Central leptin activates mitochondrial function and increases heat production in skeletal muscle

Endocrinology

Volumn 152, Issue 7, 2011, Pages 2609-2618

  Henry, Belinda A ^a   Andrews, Zane B ^a   Rao, Alexandra ^a   Clarke, Iain J ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEPTIN; MESSENGER RNA; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL RESPIRATION; CONTROLLED STUDY; FEMALE; FEMORAL ARTERY; MUSCLE BIOPSY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATION CONTROL; SKELETAL MUSCLE; TEMPERATURE MEASUREMENT; THERMOGENESIS;

ADENOSINE DIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFUSIONS, INTRAVENTRICULAR; ION CHANNELS; LEPTIN; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE PROTEINS; MUSCLE, SKELETAL; NEURONS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; RNA, MESSENGER; SHEEP, DOMESTIC; THERMOGENESIS; UNCOUPLING AGENTS;

EID: 79959449682     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2011-0143     Document Type: Article

References (44)

1. Gonzalez-Alonso J, Quistorff B, Krustrup P, Bangsbo J, Saltin B 2000 Heat production in human skeletal muscle at the onset of intense dynamic exercise. J Physiol 524(Pt 2):603-615 (Pubitemid 30229522)
2. Janský L 1977 Contribution of striated muscles to regulatory heat production. Experientia 33:1123-1124 (Pubitemid 8173316)
3. Stewart MA, Franks-Skiba K, Chen S, Cooke R Myosin 2010 ATP turnover rate is a mechanism involved in thermogenesis in resting skeletal muscle fibers. Proc Natl Acad Sci USA 107:430-435
4. Tseng YH, Cypess AM, Kahn CR 2010 Cellular bioenergetics as a target for obesity therapy. Nat Rev Drug Discov 9:465-482
5. Dulhunty AF, Beard NA, Pouliquin P, Kimura T 2006 Novel regulators of RyR Ca2+ release channels: insight into molecular changes in genetically-linked myopathies. J Muscle Res Cell Motil 27:351-365 (Pubitemid 44325614)
6. Lowell BB, Spiegelman BM 2000 Towards a molecular understanding of adaptive thermogenesis. Nature 404:652-660 (Pubitemid 30205070)
7. Cannon B, Nedergaard J 2004 Brown adipose tissue: function and physiological significance. Physiol Rev 84:277-359 (Pubitemid 38054374)
8. Gong DW, He Y, Karas M, Reitman M 1997 Uncoupling protein-3 is a mediator of thermogenesis regulated by thyroid hormone, β3-adrenergic agonists, and leptin. J Biol Chem 272:24129-24132 (Pubitemid 27418606)
9. Schrauwen P, Hesselink M 2002 UCP2 and UCP3 in muscle controlling body metabolism. J Exp Biol 205:2275-2285
10. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, Levi-Meyrueis C, Bouillaud F, Seldin MF, Surwit RS, Ricquier D, Warden CH 1997 Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15:269-272 (Pubitemid 27098720)
11. Almind K, Manieri M, Sivitz WI, Cinti S, Kahn CR 2007 Ectopic brown adipose tissue in muscle provides a mechanism for differences in risk of metabolic syndrome in mice. Proc Natl Acad Sci USA 104:2366-2371 (Pubitemid 46391403)
12. Costford SR, Chaudhry SN, Crawford SA, Salkhordeh M, Harper ME 2008 Long-term high-fat feeding induces greater fat storage in mice lacking UCP3. Am J Physiol Endocrinol Metab 295:E1018-E1024
13. Choi CS, Fillmore JJ, Kim JK, Liu ZX, Kim S, Collier EF, Kulkarni A, Distefano A, Hwang YJ, Kahn M, Chen Y, Yu C, Moore IK, Reznick RM, Higashimori T, Shulman GI 2007 Overexpression of uncoupling protein 3 in skeletal muscle protects against fat-induced insulin resistance. J Clin Invest 117:1995-2003
14. Tiraby C, Tavernier G, Capel F, Mairal A, Crampes F, Rami J, Pujol C, Boutin JA, Langin D 2007 Resistance to high-fat-diet-induced obesity and sexual dimorphism in the metabolic responses of transgenic mice with moderate uncoupling protein 3 overexpression in glycolytic skeletal muscles. Diabetologia 50:2190-2199 (Pubitemid 47373849)
15. Harper ME, Dent R, Monemdjou S, Bézaire V, Van Wyck L, Wells G, Kavaslar GN, Gauthier A, Tesson F, McPherson R 2002 Decreased mitochondrial proton leak and reduced expression of uncoupling protein 3 in skeletal muscle of obese diet-resistant women. Diabetes 51:2459-2466 (Pubitemid 34827394)
16. Shabalina IG, Hoeks J, Kramarova TV, Schrauwen P, Cannon B, Nedergaard J 2010 Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects. Biochim Biophys Acta 1797:968-980
17. Samec S, Seydoux J, Russell AP, Montani JP, Dulloo AG 2002 Skeletal muscle heterogeneity in fasting-induced upregulation of genes encoding UCP2, UCP3, PPARγ and key enzymes of lipid oxidation. Pflugers Arch 445:80-86 (Pubitemid 35370418)
18. Kus V, Prazak T, Brauner P, Hensler M, Kuda O, Flachs P, Janovska P, Medrikova D, Rossmeisl M, Jilkova Z, Stefl B, Pastalkova E, Drahota Z, Houstek J, Kopecky J 2008 Induction of muscle thermogenesis by high-fat diet in mice: association with obesity-resistance. Am J Physiol Endocrinol Metab 295:E356-E367
19. Henry BA, Dunshea FR, Gould M, Clarke IJ 2008 Profiling postprandial thermogenesis in muscle and fat of sheep and the central effect of leptin administration. Endocrinology 149:2019-2026 (Pubitemid 351468325)
20. Rahmouni K, Morgan DA 2007 Hypothalamic arcuate nucleus mediates the sympathetic and arterial pressure responses to leptin. Hypertension 49:647-652
21. Tajima D, Masaki T, Hidaka S, Kakuma T, Sakata T, Yoshimatsu H 2005 Acute central infusion of leptin modulates fatty acid mobilization by affecting lipolysis and mRNA expression for uncoupling proteins. Exp Biol Med 230:200-206 (Pubitemid 40293693)
22. Scarpace PJ, Matheny M, Pollock BH, Tümer N 1997 Leptin increases uncoupling protein expression and energy expenditure. Am J Physiol 273:E226-E230
23. Mostyn A, Bispham J, Pearce S, Evens Y, Raver N, Keisler DH, Webb R, Stephenson T, Symonds ME 2002 Differential effects of leptin on thermoregulation and uncoupling protein abundance in the neonatal lamb. FASEB J 16:1438-1440
24. Zhang J, Matheny MK, Tümer N, Mitchell MK, Scarpace PJ 2007 Leptin antagonist reveals that the normalization of caloric intake and the thermic effect of food after high-fat feeding are leptin dependent. Am J Physiol Regul Integr Comp Physiol 292:R868-R874 (Pubitemid 46207742)
25. Henry BA, Goding JW, Tilbrook AJ, Dunshea FR, Clarke IJ 2001 Intracerebroventricular infusion of leptin elevates the secretion of luteinising hormone without affecting food intake in long-term food-restricted sheep, but increases growth hormone irrespective of bodyweight. J Endocrinol 168:67-77 (Pubitemid 32099354)
26. Henry BA, Goding JW, Alexander WS, Tilbrook AJ, Canny BJ, Dunshea F, Rao A, Mansell A, Clarke IJ 1999 Central administration of leptin to ovariectomized ewes inhibits food intake without affecting the secretion of hormones from the pituitary gland: evidence for a dissociation of effects on appetite and neuroendocrine function. Endocrinology 140:1175-1182 (Pubitemid 29104218)
27. Laker RC, Henry BA, Wadley GD, Clarke IJ, Canny BJ, McConell GK2011 Central infusion of leptin does not increase AMP-activated protein kinase (AMPK) signaling in skeletal muscle of sheep. Am J Physiol Regul Integr Comp Physiol 300:R511-R518
28. Golozoubova V, Cannon B, Nedergaard J 2006 UCP1 is essential for adaptive adrenergic nonshivering thermogenesis. Am J Physiol Endocrinol Metab 291:E350-E357 (Pubitemid 44035295)
29. Ukropec J, Anunciado RV, Ravussin Y, Kozak LP 2006 Leptin is required for uncoupling protein-1-independent thermogenesis during cold stress. Endocrinology 147:2468-2480
30. Ukropec J, Anunciado RP, Ravussin Y, Hulver MW, Kozak LP 2006 UCP1-independent thermogenesis in white adipose tissue of cold-acclimated Ucp1-/- mice. J Biol Chem 281:31894-31908 (Pubitemid 46041452)
31. Fromme T, Hoffmann C, Nau K, Rozman J, Reichwald K, Utting M, Platzer M, Klingenspor M 2009 An intronic single base exchange leads to a brown adipose tissue-specific loss of Ucp3 expression and an altered body mass trajectory. Physiol Genomics 38:54-62
32. Nau K, Fromme T, Meyer CW, von Praun C, Heldmaier G, Klingenspor M 2008 Brown adipose tissue specific lack of uncoupling protein 3 is associated with impaired cold tolerance and reduced transcript levels of metabolic genes. J Comp Physiol B 178:269-277 (Pubitemid 351640697)
33. Mills EM, Banks ML, Sprague JE, Finkel T 2003 Pharmacology: uncoupling the agony from ecstasy. Nature 426:403-404
34. Gómez-Ambrosi J, Frühbeck G, Martínez JA 1999 Leptin, but not a β3-adrenergic agonist, upregulates muscle uncoupling protein-3 messenger RNA expression: short-term thermogenic interactions. Cell Mol Life Sci 55:992-997 (Pubitemid 29304451)
35. Symonds ME, Budge H, Perkins AC, Lomax MA 13 December 2010 Adipose tissue development - Impact of the early life environment. Prog Biophys Mol Biol 10.1016/j.pbiomolbio.2010.11.008
36. Guerra C, Koza RA, Yamashita H, Walsh K, Kozak LP 1998 Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J Clin Invest 102:412-420 (Pubitemid 28335201)
37. Surwit RS, Wang S, Petro AE, Sanchis D, Raimbault S, Ricquier D, Collins S 1998 Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci USA 95:4061-4065 (Pubitemid 28173254)
38. Lombardi A, de Lange P, Silvestri E, Busiello RA, Lanni A, Goglia F, Moreno M 2009 3,5-Diiodothyronine rapidly enhances mitochondrial fatty acid oxidation rate and thermogenesis in rat skeletal muscle: AMP-activated protein kinase involvement. Am J Physiol Endocrinol Metab 296:E497-E502
39. Solinas G, Summermatter S, Mainieri D, Gubler M, Pirola L, Wymann MP, Rusconi S, Montani JP, Seydoux J, Dulloo AG 2004 The direct effect of leptin on skeletal muscle thermogenesis is mediated by substrate cycling between de novo lipogenesis and lipid oxidation. FEBS Lett 577:539-544 (Pubitemid 39535345)
40. Minokoshi Y, Kahn BB 2003 Role of AMP-activated protein kinase in leptin-induced fatty acid oxidation in muscle. Biochem Soc Trans 31:196-201 (Pubitemid 36241427)
41. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Müller C, Carling D, Kahn BB 2002 Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415:339-343 (Pubitemid 34087557)
42. Janovská A, Hatzinikolas G, Staikopoulos V, McInerney J, Mano M, Wittert GA 2008 AMPK and ACC phosphorylation: effect of leptin, muscle fibre type and obesity. Mol Cell Endocrinol 284:1-10
43. Roman EA, Reis D, Romanatto T, Maimoni D, Ferreira EA, Santos GA, Torsoni AS, Velloso LA, Torsoni MA 2010 Central leptin action improves skeletal muscle AKT, AMPK, and PGC1α activation by hypothalamic PI3K-dependent mechanism. Mol Cell Endocrinol 314:62-69
44. Hoehn KL, Turner N, Swarbrick MM, Wilks D, Preston E, Phua Y, Joshi H, Furler SM, Larance M, Hegarty BD, Leslie SJ, Pickford R, Hoy AJ, Kraegen EW, James DE, Cooney GJ 2010 Acute or chronic upregulation of mitochondrial fatty acid oxidation has no net effect on whole-body energy expenditure or adiposity. Cell metabolism 11:70-76