Insights into brown adipose tissue physiology as revealed by imaging studies

Adipocyte

Volumn 4, Issue 1, 2015, Pages 1-12

  Izzi Engbeaya, Chioma ^a   Salem, Victoria ^a   Atkar, Rajveer S ^a   Dhillo, Waljit S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Brown adipose tissue; Energy expenditure; Imaging; Metabolism; Thermogenesis

Indexed keywords

ADULT; BROWN ADIPOSE TISSUE; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMAGING; PHYSIOLOGY; PREVALENCE; RODENT;

EID: 85050578809     PISSN: 21623945     EISSN: 2162397X     Source Type: Journal    
DOI: 10.4161/21623945.2014.965609     Document Type: Review

References (88)

1. 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; PMID: 17473055; http: //dx. doi. org/10. 1152/ ajpendo. 00691. 2006
2. Hany TF, Gharehpapagh E, Kamel EM, 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: 1393-8; PMID: 12271425; http: //dx. doi. org/10. 1007/s00259-002-0902-6
3. Yeung HW, Grewal RK, Gonen M, Schoder H, Larson SM. Patterns of (18)F-FDG uptake in adipose tissue and muscle: a potential source of false positives for PET. J Nucl Med 2003; 44: 1789-96; PMID: 14602861
4. Cohade C, Mourtzikos KA, Wahl RL. "USA-fat": prevalence is related to ambient outdoor temperature-evaluation with 18F-FDG PET/CT. J Nucl Med 2003; 44: 1267-70; PMID: 12902417
5. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergreen R, Niemi T, Taittonen M, Laine J, Savisto N-J, Enerback S, et al. Functional brown adipose tissue in healthy adults. N Engl J Med 2009; 360: 1518-25; PMID: 19357407; http: //dx. doi. org/10. 1056/NEJMoa0808949
6. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng Y-H, Doria A, et al. Identification and importance of brown adipose tissue in adult humans. N Eng J Med 2009; 360: 1509-17; http: //dx. doi. org/10. 1056/NEJMoa0810780
7. Au-Yong ITH, Thorn N, Ganatra R, Perkins AC, Symonds ME. Brown adipose tissue and seasonal variation in humans. Diabetes 2009; 58: 2583-7; PMID: 19696186; http: //dx. doi. org/10. 2337/db09-0833
8. Zhang Z, Cypess AM, Miao Q, Ye H, Liew CW, Zhang Q, Xue R, Zhang S, Zuo C, Xu Z, et al. The prevalence and predictors of active brown adipose tissue in Chinese adults. Eur J Endocrinol 2014; 170: 359-66; PMID: 24288355; http: //dx. doi. org/10. 1530/EJE-13-0712
9. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanga T, Miyagawa M, Kameya T, Nakada K, 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; PMID: 19401428; http: //dx. doi. org/10. 2337/db09-0530
10. Matsushita M, Yoneshiro T, Kameya T, Sugie H, Saito M. Impact of brown adipose tissue on body fatness and glucose metabolism in healthy humans. Int J Obesity 2014; 38: 812-7; http: //dx. doi. org/10. 1038/ijo. 2013. 206
11. van Marken Lichtenbelt W, Vanhommergig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Jaap Teule GJ. Cold-activated brown adipose tissue in healthy men. N Eng J Med 2009; 360: 1500-8; http: //dx. doi. org/10. 1056/ NEJMoa0808718
12. Vijgen GHE, Bouvy ND, Jaap Teule GJ, Brans B, Schrauwen P, van Marken Lichtenbelt WD. Brown adipose tissue in morbidly obese subjects. PLoS One 2011; 6: e17247. DOI: 10. 1371/journal. pone. 0017247; PMID: 21390318; http: //dx. doi. org/ 10. 1371/journal. pone. 0017247
13. Perkins AC, Mshelia DS, Symonds ME, Sathekge M. Prevalence and pattern of brown adipose tissue distribution of 18F-FDG in patients undergoing PET-CT in subtropical climatic zone. Nucl Med Commun 2013; 34: 168-74; PMID: 23196673; http: //dx. doi. org/ 10. 1097/MNM. 0b013e32835bbbf0
14. Ouellet V, Routhier-Labadie A, Bellemare W, Lakhal-Chaieb L, Turcotte E, Carpentier AC, Richard D. Outdoor temperature, age, sex, body mass index, an 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; PMID: 20943785; http: //dx. doi. org/10. 1210/jc. 2010-0989
15. Pasanisi F, Pace L, Fonti R, Marra M, Sgambati D, De Caprio C, De Filippo E, Vaccaro A, Salvatore M, Contaldo F. Evidence of brown fat activity in constitutional leanness. J Clin Endocrinol Metab 2013; 98: 1214-8; PMID: 23393181; http: //dx. doi. org/10. 1210/jc. 2012-2981
16. Admiraal WM, Verberne HJ, Karamat FA, Soeters MR, Hoekstra JBL, Holleman F. Cold-induced activity of brown adipose tissue in young lean men of South-Asian and European origin. Diabetologia 2013; 56: 2231-37; http: //dx. doi. org/10. 1007/ s00125-013-2938-5
17. Bakker LE, Boon MR, van der Linden RA, Arias-Bouda LP, van Klinken JB, Smit F, Verberne HJ, Jukema JW, Tamsma JT, Havekes LM, et al. Brown adipose tissue volume in healthy lean south Asian adults compared with white Caucasians: a prospective, casecontrolled observational study. Lancet Diabetes Endocrinol 2014; 2: 210-7; PMID: 24622751; http: //dx. doi. org/10. 1016/S2213-8587(13)70156-6
18. Drubach LA, Palmer EL, Connolly LP, Baker A, Zurakowski D, Cypess AM. Pediatric brown adipose tissue: detection, epidemiology, and differences from adults. J Pediatr 2011; 159: 939-44; PMID: 21839465; http: // dx. doi. org/10. 1016/j. jpeds. 2011. 06. 028
19. Zukotynski KA, Fahey FH, Laffin S, Davis R, Treves ST, Grant FD, Drubach LA. Constant ambient temperature of 24_C significantly reduces FDG uptake by brown adipose tissue in children scanned during the winter. Eur J Nucl Med Mol Imaging 2009; 36: 602-6; PMID: 19037639; http: //dx. doi. org/10. 1007/s00259-008-0983-y
20. Lee P, Zhao JT, Swarbrick MM, Gracie G, Bova R, Greenfield JR, Freund J, Ho KKY. High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab 2011; 96: 2450-5; PMID: 21613352; http: // dx. doi. org/10. 1210/jc. 2011-0487
21. Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, Scheinin M, Taittonen M, Niemi T, Enerback S, et al. Cell Metab 2011; 14: 272-9; PMID: 21803297; http: //dx. doi. org/10. 1016/j. cmet. 2011. 06. 012
22. Yoneshiro T, Aita S, Matsushita M, Kameya T, Nakada K, Kawai Y, Saito M. Brown adipose tissue, wholebody energy expenditure, and thermogenesis in healthy adult men. Obesity 2011; 19: 13-6; PMID: 20448535; http: //dx. doi. org/10. 1038/oby. 2010. 105
23. Cypess AM, Doyle AN, Sass CA, Huang TL, Mowschenson PM, Rosen HN, Tseng Y-H, Palmer EL, Kolodny GM. Quantification of human and rodent brown adipose tissue function using 99mTc-methoxyisobutylisonitrile SPECT/CT and 18F-FDG PET/CT. J Nucl Med 2013; 54: 1896-901; PMID: 24071505; http: //dx. doi. org/10. 2967/jnumed. 113. 121012
24. Ouellet V, Labbe SM, Blondin DP, Phoenix S, Guerin B, Haman F, Turcotte EE, Richard D, Carpentier AC. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 2012; 122: 545-52; PMID: 22269323; http: //dx. doi. org/10. 1172/JCI60433
25. Chen KY, Brychta RJ, Linderman JD, Smith S, Courville A, Dieckmann W, Herscovitch P, Millo CM, Remaley A, Lee P, et al. Brown fat activation mediates cold-induced thermogenesis in adult humans in response to a mild decrease in ambient temperature. J Clin Endocrinol Metab 2013; 98: E1218-23; PMID: 23780370; http: //dx. doi. org/10. 1210/jc. 2012-4213
26. Muzik O, Manger TJ, Leonard WR, Kumar A, Janisse J, Granneman JG. 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat. J Nucl Med 2013; 54: 523-31; PMID: 23362317; http: //dx. doi. org/10. 2967/jnumed. 112. 111336
27. van der Lans AA, Hoeks J, Brans B, Vijgen GH, Visser MG, Vosselman MJ, Hansen J, Jorgensen JA, Wu J, Mottaghy FM, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 2013; 123: 3395-403; PMID: 23867626; http: //dx. doi. org/10. 1172/JCI68993
28. van Rooijen BD, van der Lans AAJJ, Brans B, Wildberger JE, Mottaghy FM, Schrauwen P, Backes WH, van Marken Lichtenbelt WD. Imaging cold-activated brown adipose tissue using dynamic T2*-weighted magnetic resonance imaging and 2-deoxy-2-[18F]fluoro-D-glucose positron emission tomography. Invest Radiol 2013; 48: 708-14; PMID: 23695084; http: //dx. doi. org/10. 1097/RLI. 0b013e31829363b8
29. Yoneshiro T, Aita S, Matsushita M, Kayahara T, Kameya T, Kawai Y, Iwanaga T, Saito M. Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest 2013; 123: 3404-8; PMID: 23867622; http: //dx. doi. org/10. 1172/JCI67803
30. Blondin DP, Labbe SM, Tingelstad HC, Noll C, Kunach M, Phoneix S, Guerin B, Turcotte EE, Carpentier AC, Richard D, et al. Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J Clin Endocrinol Metab 2014; 99: E438-46; PMID: 24423363
31. van der Veen DR, Shao J, Chapman S, Leevy WM, Duffield GE. A diurnal rhythm in glucose uptake in brown adipose tissue revealed by in vivo PETFDG imaging. Obesity (Silver Spring) 2012; 20: 1527-9; PMID: 22447290; http: //dx. doi. org/ 10. 1038/oby. 2012. 78
32. Baba S, Tatsumi M, Ishimori T, Lilien DL, Engles JM, Wahl RL. Effect of nicotine and ephedrine on the accumulation of 18F-FDG in brown adipose tissue. J Nucl Med 2007; 48: 981-6; PMID: 17504863; http: //dx. doi. org/10. 2967/jnumed. 106. 039065
33. Tatsumi M, Engles JM, Ishimori T, Nicely O'B, Cohade C, Wahl RL. Intense 18F-FDG uptake in brown fat can be reduced pharmacologically. J Nucl Med 2004; 45: 1189-93; PMID: 15235065
34. Gelfand MJ, O'Hara SM, Curtwright LA, MacLean JR. Pre-medication to block [18F]FDG uptake in the brown adipose tissue of pediatric and adolescent patients. Pediatr Radiol 2005; 35: 984-90; PMID: 15988582; http: //dx. doi. org/10. 1007/s00247-005-1505-8
35. Parysow O, Mollerach AM, Jager V, Racioppi S, Roman JS, Gerbaudo VH. Oral propranolol could reduce brown adipose tissue F-18 FDG uptake in patients undergoing PET scans. Clin Nucl Med 2007; 32: 351-7; PMID: 17452860; http: //dx. doi. org/ 10. 1097/01. rlu. 0000259570. 69163. 04
36. Soderlund V, Larsson SA, Jacobsson H. Reduction of FDG uptake in brown adipose tissue in clinical patients by a single dose of propranolol. Eur J Nucl Med Mol Imaging 2007; 34: 1018-22; PMID: 17225118; http: // dx. doi. org/10. 1007/s00259-006-0318-9
37. Mirbolooki MR, Constantinescu CC, Pan M-L, Mukherjee J. Targeting presynaptic norepinephrine transporter in brown adipose tissue: a novel imaging approach and potential treatment for diabetes and obesity. Synapse 2013; 67: 79-93; PMID: 23080264; http: //dx. doi. org/10. 1002/syn. 21617
38. Ohlson KB, Mohell N, Cannon B, Nedegaard J. Thermogenesis in brown adipocytes is inhibited by volatile anesthetic agents. A factor contributing to hypothermia in infants? Anesthesiology 1994; 81: 176-83; PMID: 8042786; http: //dx. doi. org/10. 1097/ 00000542-199407000-00024
39. Dicker A, Ohlson KB, Johnson L, Cannon B, Nedegaard J. Halothane selectively inhibits nonshivering thermogenesis. Possible implications for thermoregulation during anesthesia of infants. Anesthesiology 1995; 82: 491-501; PMID: 7856907; http: //dx. doi. org/ 10. 1097/00000542-199502000-00019
40. Ohlson KB, Lindahl SG, Cannon B, Nedergaard J. Thermogenesis inhibition in brown adipocytes is a specific property of volatile anesthetics. Anethesiology 2003; 98: 437-48; http: //dx. doi. org/10. 1097/ 00000542-200302000-00025
41. Cannon B, Nedegaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004; 84: 277-359; PMID: 14715917; http: //dx. doi. org/ 10. 1152/physrev. 00015. 2003
42. Chernogubova E, Cannon B, Bengtsson T. Norepienphrine increases glucose transport in brown adipocytes via beta 3-adrenoreceptors through a cAMP, PKA, and PI3-kinase-dependent pathway stimulating conventional and novel PKCs. Endocrinology 2004; 145: 269-80; PMID: 14551227; http: //dx. doi. org/ 10. 1210/en. 2003-0857
43. Kuji I, Imabayashi E, Minagawa A, Matsuda H, Miyauchi T. Brown adipose tissue demonstrating intense FDG uptake in a patient with mediastinal pheochromocytoma. Ann Nucl Med 2008; 22: 231-5; PMID: 18498040; http: //dx. doi. org/10. 1007/s12149-007-0096-x
44. Yamaga LY, Thom AF, Wagner J, Baroni RH, Hidal JT, Funari MG. The effect of catecholamines on the glucose uptake in brown adipose tissue demonstrated by 18F-FDG PET/CT in a patient with adrenal pheochromocytoma. Eur J Nucl Med Mol Imaging 2008; 35: 446-667; PMID: 17909796; http: //dx. doi. org/ 10. 1007/s00259-007-0538-7
45. Iyer RB, Guo CC, Perrier N. Adrenal pheochromocytoma with surrounding brown fat stimulation. Am J Roent 2009; 192: 300-1; http: //dx. doi. org/10. 2214/ AJR. 08. 1166
46. Sekizawa N, Yoshimoto T, Izumiyama H, Hirata Y. Distinct uptake of 18F-fluorodeoxyglucose by brown adipose tissue with a catecholamine-secreting tumor. Inter Med 2010; 49: 2363; http: //dx. doi. org/10. 2169/ internalmedicine. 49. 4293
47. Cheng W, Zhu Z, Jin X, Chen L, Zhuang H, Li F. Intense FDG activity in the brown adipose tissue in omental and mesenteric regions in a patient with malignant pheochromocytoma. Clin Nucl Med 2012; 37: 514-5; PMID: 22475909; http: //dx. doi. org/10. 1097/ RLU. 0b013e31824d2121
48. Joshi PV, Lele VR. Unexpected visitor on FDG PET/ CT-Brown adipose tissue (BAT) in mesentery in a case of retroperitoneal extra-adrenal pheochromocytoma. Clin Nucl Med 2012; 37: e119-20; PMID: 22475922; http: //dx. doi. org/10. 1097/RLU. 0b013e31824437e7
49. Dong A, Wang Y, Lu J, Zuo C. Hypermetabolic mesenteric brown adipose tissue on dual-time point FDG PET/CT in a patient with benign retroperitoneal pheochromocytoma. Clin Nucl Med 2014; 39: e229-32; PMID: 23455523; http: //dx. doi. org/10. 1097/ RLU. 0b013e3182816515
50. Wang Q, Zhang M, Ning G, GuW, Su T, Xu M, Li B, Wang W. Brown adipose tissue in humans is activated by elevated plasma catecholamine levels and is inversely related to central obesity. PLoS One 2011; 6: e21006. DOI: 10. 1371; PMID: 21701596; http: //dx. doi. org/ 10. 1371/journal. pone. 0021006
51. Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue in patients with phaeochromocytoma. Int J Obes 1986; 10: 219-27; PMID: 3019909
52. Frontini A, Vitali A, Perugini J, Murano I, Romiti C, Ricquier D, Guerrieri M, Cinti S. White-to-brown transdifferentiaition of omental adipocytes in patients affected by pheochromocytoma. Biochim Biophys Acta 2013; 1831: 950-9; PMID: 23454374; http: //dx. doi. org/10. 1016/j. bbalip. 2013. 02. 005
53. Segal SS. Regulation of blood flow in the microcirculation. Microcirculation 2005; 12: 33-45; PMID: 15804972; http: //dx. doi. org/10. 1080/10739680590895028
54. Lahesmaa M, Orava J, Schalin-Jantti C, Soinio M, Hannukainen JC, Noponen T, Kirjavainen A, Iida H, Kudomi N, Enerback S, et al. Hyperthyroidism increases brown fat metabolism in humans. J Clin Endocrinol Metab 2014; 99: E28-35; PMID: 24152690; http: //dx. doi. org/10. 1210/jc. 2013-2312
55. Quarta C, Lodi F, Mazza R, Giannone F, Boschi L, Nanni C, Nisoli E, Boschi S, Pasquali R, Fanti S, et al. 11C-meta-hydroxyephedrine PET/CT imaging allows in vivo study of adaptive thermogenesis and white-to-brown fat conversion. Mol Metab 2013; 2: 153-60; PMID: 24049730; http: // dx. doi. org/10. 1016/ j. molmet. 2013. 04. 002
56. Higuchi T, Kinuya S, Taki J, Nakajima K, Ikeda M, Namura M, Tonami N. Brown adipose tissue: Evaluation with 201Tl and 99mTc-sestamibi dual-tracer SPECT. Ann Nucl Med 2004; 18: 547-9; PMID: 15515758; http: //dx. doi. org/10. 1007/BF02984575
57. Belhocine T, Shastry A, Driedger A, Urbain J-L. Detection of 99mTc-sestamibi uptake in brown adipose tissue with SPECT-CT. Eur J Nucl Med Mol Imaging 2007; 34: 149; PMID: 17021807; http: //dx. doi. org/ 10. 1007/s00259-006-0244-x
58. Kyparos D, Arsos G, Georga S, Petridou A, Kyparos A, Papageorgiou E, Mougios V, Matziari C, Karakatsanis C. Assessment of brown adipose tissue activity in rats by 99mTc-sestamibi uptake. Physiol Res 2006; 55: 653-9; PMID: 16497107
59. Goetze S, Lavely WC, Ziessman HA, Wahl RL. Visualization of brown adipose tissue with 99mTc-methoxyisobutylisonitrile on SPECT/CT. J Nucl Med 2008; 49: 752-6; PMID: 18413387; http: //dx. doi. org/10. 2967/ jnumed. 107. 048074
60. Fukuchi K, Ono Y, Nakahata Y, Okada Y, Hayashida K, Ishida Y. Visualization of interscapular brown adipose tissue using 99mTc-tetrofosmin in pediatric patients. J Nucl Med 2003; 44: 1582-5; PMID: 14530470
61. Okuyama C, Sakane N, Yoshida T, Shima K, Kurosawa H, Kumamoto K, Ushijima Y, Nishimura T. 123Ior 125I-metaiodobenzylguanidine visualization of brown adipose tissue. J Nucl Med 2002; 43: 1234-40; PMID: 12215564
62. Gelfand MJ. 123I-MIBG uptake in the neck and shoulders of a neuroblastoma patient: damage to sympathetic innervation blocks uptake in brown adipose tissue. Pediatr Radiol 2004; 34: 577-9; PMID: 15205842; http: //dx. doi. org/10. 1007/s00247-003-1136-x
63. Admiraal WM, Holleman F, Bahler L, Soeters MR, Hoekstra JB, Verberne HJ. Combining 123I-metaiodobenzylguanidine SPECT/CT and 18F-FDG PET/CT for the assessment of brown adipose tissue activity in humans during cold exposure. J Nucl Med 2013; 54: 208-12; PMID: 23318291; http: //dx. doi. org/10. 2967/ jnumed. 112. 111849
64. Hamilton G, Smith DL, Bydder M, Nayak KS, Hu HH. MR properties of brown and white adipose tissue. J Magn Reson Imaging 2011; 34: 468-73; PMID: 21780237; http: //dx. doi. org/10. 1002/jmri. 22623
65. Sbarbarti A, Guerrni U, Marzola P, Asperio R, Osculati F. Chemical shift imaging at 4. 7 tesla of brown adipose tissue. J Lipid Res 1997; 38: 343-7; PMID: 9162753
66. Lunati E, Marzola P, Nicolato E, Fedrigo M, Sharbarti A. In vivo quantitative lipidic map of brown adipose tissue by chemical shift imaging at 4. 7 tesla. J Lipid res 1999; 40: 1395-400; PMID: 10428975
67. Hu H, Smith DL, nayak KS, Goran MI, Nagy TR. Identification of brown adipose tissue in mice with fat-water IDEAL-MRI. J Magn Reson Imaging 2010; 31: 1195-202; PMID: 20432356; http: //dx. doi. org/10. 1002/jmri. 22162
68. Smith DL, Yang Y, Hu HH, Zhai G, Nagy TR. Measurement of interscapular brown adipose tissue of mice in differentally housed temperatures by chemical-shiftencoded water-fat MRI. J Magn Reson Imaging 2013; 38: 1425-33; PMID: 23580443; http: //dx. doi. org/ 10. 1002/jmri. 24138
69. Rasmussen JM, Entringer S, Nguyen A, van Erp TGM, Guijarro A, Oveisi F, Swanson JM, Piomelli D, Wadhwa PD, Buss C, et al. Brown adipose tissue quantification in human neonates using water-fat separated MRI. PLOS One 2013; 8: e77907; PMID: 24205024; http: //dx. doi. org/10. 1371/journal. pone. 0077907
70. Hu HH, Yin L, Aggabao PC, Perkins TG, Chia JM, Gilsanz V. Comparison of brown and white adipose tissues in infants and children with chemical-shiftencoded water-fat MRI. J Magn Reson Imaging 2013; 38: 885-96; PMID: 23440739; http: //dx. doi. org/ 10. 1002/jmri. 24053
71. Hu HH, Perkins TG, Chia JM, Gilsanz V. Characterization of human brown adipose tissue by chemical-shift water-fat MRI. 2013; 200: 177-83; PMID: 23255760
72. Reddy NL, Jones TA, Wayte SC, Adesanya O, Sankar S, Yeo YC, Tripathi G, McTernan PG, Randeva HS, Kumar S, et al. Identification of brown adipsoe tissue using MR imaging in a human adult with histological and immunohistochemical confirmation. J Clin Endocrinol Metab 2014; 99: E117-21; PMID: 24384025; http: //dx. doi. org/10. 1210/jc. 2013-2036
73. Sbarbati A, Cavallini I, Marzola P, Nicolato E, Osculati F. Contrast-enhanced MRI of brown adipose tissue after pharmacological stimulation. Magn Reson Med 2006; 55: 715-8; PMID: 16506160; http: //dx. doi. org/ 10. 1002/mrm. 20851
74. Matthias A, Ohlson KB, Fredriksson JM, Jacobsson A, Nedegaard J, Cannon B. Thermogenic responses in brown fat cells are fully UCP-1dependent. UCP2 or UCP3 do not substitute for UCP1 adrenergically or fatty acid-induced thermogenesis. J Biol Chem 2000; 275: 25073-81; PMID: 10825155; http: //dx. doi. org/ 10. 1074/jbc. M000547200
75. Khanna A, Branca RT. Detecting brown adipose tissue activity with BOLD MRI in mice. Magn Reson Med 2012; 68: 1285-90; PMID: 22231619; http: //dx. doi. org/10. 1002/mrm. 24118
76. Chen Y-C I, Cypess AM, Chen Y-C, Palmer M, Kolodny G, Kahn CR, Kwong KK. Measurement of human brown adipose tissue volume and activity using anatomic MR imaging and functional MR imaging. J Nucl Med 2013; 54: 1584-7; PMID: 23868958; http: // dx. doi. org/10. 2967/jnumed. 112. 117275
77. Lau AZ, Chen AP, Ladouceur-Wodzak M, Nayak KS, Cunningham CH. Noninvasive identification and assessment of functional brown adipose tissue in rodents using hyperpolarized 13C imaging. Int J Obes 2013; 1-6; http: //dx. doi. org/10. 1155/2013/359763
78. Ma SWY, 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: 609-14; PMID: 3730946; http: //dx. doi. org/10. 1139/y86-101
79. Sjogren M, Alkemade A, Mittag J, Nordstrom K, Katz A, Rozell B, Westerblad H, Arner A, Vennstrom B. Hypermetabolism in mice caused by the central action of an unliganded thyroid hormone receptor alpha1. EMBO J 2007; 26: 4535-45; PMID: 17932484; http: // dx. doi. org/10. 1038/sj. emboj. 7601882
80. Warner A, Rahman A, Solsjo P, Gottschling K, Davis B, Vennstrom B, Arner A, Mittag J. Inappropriate heat dissipation ignites brown fat thermogenesis in mice with a mutant thyroid hormone receptor a1. Proc Natl Acad Sci USA 2013; 110: 16241-6; PMID: 24046370; http: //dx. doi. org/10. 1073/pnas. 1310300110
81. Lee SJ, Pfluger PT, Kim JY, Nogueiras R, Duran A, Pages G, Pouyssegur J, Tschop MH, Diaz-Meco MT, Moscat J. A functional role for the p62-ERK1 axis in the control of energy homeostasis and adipogenesis. EMBO Rep 2010; 11: 226-32; PMID: 20154642; http: //dx. doi. org/10. 1038/embor. 2010. 7
82. Carter EA, Bonab AA, Paul K, Yerxa J, Tompkins RG, Fischman AJ. Association of heat production with 18FFDG accumulation in murine brown adipose tissue after stress. J Nucl Med 2011; 52: 1616-20; PMID: 21914754; http: //dx. doi. org/10. 2967/jnumed. 111. 090175
83. Symonds ME, Henderson K, Elvidge L, Bosman C, Sharkey D, Perkins AC, Budge H. 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; PMID: 22677567; http: //dx. doi. org/10. 1016/j. jpeds. 2012. 04. 056
84. Robinson L, Ojha S, Symonds ME, Budge H. Body mass index as a determinant of brown adipose tissue in healthy children. J Pediatr 2014; 164: 318-22; PMID: 24238856; http: //dx. doi. org/10. 1016/j. jpeds. 2013. 10. 005
85. Kim MS, Hu HH, Aggabao PC, Geffner ME, Gilsanz V. Presence of brown adipose tissue in an adolescent with severe primary hypothyroidism. J Clin Endocrinol Metab 2014; http: //dx. doi. org/10. 1210/jc. 2014-1343
86. Murakami M, Kamiya Y, Morimura T, Araki O, Imamura M, Ogiwara T, Mizuma H, Mori M. Thyrotropin receptors in brown adipose tissue: thyrotropin stimulates type II iodothyronine deiodinase and uncoupling protein-1 in brown adipocytes. Endocrinology 2001; 142: 1195-201; PMID: 11181535
87. Baron DM, Clerte M, Brouckaert P, Raher MJ, Flynn AW, Zhang H, Carter EA, Picard MH, Block KD, buys ES, et al. in vivo characterization of brown adipose tissue blood flow by contrast ultrasound inmice. Circ Cardiovasc Imaging 2012; 5: 652-9; PMID: 22776888; http: //dx. doi. org/10. 1161/CIRCIMAGING. 112. 975607
88. Clerte M, Baron DM, Brouckaert P, Ernande L, Raher MJ, Flynn AW, PicardMH, Bloch KD, Buys ES, Scherrer-Crosbie M. Brown adipose tissue blood flow and mass in obesity: a contrast ultrasound study in mice. J Am Soc Echocardiogr 2013; 26: 1465-73; PMID: 23993691; http: //dx. doi. org/10. 1016/j. echo. 2013. 07. 015