Brown adipose tissue: What have we learned since its recent identification in human adults;Tecido adiposo marrom: O que aprendemos desde sua recente identificação em humanos adultos

Arquivos Brasileiros de Endocrinologia e Metabologia

Volumn 58, Issue 9, 2014, Pages 889-899

  Halpern, Bruno ^a   Mancini, Marcio Correa ^a   Halpern, Alfredo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Brown adipose tissue; Energy expenditure; Obesity; Thermogenesis; UCP 1

Indexed keywords

FLUORODEOXYGLUCOSE F 18; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN; RADIOPHARMACEUTICAL AGENT;

ADULT; BROWN ADIPOSE TISSUE; DRUG EFFECTS; ENERGY METABOLISM; HUMAN; METABOLISM; OBESITY; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PROCEDURES; THERMOGENESIS;

ADIPOSE TISSUE, BROWN; ADULT; ENERGY METABOLISM; FLUORODEOXYGLUCOSE F18; HUMANS; ION CHANNELS; MITOCHONDRIAL PROTEINS; OBESITY; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; THERMOGENESIS;

EID: 84921941748     PISSN: 00042730     EISSN: 16779487     Source Type: Journal    
DOI: 10.1590/0004-2730000003492     Document Type: Review

References (111)

1. Gessner K. Historiae Animalium: Lib I De Quadrupedibus viviparis. 1551.
2. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84(1):277-359.
3. Tam CS, Lecoultre V, Ravussin E. Brown adipose tissue: mechanisms and potential therapeutic targets. Circulation. 2012;125(22):2782-91.
4. Himms-Hagen J. Obesity may be due to a malfunctioning of brown fat. Can Med Assco J. 1979;121:1361-4.
5. Joy RTJ. Responses of cold-acclimated men to infused norepinephrine. J Appl Physiol. 1963;18:1209-12.
6. Jung RT, Leslie P, Nicholls DG, Cunningham S, Isles TE. Energy expenditure in normal and diabetic man: the role of brown adipose tissue. Health Bull (Edinb). 1988;46(1):55-62.
7. Kang BS, Han DS, Paik KS, Park YS, Kim JK, Kim CS, et al. Calorigenic action of norepinephrine in the Korean women divers. J Appl Physiol. 1970;29:6-9.
8. Lesna I, Vybıral S, Jansky L, Zeman V. Human nonshivering thermogenesis. J Therm Biol. 1999;24:63-9.
9. Bouillaud F, Villarroya F, Hentz E, Raimbault S, Cassard AM, Ricquier D. Detection of brown adipose tissue uncoupling protein mRNA in adult patients by a human genomic probe. Clin Sci. 1988;75:21-7.
10. Hany T F, Gharehpapagh E, Kamel FM, Buck A, Himms-Hagen J, von Schulthess GK. Brown adipose tissue: a factor to consider in symmetrical tracer uptake in the neck and upper chest region. Eur J Nucl Med Mol Imaging. 2002;29(10):1393-8.
11. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2007;293:E444-52.
12. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360(15):1509-17.
13. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360 (15):1500-8.
14. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360(15):1500-8.
15. Nedergaard J, Bengtsson T, Cannon B. Three years with adult human brown adipose tissue. Ann N Y Acad Sci. 2010;1212:E20-36.
16. Matthias A, Ohlson KB, Fredriksson JM, Jacobsson A, Nedergaard J, Cannon B. Thermogenic responses in brown cells are fully UCP1-dependent. UCP2 or UCP3 do not substitute for UCP1 in adrenergically or fatty-acid indeuced thermogenesis. J Biol Chem. 2000;275:25073-81.
17. Chechi K, Nedergaard J, Richard D. Brown adipose tissue as an anti-obesity tissue in humans. Obes Rev. 2014;15:92-106.
18. Arch JAT, Ainsworth AT, Cawthorne MA, Piercy V, Sennitt MV, Thody VE, et al. Atypical beta-adrenoceptor on brown adipocytes as target for anti-obesity drugs. Nature. 1984;309:163-5.
19. Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature. 1979;281(5726):31-5.
20. Cinti S. The adipose organ at a glance. Dis Model Mech. 2012;5(5):588-94.
21. Smith RE, Hock RJ. Brown fat: thermogenic effector of arousal in hibernators. Science. 1963;140:199-200.
22. Smith RE. Thermoregulatory and adaptive behavior of brown adipose tissue. Science. 1964;146:1686-9.
23. Lee P, Swarbrick MM, Ho KK. Brown adipose tissue in adult humans: a metabolic renaissance. Endocr Rev. 2013;34(3):413-38.
24. Silva JE. Thermogenic mechanisms and their hormonal regulation. Physiol Rev. 2006;86(2):435-64.
25. Ravussin E, Galgani JE. The implication of brown adipose tissue for humans. Ann Rev Nutr. 2011;31:33-47.
26. Hatai S. On the presence in human embryos of an interscapular gland corresponding to the so-called hibernating gland of lower mammals. Anat Anz. 1902;21:369-73.
27. Rasmussen A. The glandular status of brown multilocular adipose tissue. Endocrinology. 1922;6:760-70.
28. Dawkins MJ, Scopes JW. Non-shivering thermogenesis and brown adipose tissue in the human new-born infant. Nature. 1965;206:201-2.
29. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2007;293:E444-52.
30. Yeung HWD, Grewal RK, Gonen M, Schöder H, Larson SM. Patterns of 18F-FDG uptake in adipose tissue and muscle: a potential source of false-positives for PET. J Nucl Med. 2003;44:1789-96.
31. Hironaka FH, Sapienza M T, Ono CR, Lima MS, Buchpiguel CA. Base do estudo PET com FDG. In: Medicina Nuclear: Princípios e Aplicações. Ed Atheneu. 2012;15;332-5.
32. Barrington S F, Maisey MN. Skeletal muscle uptake of fluorine-18-FDG: effect of oral diazepam. J Nucl Med. 1996;37:1127-9.
33. Lean ME, James W P, Jennings G, Trayhurn P. Brown adipose tissue in patients with phaeochromocytoma. Int J Obes. 1986;10:219-27.
34. Hadi M, Chen CC, Whatley M, Pacak K, Carrasquillo J. Brown fat imaging with 18F-6-Fluorodopamine PET/CT, 18F-FDG PET/CT, and 123I-MIBG SPECT: a study of patients being evaluated for pheochromocytoma. J Nucl Med. 2007;48:1077-83.
35. Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011;14:272-9.
36. Peirce V, Vidal-Puig A. Regulation of glucose homeostasis by brown adipose tissue. Lancet. 2013;1(4):353-60.
37. Ouellet V, Labbe SM, Blondin D P, Phoenix S, Guérin B, Haman F, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545-52.
38. Yoneshiro T, Aita S, Matsushita M, Kameya T, Nakada K, Kwai Y, et al. Brown adipose tissue, whole body energy expenditure and thermogenesis in healthy adult men. Obesity (Silver Spring). 2011;19:1755-60.
39. Cannon B, Nedergaard J. Thermogenesis challenges the adipostat hypothesis for body weight control. Proc Nutr Soc. 2009;68(4):401-7.
40. Kennedy GC. The role of depot fat in the hypothalamic control of food intake in the rat. Proc Royal Soc Lond B Biol. Sci. 1953;140:578-92.
41. Barnett SA. Adaptation of mice to cold. Biol Rev Camb Philos Soc. 1965;40:5-51.
42. Ravussin Y, Xiao C, Gavrilova O, Reitman ML. Effect of intermittent cold exposure on brown fat activation, obesity and energy homeostasis in mice. PLoS ONE. 2014;9(1):e85876.
43. Yoneshiro T, Aita S, Matsushita M, Okamatsu-Ogura Y, Kameya T, Kawai Y, et al. Age-related decrease in cod-activated brown adipose tissue and accumulation of body fat in healthy humans. Obesity. 2011;19:1755-60.
44. Gadea E, Thivat E, Paulon R, Mishellany F, Gimbergues P, Capel F, et al. Hibernoma: a clinical model for exploring the role of brown adipose tissue in the regulation of body weight? J Clin Endocrol Metab. 2014;99(1):1-6.
45. Lahesmaa M, Orava J, Schalin-Jäntii C, SOinio M, Hannukainen JC, Noponen T, et al. Hyperthyroidism increases brown fat metabolism in humans. J Clin Endocr Metab. 2014;99(1):E28-35.
46. Branco M, Ribeiro M, Negrao N, Bianco AC. 3,5,3´-Triiodothyronine actively stimulates UCP in brown fat under minimal sympathetic activity. Am J Physiol Endocrinol Metab. 1999;276: E179-87.
47. Bianco AC, Sheng X, Silva JE. Triiodothyronine amplifies norepinephrine stimulation of uncoupling protein gene transcription by a mechanism not requiring protein synthesis. J Biol Chem. 1988;263:18168-75.
48. Ilye’s I, Stock MJ. Effects of hypothyroidism and hyperthyroidism on thermogenic responses to selective and nonselective beta-adrenergic agonists in rats. Acta Med Hung. 1990;47:179-88.
49. Rothwell NJ, Stock MJ, Sudera DK. Changes in adrenoreceptor density in brown adipose tissue from hyperthyroid rats. Eur J Pharmacol. 1985;114:227-9.
50. Sundin U, Mills I, Fain JN. Thyroid-catecholamine interactions in isolated rat brown adipocytes. Metabolism. 1984;33:1028-33.
51. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest. 1986;78:1568-78.
52. Stock MJ. Gluttony and thermogenesis revisited. Int J Obes. 1999;23:1105-17.
53. Wijers SLJ, Saris WHM, Wouter D. Individual thermogenic responses to mild cold and overfeeding are closely related. J Clin Endocrinol Metab. 2007;92(11):4299-305.
54. Vosselman MJ, Brans B, van der Lans AA, Wierts R, van Baak MA, Mottaghy FM, et al. Brown adipose tissue after a high-calorie meal in humans. Am J Clin Nutr. 2013;98:57-64.
55. Schlögl M, Piaggi P, Thiyyagura P, Reiman EM, Chen K, Lutrin C, et al. Overfeeding over 24 hours does not activate brown adipose tissue in humans. J Cin Endocrinol Metab. 2013;98(12):E1956-60.
56. Pasanisi F, Pace L, Fonti R, Marra M, Sgambati D, De Caprio C, et al. Evidence of brown fat activity in constitutional leanness. J Clin Endocrinol Metab. 2013;98(3):1214-8.
57. Hamilton JS. Heat increments of diets balanced and unbalanced with respect to protein. J Nutr. 1939;17:583-99.
58. Miller DS, Payne PR. Weight-maintenance and food intake. J Nutr. 1962;78:255-62.
59. Rothwell NJ, Stock MJ, Tyzbir RS. Energy balance and mitochondrial function in liver and brown fat of rats fed ‘cafeteria’ diets of varying protein content. J Nutr. 1982;112:1663-72.
60. Maxwell GM, Nobbs S, Bates DJ. Diet-induced thermogenesis in cafeteria-fed rats: a myth? Am J Physiol. 1987;253:E264-70.
61. Kozak L P. Brown fat and the myth of diet-induced thermogenesis. Cell Metab. 2010;11:263-7.
62. Cohade C, Osman M, Pannu HK, Wahl RL. Uptake in supraclavicular area fat (“USA-Fat”): description on 18FFDG-PET/CT. J Nucl Med. 2003;44:170-6.
63. Au-Yong I T, Thorn N, Ganatra R, Perkins AC, Symonds ME. Brown adipose tissue and seasonal variation in humans. Diabetes. 2009;58:2583-7.
64. Ouellet V, Routhier-Labadie A, Bellemare W, Lakhal-Chaieb L, Turcotte E, Carpentier AC, 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;96:192-9.
65. Lee P, Ho KK, Fulham MJ. The importance of brown adipose tissue. N Engl J Med. 2009;361:418; author reply, 419-20.
66. Stefan N, Pfannenberg C, Haring HU. The importance of brown adipose tissue. N Engl J Med. 2009;361:416-417; author reply, 418-21.
67. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshi-ro T, Nio-Kobayashi J, et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009;58:1526-31.
68. Griggio MA. The participation of shivering and nonshivering thermogenesis in warm and cold-acclimated rats. Comp Biochem Physiol A Physiol. 1982;73:481-4.
69. Soni A, Katoch SS. Structural and metabolic changes in skeletal muscle of cold acclimated rats. J Therm Biol. 1997;22:95-107.
70. Hart JS, Heroux O, Depocas F. Cold acclimation and the electromyogram of unanesthetized rats. J Appl Physiol. 1956;9:404-8.
71. Foster DO, Frydman ML. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can J Physiol Pharmacol. 1979;57:257-79.
72. Jacobsson A, Muhleisen M, Cannon B, Nedergaard J. The uncoupling protein thermogenin during acclimation: indications for pretranslational control. Am J Physiol. 1994;267(4 Pt 2):R999-1007.
73. Anouk AJJ, Hoeks J, Brans B, Vijgen GHEJ, Visser MGW, Vosselman MJ, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest. 2013;123(8):3395-403.
74. Yoneshiro T, Aita S, Matsushita M, Kayahara T, Kameya T, Kaway Y, et al. Recruited brown adipose tissue as an antiobesity target in humans. J Clin Invest. 2013;123(8):3404-8.
75. Tan DX, Manchester LC, Fuentes-Broto L, Paredes SD, Reiter RJ. Significance and application of melatonin in the regulation of brown adipose tissue metabolism: relation to human obesity. Obes Rev. 2011;12:167-88.
76. Jimenez-Aranda A, Fernadez-Vazquez G, Campos D, Tassim M, Velasco-Perez, Tan DX, et al. Melatonin induces browning of inguinal white adipose tissue in Zucker diabetic fatty rats. J Pineal Res. 2013;55(4):416-23.
77. Enerback E. The origins of brown adipose tissue. N Engl J Med. 2009;360(19):2021-3.
78. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, et al. White fat progenitor cells reside in the adipose vasculature. Science. 2008;322:583-6.
79. Seale P, Bjork B, Yang W, Kajimura S, Kuang S, Scime A, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008;454:961-8.
80. Xue B, Cao R, Hogan JC, Coulter AA, Koza RA, Kozak L P. Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. J Lipid Res. 2007;48:41-51.
81. Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang AH, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell. 2012;150:366-76.
82. Smorlesi A, Frontini A, Giordano A, Cinti S. The adipose organ: white-brown adipocyte plasticity and metabolic inflammation. Obes Rev. 2012;13(2):83-96.
83. Sharp LZ, Shinoda K, Ohno H, Scheel DW, Tomoda E, Ruiz L, et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS ONE. 2012;7:e49452.
84. Cannon B, Nedergaard J. Cell biology: neither brown nor white. Nature. 2012;488:286-7.
85. Lidell ME, Betz MJ, Leinhard OD, Heglind M, Elander L, Slawik M, et al. Evidence for two types of brown adipose tissue in humans. Nat Med. 2013;19(5):631-4.
86. Bonet ML, Oliver P, Palou A. Pharmacological and nutritional agents promoting browning of white adipose tissue. Biochim Biophys Acta. 2013;1831(5):969-85.
87. Lidell ME, Betz MJ, Enerbäck S. Brown adipose tissue and its therapeutical potential. J Intern Med. 2014;276(4):364-77.
88. Broeders E, Bouvy ND, van Marken Lichtenbelt WD. Endogenous ways to stimulate brown adipose tissue in humans. Ann Med. 2014 [Epub ahead of print].
89. Yoneshiro T, Aita S, Kawai Y, Iwanaga T, Saito M. Nonpungent capsaicin analogs (capsinoids) increase energy expenditure through the activation of brown adipose tissue in humans. Am J Clin Nutr. 2012;95(4):845-50.
90. Bostrom P, Wu J, Jedrychowski M P, Korde A, Ye L, Lo JC, et al. A PGC1-a-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 481:463-8.
91. Raschke S, Elsen M, Gassenhuber H, Sommerfeld M, Scwahn U, Brockmann B, et al. Evidence against a beneficial effect of irisin in humans. PLoS One. 2013;8(9):e73680.
92. Kurdiova T, Balaz M, Mayer A, Maderova D, Belan V, Wolfrum C, et al. Exercise-mimicking treatment fails to increase Fndc5 mRNA & irisin secretion in primary human myotubes. Peptides. 2014;56C:1-7.
93. Sellayah D, Bharaj P, Sikder D. Orexin is required for brown adipose tissue development, differentiation and function. Cell Metab. 2011;14:478-90.
94. Giordano A, Centemeri C, Zingaretti MC, Cinti S. Sibutramine-dependent brown fat activation in rats: an immunohistochemical study. Int J Obes Relat Metab Disord. 2002;26(3):354-60.
95. Lockie SH, Heppner KM, Chaudhary N, Chabenne JR, Morgan DA, Veyrat-Durebex C, et al. Direct control of brown adipose tissue thermogenesis by central nervous system glucagon-like peptide receptor signaling. Diabetes. 2012;61(11):2753-62.
96. Lockie SH, Stefanidis A, Oldfeld BJ, Perez-Tilve D. Brown adipose tissue thermogenesis in the resistance to and reversal of obesity: a potential new mechanism contributing to the metabolic ben-efts of proglucagon-derived peptides. Adipocyte. 2013;2(4):196-200.
97. Arterburn DE, Crane PK, Veenstra DL. The efficacy and safety of sibutramine for weigth loss. Arch Intern Med. 2004;164(9):994-1003.
98. Vilsboll T, Christensen M, Junker AE, Knopp FK, Gluud K. Effects of glucagon-like peptide-1 receptor agonists on weight loss: systematic review and meta-analyses of randomized controlled trials. BMJ. 2012;344:d7771.
99. Peirce V, Vidal-Puig A. Regulation of glucose homeostasis by brown adipose tissue. Lancet. 2013;1(4):353-60.
100. Stanford KI, Middelbeek JW, Townsend KL, An D, Nygaard EB, Hitchcox KM, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013;123(1): 215-23.
101. Gunawardana SC, Piston DW. Reversal of type 1 diabetes in mice by brown adipose tissue transplant. Diabetes. 2012;61(3):674-82.
102. Borga M, Virtanen KA, Romu T, Leinhard OD, Persson A, Nuutila P, et al. Brown adipose tissue in humans: detection and functional analysis using PET (positron emission tomography), MRI (magnetic resonance imaging), and DECT (dual energy computed tomography). Methods Enzymol. 2014;537:141-59.
103. Chen YI, Cypess AM, Sass CA, Brownell A, Jokivarsi K T, Kahn CR, et al. Anatomical and functional assessment of brown adipose tissue by magnetic resonance imaging. Obesity. 2012;20:1519-26.
104. Grimpo K, Volker MN, Heppe EN, Braun S, Heverhagen J T, Heldmaier G. Brown adipose tissue dynamics in wild-type and UC-1-knockout mice: in vivo insights with magnetic resonance. J Lipid Res. 2014;55(3):398-409.
105. Branca RT, Zhang L, Warren WS, Auerbach E, Khanna A, Degan S, et al. In vivo noninvasive detection of brown adipose tissue throughintermolecular zero-quantum MRI. PLoS. 2013;8(9):e74206.
106. Holstila M, Virtanen KA, Grönroos TJ, Laine J, Lepomäki V, Saunavaara J, et al. Measurement of brown adipose tissue mass using a novel dual-echo magnetic resonance imaging approach: a validation study. Metabolism. 2013;62(8):1189-98.
107. Reddy NL, Jones TA, Wayte SC, Adesanya O, Sankar S, Yeo YC, et al. Identification of brown adipose tissue in a human adult with histological and immunohistochemical confirmation. J Clin Endocrinol Metab. 2014;99(1):E117-21.
108. Ramanathan NL. A new weighting system for mean surface temperature of the human body. J Appl Physiol. 1964;19:531-3.
109. Deng ZS, Liu J. Mathematical modeling of temperature mapping over skin surface and its implementation in thermal disease diagnostics. Comput Biol Med. 2004;34:495-521.
110. Lee P, Ho KKY. Hot fat in a cool man: infrared thermography and brown adipose tissue. Diab Obes Metab. 2011;13:92-3.
111. Symonds ME, Henderson K, Elvidge L, Bosman C, Sharkey D, Perkins AC, et al. Thermal imaging to assess age-related changes of skin temperature within the supraclavicular region co-locating with brown adipose tissue in healthy children. J Pediatr. 2012;161:892-8.