Selective impairment of glucose but not fatty acid or oxidative metabolism in brown adipose tissue of subjects with type 2 diabetes

Diabetes

Volumn 64, Issue 7, 2015, Pages 2388-2397

  Blondin, Denis P ^a   Labbé, Sébastien M ^b   Noll, Christophe ^a   Kunach, Margaret ^a   Phoenix, Serge ^a,c   Guérin, Brigitte ^c   Turcotte, Éric E ^c   Haman, Francois ^d   Richard, Denis ^b   Carpentier, André C ^a  

^a CENTRE HOSPITALIER UNIVERSITAIRE DE SHERBROOKE   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE SHERBROOKE   (Canada)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID C 11; FATTY ACID; FLUORO THIAHEPTADECANOIC ACID F 18; FLUORODEOXYGLUCOSE F 18; GLUCOSE; GLYCEROL; HEMOGLOBIN A1C; HYDROCORTISONE; INSULIN; LEPTIN; ORAL ANTIDIABETIC AGENT; RADIOPHARMACEUTICAL AGENT; THYROTROPIN; THYROXINE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADULT; AEROBIC METABOLISM; AGE; ARTICLE; BROWN ADIPOSE TISSUE; CLINICAL ARTICLE; COLD EXPOSURE; COMPARATIVE STUDY; CONTROLLED STUDY; CORE TEMPERATURE; ENERGY EXPENDITURE; ENVIRONMENTAL STRESS; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HEMOGLOBIN BLOOD LEVEL; HUMAN; HYDROCORTISONE BLOOD LEVEL; INSULIN BLOOD LEVEL; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; RADIOACTIVITY; SHIVERING; SKIN TEMPERATURE; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL; TRIACYLGLYCEROL BLOOD LEVEL; TURNOVER TIME; WATER TEMPERATURE; COLD; ENERGY METABOLISM; METABOLISM; MIDDLE AGED; OXIDATION REDUCTION REACTION;

ADIPOSE TISSUE, BROWN; ADULT; COLD TEMPERATURE; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; FATTY ACIDS, NONESTERIFIED; FLUORODEOXYGLUCOSE F18; GLUCOSE; HUMANS; MALE; MIDDLE AGED; OXIDATION-REDUCTION;

EID: 84934317617     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1651     Document Type: Article

References (45)

1. Morrison SF. 2010 Carl Ludwig Distinguished Lectureship of the APS Neural Control and Autonomic Regulation Section: Central neural pathways for thermoregulatory cold defense. J Appl Physiol (1985) 2011;110:1137-1149
2. Cannon B, Nedergaard J. Brown adipose tissue: Function and physiological significance. Physiol Rev 2004;84:277-359
3. Richard D, Picard F. Brown fat biology and thermogenesis. Front Biosci (Landmark Ed) 2011;16:1233-1260
4. Sharp LZ, Shinoda K, Ohno H, et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS One 2012;7:e49452
5. Blondin DP, Labbé SM, Tingelstad HC, et al. Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J Clin Endocrinol Metab 2014;99: E438-E446
6. Ouellet V, Labbé SM, Blondin DP, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 2012;122:545-552
7. Orava J, Nuutila P, Noponen T, et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity (Silver Spring) 2013;21:2279-2287
8. Van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Coldactivated brown adipose tissue in healthy men. N Engl J Med 2009;360:1500-1508
9. Vijgen GH, Bouvy ND, Teule GJ, Brans B, Schrauwen P, Van Marken Lichtenbelt WD. Brown adipose tissue in morbidly obese subjects. PLoS One 2011;6:e17247
10. Ouellet V, Routhier-Labadie A, Bellemare W, et al. Outdoor temperature, age, sex, body mass index, and diabetic status determine the prevalence, mass, and glucose-uptake activity of 18F-FDG-detected BAT in humans. J Clin Endocrinol Metab 2011;96:192-199
11. Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009;360:1509-1517
12. Saito M, Okamatsu-Ogura Y, Matsushita M, et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes 2009;58:1526-1531
13. Ma SW, Foster DO. Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol 1986;64:609-614
14. Palmes ED, Park CR. Thermocouples for the measurement of the surface temperature of the skin. Fed Proc 1947;6:175
15. Haman F, Péronnet F, Kenny GP, et al. Effect of cold exposure on fuel utilization in humans: Plasma glucose, muscle glycogen, and lipids. J Appl Physiol (1985) 2002;93:77-84
16. Haman F, Legault SR, Weber J-M. Fuel selection during intense shivering in humans: EMG pattern reflects carbohydrate oxidation. J Physiol 2004;556: 305-313
17. Carpentier A, Patterson BW, Uffelman KD, et al. The effect of systemic versus portal insulin delivery in pancreas transplantation on insulin action and VLDL metabolism. Diabetes 2001;50:1402-1413
18. Carpentier AC, Frisch F, Cyr D, et al. On the suppression of plasma nonesterified fatty acids by insulin during enhanced intravascular lipolysis in humans. Am J Physiol Endocrinol Metab 2005;289:E849-E856
19. Labbé SM, Croteau E, Grenier-Larouche T, et al. Normal postprandial nonesterified fatty acid uptake in muscles despite increased circulating fatty acids in type 2 diabetes. Diabetes 2011;60:408-415
20. Buck A, Wolpers HG, Hutchins GD, et al. Effect of carbon-11-acetate recirculation on estimates of myocardial oxygen consumption by PET. J Nucl Med 1991;32:1950-1957
21. Klein LJ, Visser FC, Knaapen P, et al. Carbon-11 acetate as a tracer of myocardial oxygen consumption. Eur J Nucl Med 2001;28:651-668
22. Ménard SL, Croteau E, Sarrhini O, et al. Abnormal in vivo myocardial energy substrate uptake in diet-induced type 2 diabetic cardiomyopathy in rats. Am J Physiol Endocrinol Metab 2010;298:E1049-E1057
23. Croteau E, Lavallée E, Labbe SM, et al. Image-derived input function in dynamic human PET/CT: Methodology and validation with 11C-acetate and 18F-fluorothioheptadecanoic acid in muscle and 18F-fluorodeoxyglucose in brain. Eur J Nucl Med Mol Imaging 2010;37:1539-1550
24. Dunn JT, Anthony K, Amiel SA, Marsden PK. Correction for the effect of rising plasma glucose levels on quantification of MR(glc) with FDG-PET. J Cereb Blood Flow Metab 2009;29:1059-1067
25. Ci X, Frisch F, Lavoie F, et al. The effect of insulin on the intracellular distribution of 14(R,S)-[18F]Fluoro-6-thia-heptadecanoic acid in rats. Mol Imaging Biol 2006;8:237-244
26. Plourde CE, Grenier-Larouche T, Caron-Dorval D, et al. Biliopancreatic diversion with duodenal switch improves insulin sensitivity and secretion through caloric restriction. Obesity (Silver Spring) 2014;22:1838-1846
27. Tadamura E, Tamaki N, Matsumori A, et al. Myocardial metabolic changes in hypertrophic cardiomyopathy. J Nucl Med 1996;37:572-577
28. Brown M, Marshall DR, Sobel BE, Bergmann SR. Delineation of myocardial oxygen utilization with carbon-11-labeled acetate. Circulation 1987;76:687-696
29. Ng CK, Huang SC, Schelbert HR, Buxton DB. Validation of a model for [1-11C]acetate as a tracer of cardiac oxidative metabolism. Am J Physiol 1994; 266:H1304-H1315
30. Summers LK, Samra JS, Humphreys SM, Morris RJ, Frayn KN. Subcutaneous abdominal adipose tissue blood flow: Variation within and between subjects and relationship to obesity. Clin Sci (Lond) 1996;91:679-683
31. Pasarica M, Sereda OR, Redman LM, et al. Reduced adipose tissue oxygenation in human obesity: Evidence for rarefaction, macrophage chemotaxis, and inflammation without an angiogenic response. Diabetes 2009;58:718-725
32. Shimizu I, Aprahamian T, Kikuchi R, et al. Vascular rarefaction mediates whitening of brown fat in obesity. J Clin Invest 2014;124:2099-2112
33. Baba S, Jacene HA, Engles JM, Honda H, Wahl RL. CT Hounsfield units of brown adipose tissue increase with activation: Preclinical and clinical studies. J Nucl Med 2010;51:246-250
34. Blondin DP, Labbe SM, Phoenix S, et al. Contributions of white and brown adipose tissues and skeletal muscles to acute cold-induced metabolic responses in healthy men. J Physiol 2015;593:701-714.
35. Muzik O, Mangner TJ, Granneman JG. Assessment of oxidative metabolism in brown fat using PET imaging. Front Endocrinol (Lausanne) 2012;3:15
36. Heaton JM. The distribution of brown adipose tissue in the human. J Anat 1972;112:35-39
37. Chaffee RR, Roberts JC, Conaway CH, Sorenson MW. Comparative effects of temperature exposure on mass and oxidative enzyme activity of brown fat in insectivores, tupaiads and primates. Lipids 1970;5:23-29
38. Cypess AM, Haft CR, Laughlin MR, Hu HH. Brown fat in humans: Consensus points and experimental guidelines. Cell Metab 2014;20:408-415
39. Blondin DP, Tingelstad HC, Mantha OL, Gosselin C, Haman F. Maintaining thermogenesis in cold exposed humans: Relying on multiple metabolic pathways. Compr Physiol 2014;4:1383-1402
40. Bougnères P, Stunff CL, Pecqueur C, Pinglier E, Adnot P, Ricquier D. In vivo resistance of lipolysis to epinephrine. A new feature of childhood onset obesity. J Clin Invest 1997;99:2568-2573
41. Marette A, Géloën A, Collet A, Bukowiecki LJ. Defective metabolic effects of norepinephrine and insulin in obese Zucker rat brown adipose tissue. Am J Physiol 1990;258:E320-E328
42. Li Y, Fromme T, Schweizer S, Schöttl T, Klingenspor M. Taking control over intracellular fatty acid levels is essential for the analysis of thermogenic function in cultured primary brown and brite/beige adipocytes. EMBO Rep 2014;15:1069-1076
43. Jocken JW, Langin D, Smit E, et al. Adipose triglyceride lipase and hormonesensitive lipase protein expression is decreased in the obese insulin-resistant state. J Clin Endocrinol Metab 2007;92:2292-2299
44. 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 U SA 2000;97:787-792
45. 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