Contributions of white and brown adipose tissues and skeletal muscles to acute cold-induced metabolic responses in healthy men

Journal of Physiology

Volumn 593, Issue 3, 2015, Pages 701-714

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

^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

FATTY ACID; GLUCOSE;

ACCLIMATIZATION; ADRENERGIC SYSTEM; ADULT; AEROBIC METABOLISM; ARTICLE; BROWN ADIPOSE TISSUE; COLD EXPOSURE; CONTROLLED STUDY; ELECTROCHEMISTRY; ENERGY EXPENDITURE; ENVIRONMENTAL TEMPERATURE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLUCOSE UTILIZATION; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; INDWELLING CATHETER; LIPOLYSIS; MALE; MUSCLE METABOLISM; NORMAL HUMAN; OXYGEN CONSUMPTION; PHYSICAL ACTIVITY; POSITRON EMISSION TOMOGRAPHY; SKELETAL MUSCLE; SKIN TEMPERATURE; THERMOGENESIS; TISSUE METABOLISM; WHITE ADIPOSE TISSUE; YOUNG ADULT; COLD SHOCK RESPONSE; METABOLISM; PHYSIOLOGY;

ADIPOSE TISSUE, BROWN; ADIPOSE TISSUE, WHITE; ADULT; COLD-SHOCK RESPONSE; GLUCOSE; HUMANS; LIPOLYSIS; MALE; MUSCLE, SKELETAL; OXYGEN CONSUMPTION;

EID: 84921913263     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.283598     Document Type: Article

References (59)

1. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, Eychmuller A, Gordts PL, Rinninger F, Bruegelmann K, Freund B, Nielsen P, Merkel M & Heeren J (2011). Brown adipose tissue activity controls triglyceride clearance. Nat Med 17, 200-205.
2. Bell DG, Tikuisis P & Jacobs I (1992). Relative intensity of muscular contraction during shivering. J Appl Physiol 72, 2336-2342.
3. Blondin DP, Labbé SM, Tingelstad HC, Noll C, Kunach M, Phoenix S, Guérin B, Turcotte ÉE, Carpentier AC, Richard D & Haman F (2014). Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J Clin Endocrinol Metab 99, E438-E446.
4. Brito NA, Brito MN & Bartness TJ (2008). Differential sympathetic drive to adipose tissues after food deprivation, cold exposure or glucoprivation. Am J Physiol Regul Integr Comp Physiol 294, R1445-1452.
5. Buck A, Wolpers HG, Hutchins GD, Savas V, Mangner TJ, Nguyen N & Schwaiger M (1991). Effect of carbon-11-acetate recirculation on estimates of myocardial oxygen consumption by PET. J Nucl Med 32, 1950-1957.
6. Cannon B & Nedergaard J (2004). Brown adipose tissue: function and physiological significance. Physiol Rev 84, 277-359.
7. Carpentier A, Patterson BW, Uffelman KD, Giacca A, Vranic M, Cattral MS & Lewis GF (2001). The effect of systemic versus portal insulin delivery in pancreas transplantation on insulin action and VLDL metabolism. Diabetes 50, 1402-1413.
8. Carpentier AC, Frisch F, Brassard P, Lavoie F, Bourbonnais A, Cyr D, Giguere R & Baillargeon JP (2007). Mechanism of insulin-stimulated clearance of plasma nonesterified fatty acids in humans. Am J Physiol Endocrinol Metab 292, E693-701.
9. Carpentier AC, Frisch F, Cyr D, Genereux P, Patterson BW, Giguere R & Baillargeon JP (2005). On the suppression of plasma nonesterified fatty acids by insulin during enhanced intravascular lipolysis in humans. Am J Physiol Endocrinol Metab 289, E849-856.
10. 18F-fluorodeoxyglucose in brain. Eur J Nucl Med Mol Imaging 37, 1539-1550.
11. Cypess AM, Chen YC, Sze C, Wang K, English J, Chan O, Holman AR, Tal I, Palmer MR, Kolodny GM & Kahn CR (2012). Cold but not sympathomimetics activates human brown adipose tissue in vivo. Proc Natl Acad Sci USA 109, 10001-10005.
12. Davidson AG & Buford JA (2004). Motor outputs from the primate reticular formation to shoulder muscles as revealed by stimulus-triggered averaging. J Neurophysiol 92, 83-95.
13. Feldmann HM, Golozoubova V, Cannon B & Nedergaard J (2009). UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9, 203-209.
14. Glatz JFC, Luiken JFP & Bonen A (2010). Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 90, 367-417.
15. Haman F, Legault SR, Rakobowchuk M, Ducharme MB & Weber J-M (2004a). Effects of carbohydrate availability on sustained shivering II: relating muscle recruitment to fuel selection. J Appl Physiol 96, 41-49.
16. Haman F, Legault SR & Weber J-M (2004b). Fuel selection during intense shivering in humans: EMG pattern reflects carbohydrate oxidation. J Physiol 556, 305-313.
17. Haman F, Péronnet F, Kenny GP, Doucet E, Massicotte D, Lavoie C & Weber J-M (2004c). Effects of carbohydrate availability on sustained shivering I: oxidation of plasma glucose, muscle glycogen and proteins. J Appl Physiol 96, 32-40.
18. Haman F, Péronnet F, Kenny GP, Massicotte D, Lavoie C, Scott C & Weber J-M (2002). Effect of cold exposure on fuel utilization in humans: plasma glucose, muscle glycogen, and lipids. J Appl Physiol 93, 77-84.
19. Haman F, Péronnet F, Kenny GP, Massicotte D, Lavoie C & Weber J-M (2005). Partitioning oxidative fuels during cold exposure in humans: muscle glycogen becomes dominant as shivering intensifies. J Physiol 566, 247-256.
20. Horowitz JF, Coppack SW, Paramore D, Cryer PE, Zhao G & Klein S (1999). Effect of short-term fasting on lipid kinetics in lean and obese women. Am J Physiol 276, E278-284.
21. Jahoor F, Klein S, Miyoshi H & Wolfe RR (1988). Effect of isotope infusion and sampling sites on glucose kinetics during a euglycemic clamp. Am J Physiol 255, E871-874.
22. Jensen MD (1991). Regulation of forearm lipolysis in different types of obesity. In vivo evidence for adipocyte heterogeneity. J Clin Invest 87, 187-193.
23. Jensen MD, Haymond MW, Gerich JE, Cryer PE & Miles JM (1987). Lipolysis during fasting. Decreased suppression by insulin and increased stimulation by epinephrine. J Clin Invest 79, 207-213.
24. Jocken JW, Goossens GH, van Hees AM, Frayn KN, van Baak M, Stegen J, Pakbiers MT, Saris WH & Blaak EE (2008). Effect of beta-adrenergic stimulation on whole-body and abdominal subcutaneous adipose tissue lipolysis in lean and obese men. Diabetologia 51, 320-327.
25. Leibel RL & Hirsch J (1987). Site- and sex-related differences in adrenoreceptor status of human adipose tissue. J Clin Endocrinol Metab 64, 1205-1210.
26. Mauriege P, Despres JP, Prud'homme D, Pouliot MC, Marcotte M, Tremblay A & Bouchard C (1991). Regional variation in adipose tissue lipolysis in lean and obese men. J Lipid Res 32, 1625-1633.
27. Mauriege P, Galitzky J, Berlan M & Lafontan M (1987). Heterogeneous distribution of beta and alpha-2 adrenoceptor binding sites in human fat cells from various fat deposits: functional consequences. Eur J Clin Invest 17, 156-165.
28. Meigal AY, Lupandin YV & Hanninen O (1996). Head and body positions affect thermoregulatory tonus in deltoid muscles. J Appl Physiol 80, 1397-1400.
29. Meigal AY, Oksa J, Hohtola E, Lupandin YV & Rintamaki H (1998). Influence of cold shivering on fine motor control in the upper limb. Acta Physiol Scand 163, 41-47.
30. Menard SL, Croteau E, Sarrhini O, Gelinas R, Brassard P, Ouellet R, Bentourkia M, van Lier JE, Des Rosiers C, Lecomte R & Carpentier AC (2010). Abnormal in vivo myocardial energy substrate uptake in diet-induced type 2 diabetic cardiomyopathy in rats. Am J Physiol Endocrinol Metab 298, E1049-1057.
31. Muzik O, Mangner TJ & Granneman JG (2012). Assessment of oxidative metabolism in brown fat using PET imaging. Front Endocrinol 3, 15.
32. 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat. J Nucl Med 54, 523-531.
33. Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, Scheinin M, Taittonen M, Niemi T, Enerback S & Virtanen KA (2011). Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab 14, 272-279.
34. Orava J, Nuutila P, Noponen T, Parkkola R, Viljanen T, Enerbäck S, Rissanen A, Pietiläinen KH & Virtanen KA (2013). Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity 21, 2279-2287.
35. Ouellet V, Labbe SM, Blondin DP, Phoenix S, Guerin B, Haman F, Turcotte EE, Richard D & Carpentier AC (2012). Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin invest 122, 545-552.
36. Palmes ED & Park CR (1947). Thermocouples for the measurement of the surface temperature of the skin. Fed Proc 6, 175.
37. Perkins JF Jr (1945). The role of the proprioceptors in shivering. Am J Physiol 145, 264-271.
38. Phelps ME (2000). Positron emission tomography provides molecular imaging of biological processes. Proc Natl Acad Sci USA 97, 9226-9233.
39. Reynisdottir S, Ellerfeldt K, Wahrenberg H, Lithell H & Arner P (1994). Multiple lipolysis defects in the insulin resistance (metabolic) syndrome. J Clin Invest 93, 2590-2599.
40. Riddle CN, Edgley SA & Baker SN (2009). Direct and indirect connections with upper limb motoneurons from the primate reticulospinal tract. J Neurosci 29, 4993-4999.
41. Rolfe DFS & Brown GC (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77, 731-758.
42. Rothwell NJ & Stock MJ (1979). A role for brown adipose tissue in diet-induced thermogenesis. Nature 281, 31-35.
43. Sallis JF, Haskell WL, Wood PD, Fortmann SP, Rogers T, Blair SN & Paffenbarger RSJ (1985). Physical activity assessment methodology in the Five-City Project. Am J Epidemiol 121, 91-106.
44. Shapovalov AI (1972). Extrapyramidal monosynaptic and disynaptic control of mammalian alpha-motoneurons. Brain Res 40, 105-115.
45. Sharp LZ, Shinoda K, Ohno H, Scheel DW, Tomoda E, Ruiz L, Hu H, Wang L, Pavlova Z, Gilsanz V & Kajimura S (2012). Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS One 7, e49452.
46. St-Onge M, Mignault D, Allison DB & Rabasa-Lhoret R (2007). Evaluation of a portable device to measure daily energy expenditure in free-living adults. Am J Clin Nutr 85, 742-749.
47. Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM, Markan KR, Nakano K, Hirshman MF, Tseng YH & Goodyear LJ (2013). Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin invest 123, 215-223.
48. Tanaka M, Owens NC, Nagashima K, Kanosue K & McAllen RM (2006). Reflex activation of rat fusimotor neurons by body surface cooling, and its dependence on the medullary raphe. J Physiol 572, 569-583.
49. van der Lans AA, Hoeks J, Brans B, Vijgen GH, Visser MG, Vosselman MJ, Hansen J, Jorgensen JA, Wu J, Mottaghy FM, Schrauwen P & van Marken Lichtenbelt WD (2013). Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 123, 3395-3403.
50. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P & Teule GJ (2009). Cold-activated brown adipose tissue in health men. N Engl J Med 360, 1500-1508.
51. Veicsteinas A, Ferretti G & Rennie DW (1982). Superficial shell insulation in resting and exercising men in cold water. J Appl Physiol 52, 1557-1564.
52. Vijgen GH, Bouvy ND, Teule GJ, Brans B, Hoeks J, Schrauwen P & van Marken Lichtenbelt WD (2012). Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab 97, E1229-1233.
53. Vijgen GH, Bouvy ND, Teule GJ, Brans B, Schrauwen P & van Marken Lichtenbelt WD (2011). Brown adipose tissue in morbidly obese subjects. PLoS One 6, e17247.
54. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerbäck S & Nuutila P (2009). Functional brown adipose tissue in healthy adults. N Engl J Med 360, 1518-1525.
55. Vosselman MJ, van der Lans AA, Brans B, Wierts R, van Baak MA, Schrauwen P & van Marken Lichtenbelt WD (2012). Systemic β-adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes 61, 3106-3113.
56. Wahrenberg H, Lonnqvist F & Arner P (1989). Mechanisms underlying regional differences in lipolysis in human adipose tissue. J Clin Invest 84, 458-467.
57. Wasserman DH, Kang L, Ayala JE, Fueger PT & Lee-Young RS (2011). The physiological regulation of glucose flux into muscle in vivo. J Exp Biol 214, 254-262.
58. Wolfe RR & Chinkes DL (2005). Isotope Tracers in Metabolic Research: Principles and Practice of Kinetic Analysis. Wiley-Liss, Hoboken, NJ.
59. Yoneshiro T, Aita S, Matsushita M, Kameya T, Nakada K, Kawai Y & Saito M (2011). Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity (Silver Spring) 19, 13-16.