Abstract
Brown adipose tissue activation occurs most effectively by cold exposure. In the modern world, we do not spend long periods in cold environment, and eating and meals may be other activators of brown fat function. Short-term regulation of brown fat functional activity by eating involves most importantly insulin. Insulin is capable to increase glucose uptake in human brown adipose tissue fivefold to fasting conditions. Oxidative metabolism in brown fat is doubled both by cold and by a meal. Human brown adipose tissue is an insulin-sensitive tissue type, and insulin resistance impairs the function, as is found in obesity. Body weight reduction improves cold-induced activation of human brown adipose tissue.
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Blessing W, Mohammed M, Ootsuka Y (2012) Heating and eating: brown adipose tissue thermogenesis precedes food ingestion as part of the ultradian basic rest-activity cycle in rats. Physiol Behav 105(4):966–974. https://doi.org/10.1016/j.physbeh.2011.11.009
Blondin DP, Labbé SM, Tingelstad HC, Noll C, Kunach M, Phoenix S, Guérin B, Turcotte EE, Carpentier AC, Richard D, Haman F (2014) Increased brown adipose tissue oxidative capacity in cold-acclimated humans. J Clin Endocrinol Metab 99(3):E438–E446. https://doi.org/10.1210/jc.2013-3901
Blondin DP, Tingelstad HC, Noll C, Frisch F, Phoenix S, Guérin B, Turcotte ÉE, Richard D, Haman F, Carpentier AC (2017a) Dietary fatty acid metabolism of brown adipose tissue in cold-acclimated men. Nat Commun 8:14146. https://doi.org/10.1038/ncomms14146
Blondin DP, Frisch F, Phoenix S, Guérin B, Turcotte ÉE, Haman F, Richard D, Carpentier AC (2017b) Inhibition of intracellular triglyceride lipolysis suppresses cold-induced brown adipose tissue metabolism and increases shivering in humans. Cell Metab 25(2):438–447. https://doi.org/10.1016/j.cmet.2016.12.005
Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Højlund K, Gygi SP, Spiegelman BM (2012) A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481(7382):463–468. https://doi.org/10.1038/nature10777
Chondronikola M, Volpi E, Børsheim E, Porter C, Annamalai P, Enerbäck S, Lidell ME, Saraf MK, Labbe SM, Hurren NM, Yfanti C, Chao T, Andersen CR, Cesani F, Hawkins H, Sidossis LS (2014) Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes 63(12):4089–4099. https://doi.org/10.2337/db14-0746
Cohade C, Mourtzikos KA, Wahl RL (2003) “USA-Fat”: prevalence is related to ambient outdoor temperature-evaluation with 18F-FDG PET/CT. J Nucl Med 44(8):1267–1270
van der Lans AA, Hoeks J, Brans B, Vijgen GH, Visser MG, Vosselman MJ, Hansen J, Jörgensen 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(8):3395–3403. https://doi.org/10.1172/JCI68993
Hanssen MJ, Wierts R, Hoeks J, Gemmink A, Brans B, Mottaghy FM, Schrauwen P, van Marken Lichtenbelt WD (2015) Glucose uptake in human brown adipose tissue is impaired upon fasting-induced insulin resistance. Diabetologia 58(3):586–595. https://doi.org/10.1007/s00125-014-3465-8
Hany TF, Gharehpapagh E, Kamel EM, Buck A, Himms-Hagen J, von Schulthess GK (2002) Brown adipose tissue: a factor to consider in symmetrical tracer uptake in the neck and upper chest region. Eur J Nucl Med Mol Imaging 29(10):1393–1398
Himms-Hagen J (1979) Obesity may be due to a malfunctioning of brown fat. Can Med Assoc J 121(10):1361–1364
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 healthy men. N Engl J Med 360(15):1500–1508. Erratum in: N Engl J Med. 2009;360(18):1917
Muzik O, Mangner TJ, Leonard WR, Kumar A, Janisse J, Granneman JG (2013) 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat. J Nucl Med 54(4):523–531. https://doi.org/10.2967/jnumed.112.111336
Nuutila P, Koivisto VA, Knuuti J, Ruotsalainen U, Teräs M, Haaparanta M, Bergman J, Solin O, Voipio-Pulkki LM, Wegelius U et al (1992) Glucose-free fatty acid cycle operates in human heart and skeletal muscle in vivo. J Clin Invest 89(6):1767–1774
Nuutila P, Knuuti MJ, Mäki M, Laine H, Ruotsalainen U, Teräs M, Haaparanta M, Solin O, Yki-Järvinen H (1995) Gender and insulin sensitivity in the heart and in skeletal muscles. Studies using positron emission tomography. Diabetes 44(1):31–36
Oberkofler H, Dallinger G, Liu YM, Hell E, Krempler F, Patsch W (1997) Uncoupling protein gene: quantification of expression levels in adipose tissues of obese and non-obese humans. J Lipid Res 38(10):2125–2133
Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, Scheinin M, Taittonen M, Niemi T, Enerbäck S, Virtanen KA (2011) Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab 14(2):272–279. https://doi.org/10.1016/j.cmet.2011.06.012
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 (Silver Spring) 21(11):2279–2287. https://doi.org/10.1002/oby.20456
Orava J, Nummenmaa L, Noponen T, Viljanen T, Parkkola R, Nuutila P, Virtanen KA (2014) Brown adipose tissue function is accompanied by cerebral activation in lean but not in obese humans. J Cereb Blood Flow Metab 34(6):1018–1023. https://doi.org/10.1038/jcbfm.2014.50
Ouellet V, Labbé SM, Blondin DP, Phoenix S, Guérin 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(2):545–552
Parysow O, Mollerach AM, Jager V, Racioppi S, San Roman J, Gerbaudo VH (2007) Low-dose oral propranolol could reduce brown adipose tissue F-18 FDG uptake in patients undergoing PET scans. Clin Nucl Med 32(5):351–357
Pathak K, Woodman RJ, James AP, Soares MJ (2018) Fasting and glucose induced thermogenesis in response to three ambient temperatures: a randomized crossover trial in the metabolic syndrome. Eur J Clin Nutr. https://doi.org/10.1038/s41430-017-0058-x
Raiko J, Holstila M, Virtanen KA, Orava J, Saunavaara V, Niemi T, Laine J, Taittonen M, Borra RJ, Nuutila P, Parkkola R (2015) Brown adipose tissue triglyceride content is associated with decreased insulin sensitivity, independently of age and obesity. Diabetes Obes Metab 17(5):516–519. https://doi.org/10.1111/dom.12433
Rothwell NJ, Stock MJ (1979) A role for brown adipose tissue in diet-induced thermogenesis. Nature 281(5726):31–35
Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K, Kawai Y, Tsujisaki M (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58(7):1526–1531
Siegel EG, Trimble ER, Renold AE, Berthoud HR (1980) Importance of preabsorptive insulin release on oral glucose tolerance: studies in pancreatic islet transplanted rats. Gut 21(11):1002–1009
U Din M, Raiko J, Saari T, Kudomi N, Parkkola R, Nuutila P, Virtanen KA (2015) Human brown adipose tissue oxygen consumption after meal is similar to cold activated consumption. Diabetologia 58(Suppl 1):S331, 691
U Din M, Raiko J, Saari T, Kudomi N, Tolvanen T, Oikonen V, Teuho J, Sipilä HT, Savisto N, Parkkola R, Nuutila P, Virtanen KA (2016) Human brown adipose tissue [(15)O]O2 PET imaging in the presence and absence of cold stimulus. Eur J Nucl Med Mol Imaging 43(10):1878–1886. https://doi.org/10.1007/s00259-016-3364-y
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(7):E1229–E1233. https://doi.org/10.1210/jc.2012-1289
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(15):1518–1525. Erratum in: N Engl J Med. 2009;361(11):1123
Vosselman MJ, Brans B, van der Lans AA, Wierts R, van Baak MA, Mottaghy FM, Schrauwen P, van Marken Lichtenbelt WD (2013) Brown adipose tissue activity after a high-calorie meal in humans. Am J Clin Nutr 98(1):57–64. https://doi.org/10.3945/ajcn.113.059022
Williams G, Kolodny GM (2008) Method for decreasing uptake of 18F-FDG by hypermetabolic brown adipose tissue on PET. AJR Am J Roentgenol 190(5):1406–1409. https://doi.org/10.2214/AJR.07.3205
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(1):13–16
Yoneshiro T, Aita S, Matsushita M, Kayahara T, Kameya T, Kawai Y, Iwanaga T, Saito M (2013) Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest 123(8):3404–3408. https://doi.org/10.1172/JCI67803
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Virtanen, K.A. (2018). Activation of Human Brown Adipose Tissue (BAT): Focus on Nutrition and Eating. In: Pfeifer, A., Klingenspor, M., Herzig, S. (eds) Brown Adipose Tissue. Handbook of Experimental Pharmacology, vol 251. Springer, Cham. https://doi.org/10.1007/164_2018_136
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DOI: https://doi.org/10.1007/164_2018_136
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