAMUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; BRAIN; GLUCOSE; INSULIN; LIPOGENESIS; LIPOLYSIS; MALE; MICE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

MUS; RATTUS;

EID: 79551506567     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.01.008     Document Type: Article

References (63)

1. K. Ahmed, S. Tunaru, C. Tang, M. Müller, A. Gille, A. Sassmann, J. Hanson, and S. Offermanns An autocrine lactate loop mediates insulin-dependent inhibition of lipolysis through GPR81 Cell Metab. 11 2010 311 319
2. E.L. Air, S.C. Benoit, K.A. Blake Smith, D.J. Clegg, and S.C. Woods Acute third ventricular administration of insulin decreases food intake in two paradigms Pharmacol. Biochem. Behav. 72 2002 423 429
3. S. Andrikopoulos, A.R. Blair, N. Deluca, B.C. Fam, and J. Proietto Evaluating the glucose tolerance test in mice Am. J. Physiol. Endocrinol. Metab. 295 2008 E1323 E1332
4. M.W. Anthonsen, L. Rönnstrand, C. Wernstedt, E. Degerman, and C. Holm Identification of novel phosphorylation sites in hormone-sensitive lipase that are phosphorylated in response to isoproterenol and govern activation properties in vitro J. Biol. Chem. 273 1998 215 221
5. N.M. Anthony, M.P. Gaidhu, and R.B. Ceddia Regulation of visceral and subcutaneous adipocyte lipolysis by acute AICAR-induced AMPK activation Obesity (Silver Spring) 17 2009 1312 1317
6. F. Assimacopoulos-Jeannet, S. Brichard, F. Rencurel, I. Cusin, and B. Jeanrenaud In vivo effects of hyperinsulinemia on lipogenic enzymes and glucose transporter expression in rat liver and adipose tissues Metabolism 44 1995 228 233
7. T.J. Bartness, Y.B. Shrestha, C.H. Vaughan, G.J. Schwartz, and C.K. Song Sensory and sympathetic nervous system control of white adipose tissue lipolysis Mol. Cell. Endocrinol. 318 2010 34 43
8. B.F. Belgardt, T. Okamura, and J.C. Brüning Hormone and glucose signalling in POMC and AgRP neurons J. Physiol. 587 2009 5305 5314
9. R.N. Bergman, and M. Ader Free fatty acids and pathogenesis of type 2 diabetes mellitus Trends Endocrinol. Metab. 11 2000 351 356
10. G. Boden Fatty acid-induced inflammation and insulin resistance in skeletal muscle and liver Curr. Diab. Rep. 6 2006 177 181
11. G. Boden, X. Chen, J. Ruiz, J.V. White, and L. Rossetti Mechanisms of fatty acid-induced inhibition of glucose uptake J. Clin. Invest. 93 1994 2438 2446
12. D.J. Brief, and J.D. Davis Reduction of food intake and body weight by chronic intraventricular insulin infusion Brain Res. Bull. 12 1984 571 575
13. J.C. Brüning, D. Gautam, D.J. Burks, J. Gillette, M. Schubert, P.C. Orban, R. Klein, W. Krone, D. Müller-Wieland, and C.R. Kahn Role of brain insulin receptor in control of body weight and reproduction Science 289 2000 2122 2125
14. C. Buettner, and R.C. Camacho Hypothalamic control of hepatic glucose production and its potential role in insulin resistance Endocrinol. Metab. Clin. North Am. 37 2008 825 840
15. C. Buettner, E.D. Muse, A. Cheng, L. Chen, T. Scherer, A. Pocai, K. Su, B. Cheng, X. Li, and J. Harvey-White Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms Nat. Med. 14 2008 667 675
16. H. Cao, K. Gerhold, J.R. Mayers, M.M. Wiest, S.M. Watkins, and G.S. Hotamisligil Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism Cell 134 2008 933 944
17. J.B. Carvalheira, E.B. Ribeiro, E.P. Araújo, R.B. Guimarães, M.M. Telles, M. Torsoni, J.A. Gontijo, L.A. Velloso, and M.J. Saad Selective impairment of insulin signalling in the hypothalamus of obese Zucker rats Diabetologia 46 2003 1629 1640
18. A. Chaudhuri, D. Janicke, M. Wilson, H. Ghanim, G.E. Wilding, A. Aljada, and P. Dandona Effect of modified glucose-insulin-potassium on free fatty acids, matrix metalloproteinase, and myoglobin in ST-elevation myocardial infarction Am. J. Cardiol. 100 2007 1614 1618
19. M.F. Chong, L. Hodson, A.S. Bickerton, R. Roberts, M. Neville, F. Karpe, K.N. Frayn, and B.A. Fielding Parallel activation of de novo lipogenesis and stearoyl-CoA desaturase activity after 3 d of high-carbohydrate feeding Am. J. Clin. Nutr. 87 2008 817 823
20. E. Degerman, C.J. Smith, H. Tornqvist, V. Vasta, P. Belfrage, and V.C. Manganiello Evidence that insulin and isoprenaline activate the cGMP-inhibited low-Km cAMP phosphodiesterase in rat fat cells by phosphorylation Proc. Natl. Acad. Sci. USA 87 1990 533 537
21. E. Degerman, T.R. Landström, L.S. Holst, O. Göransson, L. Härndahl, F. Ahmad, Y.-H. Choi, S. Masciarelli, H. Liu, and V. Manganiello Role for Phosphodiesterase 3B in Regulation of Lipolysis and Insulin Secretion D. LeRoith, J.M. Olefsky, S.I. Taylor, Diabetes Mellitus: A Fundamental and Clinical Text 2003 Lippincott Williams & Wilkins Philadelphia 374 381
22. F. Diraison, E. Dusserre, H. Vidal, M. Sothier, and M. Beylot Increased hepatic lipogenesis but decreased expression of lipogenic gene in adipose tissue in human obesity Am. J. Physiol. Endocrinol. Metab. 282 2002 E46 E51
23. J.J. Egan, A.S. Greenberg, M.K. Chang, S.A. Wek, M.C. Moos Jr., and C. Londos Mechanism of hormone-stimulated lipolysis in adipocytes: translocation of hormone-sensitive lipase to the lipid storage droplet Proc. Natl. Acad. Sci. USA 89 1992 8537 8541
24. S.J. Fisher, J.C. Brüning, S. Lannon, and C.R. Kahn Insulin signaling in the central nervous system is critical for the normal sympathoadrenal response to hypoglycemia Diabetes 54 2005 1447 1451
25. A.J. Garton, and S.J. Yeaman Identification and role of the basal phosphorylation site on hormone-sensitive lipase Eur. J. Biochem. 191 1990 245 250
26. E. Gellhorn Blood sugar and autonomic nervous system Acta Neuroveg. (Wien) 9 1954 74 94
27. J. German, F. Kim, G.J. Schwartz, P.J. Havel, C.J. Rhodes, M.W. Schwartz, and G.J. Morton Hypothalamic leptin signaling regulates hepatic insulin sensitivity via a neurocircuit involving the vagus nerve Endocrinology 150 2009 4502 4511
28. H.N. Ginsberg, Y.L. Zhang, and A. Hernandez-Ono Metabolic syndrome: focus on dyslipidemia Obesity (Silver Spring) 14 Suppl 1 2006 41S 49S
29. J.G. Granneman, H.P. Moore, R.L. Granneman, A.S. Greenberg, M.S. Obin, and Z. Zhu Analysis of lipolytic protein trafficking and interactions in adipocytes J. Biol. Chem. 282 2007 5726 5735
30. G. Haemmerle, A. Lass, R. Zimmermann, G. Gorkiewicz, C. Meyer, J. Rozman, G. Heldmaier, R. Maier, C. Theussl, and S. Eder Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase Science 312 2006 734 737
31. R.A. Hegele Monogenic forms of insulin resistance: apertures that expose the common metabolic syndrome Trends Endocrinol. Metab. 14 2003 371 377
32. H.G. Hers, and L. Hue Gluconeogenesis and related aspects of glycolysis Annu. Rev. Biochem. 52 1983 617 653
33. L.C. Hudgins, M. Hellerstein, C. Seidman, R. Neese, J. Diakun, and J. Hirsch Human fatty acid synthesis is stimulated by a eucaloric low fat, high carbohydrate diet J. Clin. Invest. 97 1996 2081 2091
34. K. Jaworski, M. Ahmadian, R.E. Duncan, E. Sarkadi-Nagy, K.A. Varady, M.K. Hellerstein, H.Y. Lee, V.T. Samuel, G.I. Shulman, and K.H. Kim AdPLA ablation increases lipolysis and prevents obesity induced by high-fat feeding or leptin deficiency Nat. Med. 15 2009 159 168
35. L. Kang, X. Chen, B.M. Sebastian, B.T. Pratt, I.R. Bederman, J.C. Alexander, S.F. Previs, and L.E. Nagy Chronic ethanol and triglyceride turnover in white adipose tissue in rats: inhibition of the anti-lipolytic action of insulin after chronic ethanol contributes to increased triglyceride degradation J. Biol. Chem. 282 2007 28465 28473
36. L. Koch, F.T. Wunderlich, J. Seibler, A.C. Könner, B. Hampel, S. Irlenbusch, G. Brabant, C.R. Kahn, F. Schwenk, and J.C. Brüning Central insulin action regulates peripheral glucose and fat metabolism in mice J. Clin. Invest. 118 2008 2132 2147
37. M. Lafontan, and D. Langin Lipolysis and lipid mobilization in human adipose tissue Prog. Lipid Res. 48 2009 275 297
38. H.V. Lin, L. Plum, H. Ono, R. Gutiérrez-Juárez, M. Shanabrough, E. Borok, T.L. Horvath, L. Rossetti, and D. Accili Divergent regulation of energy expenditure and hepatic glucose production by insulin receptor in agouti-related protein and POMC neurons Diabetes 59 2010 337 346
39. L. Liu, G.B. Karkanias, J.C. Morales, M. Hawkins, N. Barzilai, J. Wang, and L. Rossetti Intracerebroventricular leptin regulates hepatic but not peripheral glucose fluxes J. Biol. Chem. 273 1998 31160 31167
40. S.D. Mittelman, and R.N. Bergman Inhibition of lipolysis causes suppression of endogenous glucose production independent of changes in insulin Am. J. Physiol. Endocrinol. Metab. 279 2000 E630 E637
41. B. Mittendorfer, F. Magkos, E. Fabbrini, B.S. Mohammed, and S. Klein Relationship between body fat mass and free fatty acid kinetics in men and women Obesity (Silver Spring) 17 2009 1872 1877
42. H. Miyoshi, J.W. Perfield 2nd, S.C. Souza, W.J. Shen, H.H. Zhang, Z.S. Stancheva, F.B. Kraemer, M.S. Obin, and A.S. Greenberg Control of adipose triglyceride lipase action by serine 517 of perilipin A globally regulates protein kinase A-stimulated lipolysis in adipocytes J. Biol. Chem. 282 2007 996 1002
43. R.C. Moraes, A. Blondet, K. Birkenkamp-Demtroeder, J. Tirard, T.F. Orntoft, A. Gertler, P. Durand, D. Naville, and M. Bégeot Study of the alteration of gene expression in adipose tissue of diet-induced obese mice by microarray and reverse transcription-polymerase chain reaction analyses Endocrinology 144 2003 4773 4782
44. S.T. Nadler, J.P. Stoehr, K.L. Schueler, G. Tanimoto, B.S. Yandell, and A.D. Attie The expression of adipogenic genes is decreased in obesity and diabetes mellitus Proc. Natl. Acad. Sci. USA 97 2000 11371 11376
45. C.M. Nepokroeff, M.R. Lakshmanan, and J.W. Porter Fatty-acid synthase from rat liver Methods Enzymol. 35 1975 37 44
46. S. Obici, B.B. Zhang, G. Karkanias, and L. Rossetti Hypothalamic insulin signaling is required for inhibition of glucose production Nat. Med. 8 2002 1376 1382
47. H. Ono, A. Pocai, Y. Wang, H. Sakoda, T. Asano, J.M. Backer, G.J. Schwartz, and L. Rossetti Activation of hypothalamic S6 kinase mediates diet-induced hepatic insulin resistance in rats J. Clin. Invest. 118 2008 2959 2968
48. K.F. Petersen, E.A. Oral, S. Dufour, D. Befroy, C. Ariyan, C. Yu, G.W. Cline, A.M. DePaoli, S.I. Taylor, P. Gorden, and G.I. Shulman Leptin reverses insulin resistance and hepatic steatosis in patients with severe lipodystrophy J. Clin. Invest. 109 2002 1345 1350
49. A. Pocai, T.K. Lam, R. Gutierrez-Juarez, S. Obici, G.J. Schwartz, J. Bryan, L. Aguilar-Bryan, and L. Rossetti Hypothalamic K(ATP) channels control hepatic glucose production Nature 434 2005 1026 1031
50. K.A. Posey, D.J. Clegg, R.L. Printz, J. Byun, G.J. Morton, A. Vivekanandan-Giri, S. Pennathur, D.G. Baskin, J.W. Heinecke, and S.C. Woods Hypothalamic proinflammatory lipid accumulation, inflammation, and insulin resistance in rats fed a high-fat diet Am. J. Physiol. Endocrinol. Metab. 296 2009 E1003 E1012
51. K. Rahmouni, D.A. Morgan, G.M. Morgan, X. Liu, C.D. Sigmund, A.L. Mark, and W.G. Haynes Hypothalamic PI3K and MAPK differentially mediate regional sympathetic activation to insulin J. Clin. Invest. 114 2004 652 658
52. K. Rebrin, G.M. Steil, S.D. Mittelman, and R.N. Bergman Causal linkage between insulin suppression of lipolysis and suppression of liver glucose output in dogs J. Clin. Invest. 98 1996 741 749
53. R. Roberts, L. Hodson, A.L. Dennis, M.J. Neville, S.M. Humphreys, K.E. Harnden, K.J. Micklem, and K.N. Frayn Markers of de novo lipogenesis in adipose tissue: associations with small adipocytes and insulin sensitivity in humans Diabetologia 52 2009 882 890
54. E.A. Roman, M. Cesquini, G.R. Stoppa, J.B. Carvalheira, M.A. Torsoni, and L.A. Velloso Activation of AMPK in rat hypothalamus participates in cold-induced resistance to nutrient-dependent anorexigenic signals J. Physiol. 568 2005 993 1001
55. L. Schäffer, C.L. Brand, B.F. Hansen, U. Ribel, A.C. Shaw, R. Slaaby, and J. Sturis A novel high-affinity peptide antagonist to the insulin receptor Biochem. Biophys. Res. Commun. 376 2008 380 383
56. L. Scheja, K. Toedter, R. Mohr, G. Niederfellner, M.D. Michael, A. Meissner, A. Schoettler, H. Pospisil, U. Beisiegel, and J. Heeren Liver TAG transiently decreases while PL n-3 and n-6 fatty acids are persistently elevated in insulin resistant mice Lipids 43 2008 1039 1051
57. M. Schweiger, R. Schreiber, G. Haemmerle, A. Lass, C. Fledelius, P. Jacobsen, H. Tornqvist, R. Zechner, and R. Zimmermann Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism J. Biol. Chem. 281 2006 40236 40241
58. M. Schweiger, G. Schoiswohl, A. Lass, F.P. Radner, G. Haemmerle, R. Malli, W. Graier, I. Cornaciu, M. Oberer, and R. Salvayre The C-terminal region of human adipose triglyceride lipase affects enzyme activity and lipid droplet binding J. Biol. Chem. 283 2008 17211 17220
59. I. Shimomura, R.E. Hammer, S. Ikemoto, M.S. Brown, and J.L. Goldstein Leptin reverses insulin resistance and diabetes mellitus in mice with congenital lipodystrophy Nature 401 1999 73 76
60. C.J. Smith, V. Vasta, E. Degerman, P. Belfrage, and V.C. Manganiello Hormone-sensitive cyclic GMP-inhibited cyclic AMP phosphodiesterase in rat adipocytes. Regulation of insulin- and cAMP-dependent activation by phosphorylation J. Biol. Chem. 266 1991 13385 13390
61. X. Zhang, G. Zhang, H. Zhang, M. Karin, H. Bai, and D. Cai Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity Cell 135 2008 61 73
62. R. Zimmermann, J.G. Strauss, G. Haemmerle, G. Schoiswohl, R. Birner-Gruenberger, M. Riederer, A. Lass, G. Neuberger, F. Eisenhaber, A. Hermetter, and R. Zechner Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase Science 306 2004 1383 1386
63. R. Zimmermann, A. Lass, G. Haemmerle, and R. Zechner Fate of fat: the role of adipose triglyceride lipase in lipolysis Biochim. Biophys. Acta 1791 2009 494 500