Brown adipose tissue in the treatment of obesity and diabetes: Are we hot enough?

Journal of Diabetes Investigation

Volumn 2, Issue 5, 2011, Pages 341-350

  Tan, Chong Yew ^a   Ishikawa, Ko ^a   Virtue, Samuel ^a   Vidal Puig, Antonio ^a  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Brown adipose tissue; Energy expenditure; Weight loss

Indexed keywords

2,4 DINITROPHENOL; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; LIOTHYRONINE; THYROID HORMONE;

ADAPTIVE IMMUNITY; ADRENERGIC SYSTEM; AVERAGE DAILY ENERGY EXPENDITURE; BODY WEIGHT; BROWN ADIPOSE TISSUE; CALORIC RESTRICTION; COLD EXPOSURE; COLD INDUCED THERMOGENESIS; DIABETES MELLITUS; DIET; DIET INDUCED THERMOGENESIS; DRUG ACTIVITY; ENERGY EXPENDITURE; EXERCISE; EXERCISE INDUCED ENERGY EXPENDITURE; FOOD INTAKE; HUMAN; HYPERTHYROIDISM; HYPOMETABOLIC DISORDER; METABOLIC DISORDER; METABOLIC RATE; NONHUMAN; OBESITY; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RESTING METABOLIC RATE; REVIEW; THERMOGENESIS; WEIGHT REDUCTION;

EID: 80053980028     PISSN: 20401116     EISSN: 20401124     Source Type: Journal    
DOI: 10.1111/j.2040-1124.2011.00158.x     Document Type: Review

References (104)

1. Wu T, Gao X, Chen M, et al. Long-term effectiveness of diet-plus-exercise interventions vs. diet-only interventions for weight loss: a meta-analysis. Obes Rev 2009; 10: 313-323.
2. Barte JCM, Ter Bogt NCW, Bogers RP, et al. Maintenance of weight loss after lifestyle interventions for overweight and obesity, a systematic review. Obes Rev 2010; 11: 899-906.
3. Franz MJ, VanWormer JJ, Crain AL, et al. Weight-loss outcomes: a systematic review and meta-analysis of weight-loss clinical trials with a minimum 1-year follow-up. J Am Diet Assoc 2007; 107: 1755-1767.
4. Rosenbaum M, Hirsch J, Gallagher DA, et al. Long-term persistence of adaptive thermogenesis in subjects who have maintained a reduced body weight. Am J Clin Nutr 2008; 88: 906-912.
5. Rosenbaum M, Kissileff HR, Mayer LE, et al. Energy intake in weight-reduced humans. Brain Res 2010; 1350: 95-102.
6. Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med 1995; 332: 621-628.
7. Cannon B, Nedergaard J. Thermogenesis challenges the adipostat hypothesis for body-weight control. Proc Nutr Soc 2009; 68: 401-407.
8. Rothwell NJ, Saville ME, Stock MJ. Effects of feeding a 'cafeteria' diet on energy balance and diet-induced thermogenesis in four strains of rat. J Nutr 1982; 112: 1515-1524.
9. Rothwell NJ, Stock MJ. Luxuskonsumption, diet-induced thermogenesis and brown fat: the case in favour. Clin Sci 1983; 64: 19-23.
10. 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.
11. Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 1518-1525.
12. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med 2009; 360: 1500-1508.
13. Rosenbaum M, Leibel RL, Hirsch J. Obesity. N Engl J Med 1997; 337: 396-407.
14. Stroebele N, Hill JO, Willich SN. Identifying the energy gap in the German population using results from representative national health surveys (1985-2002). Public Health Nutr 2011; 14: 44-48.
15. Donnelly JE, Hill JO, Jacobsen DJ, et al. Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women: the Midwest Exercise Trial. Arch Intern Med 2003; 163: 1343-1350.
16. Bouchard C. The magnitude of the energy imbalance in obesity is generally underestimated. Int J Obes 2008; 32: 879-880.
17. Hill JO, Peters JC, Wyatt HR. Using the energy gap to address obesity: a commentary. J Am Diet Assoc 2009; 109: 1848-1853.
18. Ravussin E. Metabolic differences and the development of obesity. Metabolism 1995; 44(Suppl 3): 12-14.
19. Astrup A, Buemann B, Toubro S, et al. Low resting metabolic rate in subjects predisposed to obesity: a role for thyroid status. Am J Clin Nutr 1996; 63: 879-883.
20. Westerterp KR, Speakman JR. Physical activity energy expenditure has not declined since the 1980s and matches energy expenditures of wild mammals. Int J Obes 2008; 32: 1256-1263.
21. Edholm OG, Fletcher JG, Widdowson EM, et al. The energy expenditure and food intake of individual men. Br J Nutr 1955; 9: 286-300.
22. Melzer K, Kayser B, Saris WHM, et al. Effects of physical activity on food intake. Clin Nutr 2005; 24: 885-895.
23. van Marken Lichtenbelt WD, Schrauwen P, van De Kerckhove S, et al. Individual variation in body temperature and energy expenditure in response to mild cold. Am J Physiol Endocrinol Metab 2002; 282: E1077-E1083.
24. Black AE, Coward WA, Cole TJ, et al. Human energy expenditure in affluent societies: an analysis of 574 doubly-labelled water measurements. Eur J Clin Nutr 1996; 50: 72-92.
25. Sjodin AM, Andersson AB, Hogberg JM, et al. Energy balance in cross-country skiers: a study using doubly labeled water. Med Sci Sports Exerc 1994; 26: 720-724.
26. Garrow JS, Summerbell CD. Meta-analysis: effect of exercise, with or without dieting, on the body composition of overweight subjects. Eur J Clin Nutr 1995; 49: 1-10.
27. Pi-Sunyer FX, Becker DM, Bouchard C, et al. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report. National Institutes of Health. Obes Res 1998; 6(Suppl 2): S51-S209.
28. Slentz CA, Duscha BD, Johnson JL, et al. Effects of the amount of exercise on body weight, body composition, and measures of central obesity: STRRIDE. A randomized controlled study. Arch Intern Med 2004; 164: 31-39.
29. Jakicic JM, Otto AD. Physical activity considerations for the treatment and prevention of obesity. Am J Clin Nutr 2005; 82(Suppl): S226-S229.
30. Krotkiewski M. Thyroid hormones and treatment of obesity. Int J Obes Relat Metab Disord 2000; 24(Suppl 2): S116-S119.
31. Hoogwerf BJ, Nuttall FQ. Long-term weight regulation in treated hyperthyroid and hypothyroid subjects. Am J Med 1984; 76: 963-970.
32. Douyon L, Schteingart DE. Effect of obesity and starvation on thyroid hormone, growth hormone, and cortisol secretion. Endocrinol Metab Clin North Am 2002; 31: 173-189.
33. Michalaki MA, Vagenakis AG, Leonardou AS, et al. Thyroid function in humans with morbid obesity. Thyroid 2006; 16: 73-78.
34. Biondi B. Thyroid and obesity: an intriguing relationship. J Clin Endocrinol Metab 2010; 95: 3614-3617.
35. Roti E, Minelli R, Salvi M. Thyroid hormone metabolism in obesity. Int J Obes Relat Metab Disord 2000; 24(Suppl 2): S113-S115.
36. Reinehr T. Obesity and thyroid function. Mol Cell Endocrinol 2010; 316: 165-171.
37. Jansson S, Lie-Karlsen K, Stenqvist O, et al. Oxygen consumption in patients with hyperthyroidism before and after treatment with beta-blockade versus thyrostatic treatment: a prospective randomized study. Ann Surg 2001; 233: 60-64.
38. Mitchell CS, Savage DB, Dufour S, et al. Resistance to thyroid hormone is associated with raised energy expenditure, muscle mitochondrial uncoupling, and hyperphagia. J Clin Invest 2010; 120: 1345-1354.
39. Kiortsis DN, Durack I, Turpin G. Effects of a low-calorie diet on resting metabolic rate and serum tri-iodothyronine levels in obese children. Eur J Pediatr 1999; 158: 446-450.
40. Buscemi S, Verga S, Maneri R, et al. Influences of obesity and weight loss on thyroid hormones. A 3-3.5-year follow-up study on obese subjects with surgical bilio-pancreatic by-pass. J Endocrinol Invest 1997; 20: 276-281.
41. Spaulding SW, Chopra IJ, Sherwin RS, et al. Effect of caloric restriction and dietary composition of serum T3 and reverse T3 in man. J Clin Endocrinol Metab 1976; 42: 197-200.
42. Koppeschaar HP, Meinders AE, Schwarz F. The effect of a low-calorie diet alone and in combination with triiodothyronine therapy on weight loss and hypophyseal thyroid function in obesity. Int J Obes 1983; 7: 123-131.
43. Rozen R, Abraham G, Falcou R, et al. Effects of a 'physiological' dose of triiodothyronine on obese subjects during a protein-sparing diet. Int J Obes 1986; 10: 303-312.
44. Kaptein SA, Gignac MA, Badley EM. Differences in the workforce experiences of women and men with arthritis disability: a population health perspective. Arthritis Rheum 2009; 61: 605-613.
45. Moore R, Grant AM, Howard AN, et al. Treatment of obesity with triiodothyronine and a very-low-calorie liquid formula diet. Lancet 1980; 1: 223-226.
46. Wilson JH, Lamberts SW. The effect of triiodothyronine on weight loss and nitrogen balance of obese patients on a very-low-calorie liquid-formula diet. Int J Obes 1981; 5: 279-282.
47. Silva JE. Thermogenic mechanisms and their hormonal regulation. Physiol Rev 2006; 86: 435-464.
48. Silva JE. The thermogenic effect of thyroid hormone and its clinical implications. Ann Intern Med 2003; 139: 205-213.
49. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004; 84: 277-359.
50. Christoffolete MA, Linardi CC, de Jesus L, et al. Mice with targeted disruption of the Dio2 gene have cold-induced overexpression of the uncoupling protein 1 gene but fail to increase brown adipose tissue lipogenesis and adaptive thermogenesis. Diabetes 2004; 53: 577-584.
51. Balaban RS. Regulation of oxidative phosphorylation in the mammalian cell. Am J Physiol 1990; 258: C377-C389.
52. Dunlop DM. The use of 2, 4-dinitrophenol as a metabolic stimulant. Br Med J 1934; 1: 524-527.
53. Rabinowitch IM. The danger from dinitrophenol. Can Med Assoc J 1934; 30: 564-565.
54. Tainter ML, Cutting WC, Stockton AB. Use of dinitrophenol in nutritional disorders a critical survey of clinical results. Am J Public Health Nations Health 1934; 24: 1045-1053.
55. Boardman WW. Rapidly developing cataracts after dinitrophenol. Cal West Med 1935; 43: 118-119.
56. Tainter ML, Stockton AB, Cutting WC. Dinitrophenol in the treatment of obesity. JAMA 1935; 105: 332-337.
57. Wijers SL, Saris WH, van Marken Lichtenbelt WD. Cold-induced adaptive thermogenesis in lean and obese. Obesity 2010; 18: 1092-1099.
58. Wijers SL, Saris WH, van Marken Lichtenbelt WD. Individual thermogenic responses to mild cold and overfeeding are closely related. J Clin Endocrinol Metab 2007; 92: 4299-4305.
59. Celi FS, Brychta RJ, Linderman JD, et al. Minimal changes in environmental temperature result in a significant increase in energy expenditure and changes in the hormonal homeostasis in healthy adults. Eur J Endocrinol 2010; 163: 863-872.
60. Dauncey MJ. Influence of mild cold on 24 h energy expenditure, resting metabolism and diet-induced thermogenesis. Br J Nutr 1981; 45: 257-267.
61. van Ooijen AM, van Marken Lichtenbelt WD, van Steenhoven AA, et al. Seasonal changes in metabolic and temperature responses to cold air in humans. Physiol Behav 2004; 82: 545-553.
62. Yoneshiro T, Aita S, Matsushita M, et al. Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity 2011; 19: 13-16.
63. Scholander PF, Hammel HT, Hart JS, et al. Cold adaptation in Australian Aborigines. J Appl Physiol 1958; 13: 211-218.
64. Wyndham CH, Morrison JF. Adjustment to cold of Bushmen in the Kalahari Desert. J Appl Physiol 1958; 13: 219-225.
65. Hassi J, Sikkila K, Ruokonen A, et al. The pituitary-thyroid axis in healthy men living under subarctic climatological conditions. J Endocrinol 2001; 169: 195-203.
66. Korhonen I, Hassi J, Leppaluoto J. Serum concentrations of thyroid and adrenal hormones and TSH in men after repeated 1h-stays in a cold room. Int J Circumpolar Health 2001; 60: 604-608.
67. Leppaluoto J, Korhonen I, Hassi J. Habituation of thermal sensations, skin temperatures, and norepinephrine in men exposed to cold air. J Appl Physiol 2001; 90: 1211-1218.
68. Leppaluoto J, Korhonen I, Huttunen P, et al. Serum levels of thyroid and adrenal hormones, testosterone, TSH, LH, GH and prolactin in men after a 2-h stay in a cold room. Acta Physiol Scand 1988; 132: 543-548.
69. Leppaluoto J, Paakkonen T, Korhonen I, et al. Pituitary and autonomic responses to cold exposures in man. Acta Physiol Scand 2005; 184: 255-264.
70. Leppaluoto J, Sikkila K, Hassi J. Seasonal variation of serum TSH and thyroid hormones in males living in subarctic environmental conditions. Int J Circumpolar Health 1998; 57(Suppl 1): 383-385.
71. Leppaluoto J, Westerlund T, Huttunen P, et al. Effects of long-term whole-body cold exposures on plasma concentrations of ACTH, beta-endorphin, cortisol, catecholamines and cytokines in healthy females. Scand J Clin Lab Invest 2008; 68: 145-153.
72. Makinen TM, Mantysaari M, Paakkonen T, et al. Autonomic nervous function during whole-body cold exposure before and after cold acclimation. Aviat Space Environ Med 2008; 79: 875-882.
73. Makinen TM, Paakkonen T, Palinkas LA, et al. Seasonal changes in thermal responses of urban residents to cold exposure. Comp Biochem Physiol A Mol Integr Physiol 2004; 139: 229-238.
74. Paakkonen T, Leppaluoto J. Cold exposure and hormonal secretion: a review. Int J Circumpolar Health 2002; 61: 265-276.
75. Smolander J, Leppaluoto J, Westerlund T, et al. Effects of repeated whole-body cold exposures on serum concentrations of growth hormone, thyrotropin, prolactin and thyroid hormones in healthy women. Cryobiology 2009; 58: 275-278.
76. Bittel JH. Heat debt as an index for cold adaptation in men. J Appl Physiol 1987; 62: 1627-1634.
77. Bruck K, Baum E, Schwennicke HP. Cold-adaptive modifications in man induced by repeated short-term cold-exposures and during a 10-day and-night cold-exposure. Pflügers Arch 1976; 363: 125-133.
78. Johnson RE, Kark RM. Environment and food intake in man. Science 1947; 105: 378-379.
79. Leonard WR, Sorensen MV, Galloway VA, et al. Climatic influences on basal metabolic rates among circumpolar populations. Am J Hum Biol 2002; 14: 609-620.
80. Steegmann AT Jr. Human cold adaptation: an unfinished agenda. Am J Hum Biol 2007; 19: 218-227.
81. Ruff C. Variation in human body size and shape. Annu Rev Anthropol 2002; 31: 211-232.
82. Holliday TW, Hilton CE. Body proportions of circumpolar peoples as evidenced from skeletal data: Ipiutak and Tigara (Point Hope) versus Kodiak Island Inuit. Am J Phys Anthropol 2010; 142: 287-302.
83. Milan FA, Rodahl K. Caloric requirements of man in the Antarctic. J Nutr 1961; 75: 152-156.
84. Orr NW. Food requirements and weight changes of men on Antarctic expeditions. Br J Nutr 1965; 19: 79-91.
85. Budd GM, Warhaft N. Body temperature, shivering, blood pressure and heart rate during a standard cold stress in Australia and Antarctica. J Physiol 1966; 186: 216-232.
86. Budd GM, Warhaft N. Cardiovascular and metabolic responses to noradrenaline in man, before and after acclimatization to cold in Antarctica. J Physiol 1966; 186: 233-242.
87. Milan FA, Elsner RW, Rodahl K. Thermal and metabolic responses of men in the Antarctic to a standard cold stress. J Appl Physiol 1961; 16: 401-404.
88. Simpson A. The effect of Antarctic residence on energy dynamics and aerobic fitness. Int J Circumpolar Health 2010; 69: 220-235.
89. Hey E. Thermal neutrality. Br Med Bull 1975; 31: 69-74.
90. Hill JR. Reaction of the new-born animal to environmental temperature. Br Med Bull 1961; 17: 164-167.
91. Lopez M, Sessler DI, Walter K, et al. Rate and gender dependence of the sweating, vasoconstriction, and shivering thresholds in humans. Anesthesiology 1994; 80: 780-788.
92. Leblanc J. Factors affecting cold acclimation and thermogenesis in man. Med Sci Sports Exerc 1988; 20(Suppl): S193-S196.
93. Whittle AJ, Lopez M, Vidal-Puig A. Using brown adipose tissue to treat obesity: the central issue. Trends Mol Med 2011; 17: 405-411.
94. Morrison SF, Nakamura K, Madden CJ. Central control of thermogenesis in mammals. Exp Physiol 2008; 93: 773-797.
95. Foster DO, Frydman ML. Nonshivering thermogenesis in the rat. II. Measurements of blood flow with microspheres point to brown adipose tissue as the dominant site of the calorigenesis induced by noradrenaline. Can J Physiol Pharmacol 1978; 56: 110-122.
96. Hong JH, Kim HJ, Kim KJ, et al. Comparison of metabolic substrates between exercise and cold exposure in skaters. J Physiol Anthropol 2008; 27: 273-281.
97. Vallerand AL, Jacobs I. Influence of cold exposure on plasma triglyceride clearance in humans. Metabolism 1990; 39: 1211-1218.
98. Inokuma K, Ogura-Okamatsu Y, Toda C, et al. Uncoupling protein 1 is necessary for norepinephrine-induced glucose utilization in brown adipose tissue. Diabetes 2005; 54: 1385-1391.
99. Shimizu Y, Nikami H, Saito M. Sympathetic activation of glucose utilization in brown adipose tissue in rats. J Biochem 1991; 110: 688-692.
100. Shibata H, Perusse F, Vallerand A, et al. Cold exposure reverses inhibitory effects of fasting on peripheral glucose uptake in rats. Am J Physiol 1989; 257: R96-R101.
101. Cawthorne MA. Does brown adipose tissue have a role to play in glucose homeostasis? Proc Nutr Soc 1989; 48: 207-214.
102. Greco-Perotto R, Zaninetti D, Assimacopoulos-Jeannet F, et al. Stimulatory effect of cold adaptation on glucose utilization by brown adipose tissue. Relationship with changes in the glucose transporter system. J Biol Chem 1987; 262: 7732-7736.
103. Bartelt A, Bruns OT, Reimer R, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med 2011; 17: 200-205.
104. Laplante M, Festuccia WT, Soucy G, et al. Tissue-specific postprandial clearance is the major determinant of PPARgamma-induced triglyceride lowering in the rat. Am J Physiol 2009; 296: R57-R66.