Advertisement

Activation of Human Brown Adipose Tissue (BAT): Focus on Nutrition and Eating

  • Kirsi A. VirtanenEmail author
Chapter
Part of the Handbook of Experimental Pharmacology book series (HEP, volume 251)

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.

Keywords

Cold Human brown fat Insulin PET Postprandial 

References

  1. 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.2011.11.009CrossRefPubMedGoogle Scholar
  2. 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.2013-3901CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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/ncomms14146CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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.2016.12.005CrossRefPubMedGoogle Scholar
  5. 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/nature10777CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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/db14-0746CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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):1267–1270PubMedGoogle Scholar
  8. 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/JCI68993CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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/s00125-014-3465-8CrossRefPubMedGoogle Scholar
  10. 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):1393–1398CrossRefGoogle Scholar
  11. Himms-Hagen J (1979) Obesity may be due to a malfunctioning of brown fat. Can Med Assoc J 121(10):1361–1364PubMedPubMedCentralGoogle Scholar
  12. 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):1917CrossRefGoogle Scholar
  13. 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.112.111336CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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):1767–1774CrossRefGoogle Scholar
  15. 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):31–36CrossRefGoogle Scholar
  16. 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):2125–2133PubMedGoogle Scholar
  17. 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.2011.06.012CrossRefGoogle Scholar
  18. 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.20456CrossRefGoogle Scholar
  19. 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.2014.50CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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):545–552CrossRefGoogle Scholar
  21. 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):351–357CrossRefGoogle Scholar
  22. 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
  23. 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.12433CrossRefPubMedGoogle Scholar
  24. Rothwell NJ, Stock MJ (1979) A role for brown adipose tissue in diet-induced thermogenesis. Nature 281(5726):31–35CrossRefGoogle Scholar
  25. 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):1526–1531CrossRefGoogle Scholar
  26. 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):1002–1009CrossRefGoogle Scholar
  27. 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, 691Google Scholar
  28. 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-yCrossRefPubMedPubMedCentralGoogle Scholar
  29. 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.2012-1289CrossRefPubMedGoogle Scholar
  30. 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):1123CrossRefGoogle Scholar
  31. 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.113.059022CrossRefPubMedGoogle Scholar
  32. 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.07.3205CrossRefPubMedGoogle Scholar
  33. 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):13–16CrossRefGoogle Scholar
  34. 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/JCI67803CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Turku PET CentreTurku University Hospital and University of TurkuTurkuFinland
  2. 2.Clinical Nutrition, Institute of Public Health and Clinical NutritionUniversity of Eastern Finland (UEF)KuopioFinland

Personalised recommendations