Brown fat in humans: Consensus points and experimental guidelines

Cell Metabolism

Volumn 20, Issue 3, 2014, Pages 408-415

  Cypess, Aaron M ^a   Haft, Carol R ^b   Laughlin, Maren R ^b   Hu, Houchun H ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c CHILDREN S HOSPITAL LOS ANGELES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHYLOMICRON; FATTY ACID; FLUORODEOXYGLUCOSE F 18; TRIACYLGLYCEROL; UNCOUPLING PROTEIN 1; VERY LOW DENSITY LIPOPROTEIN;

BIOSENSOR; BODY WEIGHT; BONE STRUCTURE; BROWN ADIPOSE TISSUE; CACHEXIA; CIRCADIAN RHYTHM; COLD TOLERANCE; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONSENSUS; ENERGY BALANCE; ENERGY EXPENDITURE; ENVIRONMENTAL TEMPERATURE; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HUMAN; INSULIN RESISTANCE; NATIONAL HEALTH ORGANIZATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSICAL ACTIVITY; PHYSIOLOGICAL PROCESS; PRACTICE GUIDELINE; PRIORITY JOURNAL; RADIATION DETECTOR; REVIEW; SLEEP; STEM CELL; THERMOGENESIS; WHOLE BODY IMAGING; WORKSHOP; ANATOMY AND HISTOLOGY; ENERGY METABOLISM; HOMEOSTASIS; NECK; OBESITY; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; PROCEDURES;

ADIPOSE TISSUE, BROWN; BODY WEIGHT; ENERGY METABOLISM; FLUORODEOXYGLUCOSE F18; HOMEOSTASIS; HUMANS; NECK; OBESITY; POSITRON-EMISSION TOMOGRAPHY; THERMOGENESIS;

EID: 84928724839     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.07.025     Document Type: Review

References (55)

1. K. Arunachalam, P.R. Stauffer, P.F. Maccarini, S. Jacobsen, and F. Sterzer Characterization of a digital microwave radiometry system for noninvasive thermometry using a temperature-controlled homogeneous test load Phys. Med. Biol. 53 2008 3883 3901
2. A. Azhdarinia, A.C. Daquinag, C. Tseng, S.C. Ghosh, P. Ghosh, F. Amaya-Manzanares, E. Sevick-Muraca, and M.G. Kolonin A peptide probe for targeted brown adipose tissue imaging Nat. Commun. 4 2013 2472 10.1038/ncomms3472
3. S. Baba, H.A. Jacene, J.M. Engles, H. Honda, and R.L.C.T. Wahl CT Hounsfield units of brown adipose tissue increase with activation: preclinical and clinical studies J. Nucl. Med. 51 2010 246 250
4. E.S. Bachman, H. Dhillon, C.Y. Zhang, S. Cinti, A.C. Bianco, B.K. Kobilka, and B.B. Lowell betaAR signaling required for diet-induced thermogenesis and obesity resistance Science 297 2002 843 845
5. M. Bauwens, R. Wierts, B. van Royen, J. Bucerius, W. Backes, F. Mottaghy, and B. Brans Molecular imaging of brown adipose tissue in health and disease Eur. J. Nucl. Med. Mol. Imaging 41 2014 776 791
6. D.P. Blondin, S.M. Labbé, H.C. Tingelstad, C. Noll, M. Kunach, S. Phoenix, B. Guérin, E.E. Turcotte, A.C. Carpentier, D. Richard, and F. Haman Increased brown adipose tissue oxidative capacity in cold-acclimated humans J. Clin. Endocrinol. Metab. 99 2014 E438 E446
7. M.L. Bonet, P. Oliver, and A. Palou Pharmacological and nutritional agents promoting browning of white adipose tissue Biochim. Biophys. Acta 1831 2013 969 985
8. Branca, R.T., White, C., and Zhang, L. (2013a). Detection of brown fat mass and activity by hyperpolarized xenon MR. Proceedings of the 21st Annual Meeting ISMRM, Salt Lake City, UT, 404.
9. R.T. Branca, L. Zhang, W.S. Warren, E. Auerbach, A. Khanna, S. Degan, K. Ugurbil, and R. Maronpot In vivo noninvasive detection of brown adipose tissue through intermolecular zero-quantum MRI PLoS ONE 8 2013 e74206
10. Branca, R.T., Zhang, L., White, C., and He, T. (2013c). Detection of brown fat thermogenesis by hyperpolarized Xenon gas MR. Proceedings of the 21st Annual Meeting ISMRM, Salt Lake City, Utah, USA, 814.
11. M.A. Bredella, C.M. Gill, C.J. Rosen, A. Klibanski, and M. Torriani Positive effects of brown adipose tissue on femoral bone structure Bone 58 2014 55 58
12. E. Broeders, N.D. Bouvy, and W.D. van Marken Lichtenbelt Endogenous ways to stimulate brown adipose tissue in humans Ann. Med. 2014 10.3109/07853890. 2013.874663 Published online February 13, 1014
13. B. Cannon, and J. Nedergaard Thermogenesis challenges the adipostat hypothesis for body-weight control Proc. Nutr. Soc. 68 2009 401 407
14. K.Y. Chen, R.J. Brychta, J.D. Linderman, S. Smith, A. Courville, W. Dieckmann, P. Herscovitch, C.M. Millo, A. Remaley, P. Lee, and F.S. Celi Brown fat activation mediates cold-induced thermogenesis in adult humans in response to a mild decrease in ambient temperature J. Clin. Endocrinol. Metab. 98 2013 E1218 E1223
15. Y.C. Chen, A.M. Cypess, Y.C. Chen, M. Palmer, G. Kolodny, C.R. Kahn, and K.K. Kwong Measurement of human brown adipose tissue volume and activity using anatomic MR imaging and functional MR imaging J. Nucl. Med. 54 2013 1584 1587
16. M. Clerte, D.M. Baron, P. Brouckaert, L. Ernande, M.J. Raher, A.W. Flynn, M.H. Picard, K.D. Bloch, E.S. Buys, and M. Scherrer-Crosbie Brown adipose tissue blood flow and mass in obesity: a contrast ultrasound study in mice J. Am. Soc. Echocardiogr. 26 2013 1465 1473
17. P. Cohen, J.D. Levy, Y. Zhang, A. Frontini, D.P. Kolodin, K.J. Svensson, J.C. Lo, X. Zeng, L. Ye, and M.J. Khandekar et al. Ablation of PRDM16 and beige adipose causes metabolic dysfunction and a subcutaneous to visceral fat switch Cell 156 2014 304 316
18. A.M. Cypess, A.P. White, C. Vernochet, T.J. Schulz, R. Xue, C.A. Sass, T.L. Huang, C. Roberts-Toler, L.S. Weiner, and C. Sze et al. Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat Nat. Med. 19 2013 635 639
19. G. Hamilton, D.L. Smith Jr., M. Bydder, K.S. Nayak, and H.H. Hu MR properties of brown and white adipose tissues J. Magn. Reson. Imaging 34 2011 468 473
20. M. Harms, and P. Seale Brown and beige fat: development, function and therapeutic potential Nat. Med. 19 2013 1252 1263
21. A.G. Hindle, and S.L. Martin Intrinsic circannual regulation of brown adipose tissue form and function in tune with hibernation Am. J. Physiol. Endocrinol. Metab. 306 2014 E284 E299
22. H.H. Hu, and H.E. Kan Quantitative proton MR techniques for measuring fat NMR Biomed. 26 2013 1609 1629
23. H.H. Hu, S.A. Chung, K.S. Nayak, H.A. Jackson, and V. Gilsanz Differential computed tomographic attenuation of metabolically active and inactive adipose tissues: preliminary findings J. Comput. Assist. Tomogr. 35 2011 65 71
24. P. Huttunen, J. Hirvonen, and V. Kinnula The occurrence of brown adipose tissue in outdoor workers Eur. J. Appl. Physiol. Occup. Physiol. 46 1981 339 345
25. N.Z. Jespersen, T.J. Larsen, L. Peijs, S. Daugaard, P. Homøe, A. Loft, J. de Jong, N. Mathur, B. Cannon, and J. Nedergaard et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans Cell Metab. 17 2013 798 805
26. S. Kajimura, and M. Saito A new era in brown adipose tissue biology: molecular control of brown fat development and energy homeostasis Annu. Rev. Physiol. 76 2014 225 249
27. A. Khanna, and R.T. Branca Detecting brown adipose tissue activity with BOLD MRI in mice Magn. Reson. Med. 68 2012 1285 1290
28. A.Z. Lau, A.P. Chen, Y. Gu, M. Ladouceur-Wodzak, K.S. Nayak, and C.H. Cunningham Noninvasive identification and assessment of functional brown adipose tissue in rodents using hyperpolarized 13C imaging Int. J. Obes. (Lond.) 38 2014 126 131
29. P. Lee, M.M. Swarbrick, J.T. Zhao, and K.K.Y. Ho Inducible brown adipogenesis of supraclavicular fat in adult humans Endocrinology 152 2011 3597 3602
30. P. Lee, C.D. Werner, E. Kebebew, and F.S. Celi Functional thermogenic beige adipogenesis is inducible in human neck fat Int. J. Obes. (Lond.) 38 2014 170 176
31. P. Lee, J.D. Linderman, S. Smith, R.J. Brychta, J. Wang, C. Idelson, R.M. Perron, C.D. Werner, G.Q. Phan, and U.S. Kammula et al. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans Cell Metab. 19 2014 302 309
32. S.F. Lin, X. Fan, C.W. Yeckel, D. Weinzimmer, T. Mulnix, J.D. Gallezot, R.E. Carson, R.S. Sherwin, and Y.S. Ding Ex vivo and in vivo evaluation of the norepinephrine transporter ligand [11C]MRB for brown adipose tissue imaging Nucl. Med. Biol. 39 2012 1081 1086
33. I. Madar, T. Isoda, P. Finley, J. Angle, and R. Wahl 18F- fluorobenzyl triphenyl phosphonium: a noninvasive sensor of brown adipose tissue thermogenesis J. Nucl. Med. 52 2011 808 814
34. M.R. Mirbolooki, S.K. Upadhyay, C.C. Constantinescu, M.L. Pan, and J. Mukherjee Adrenergic pathway activation enhances brown adipose tissue metabolism: a [18F]FDG PET/CT study in mice Nucl. Med. Biol. 41 2014 10 16
35. O. Muzik, T.J. Mangner, W.R. Leonard, A. Kumar, J. Janisse, and J.G. Granneman 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat J. Nucl. Med. 54 2013 523 531
36. J. Nedergaard, T. Bengtsson, and B. Cannon Unexpected evidence for active brown adipose tissue in adult humans Am. J. Physiol. Endocrinol. Metab. 293 2007 E444 E452
37. J. Orava, P. Nuutila, M.E. Lidell, V. Oikonen, T. Noponen, T. Viljanen, M. Scheinin, M. Taittonen, T. Niemi, S. Enerbäck, and K.A. Virtanen Different metabolic responses of human brown adipose tissue to activation by cold and insulin Cell Metab. 14 2011 272 279
38. J. Orava, P. Nuutila, T. Noponen, R. Parkkola, T. Viljanen, S. Enerbäck, A. Rissanen, K.H. Pietiläinen, and K.A. Virtanen Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans Obesity (Silver Spring) 21 2013 2279 2287
39. V. Ouellet, S.M. Labbé, D.P. Blondin, S. Phoenix, B. Guérin, F. Haman, E.E. Turcotte, D. Richard, and A.C. Carpentier Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans J. Clin. Invest. 122 2012 545 552
40. V. Peirce, and A. Vidal-Puig Regulation of glucose homoeostasis by brown adipose tissue Lancet Diabetes Endocrinol. 1 2013 353 360
41. S. Ponrartana, H.H. Hu, and V. Gilsanz On the relevance of brown adipose tissue in children Ann. N Y Acad. Sci. 1302 2013 24 29
42. D.B. Rodrigues, P.F. Maccarini, S. Salahi, E. Colebeck, E. Topsakal, P.J. Pereira, P. Limão-Vieira, and P.R. Stauffer Numerical 3D modeling of heat transfer in human tissues for microwave radiometry monitoring of brown fat metabolism Proc. SPIE 8584 2013 8584
43. T.J. Schulz, and Y.H. Tseng Brown adipose tissue: development, metabolism and beyond Biochem. J. 453 2013 167 178
44. L.Z. Sharp, K. Shinoda, H. Ohno, D.W. Scheel, E. Tomoda, L. Ruiz, H. Hu, L. Wang, Z. Pavlova, V. Gilsanz, and S. Kajimura Human BAT possesses molecular signatures that resemble beige/brite cells PLoS ONE 7 2012 e49452
45. M.C. Skarulis, F.S. Celi, E. Mueller, M. Zemskova, R. Malek, L. Hugendubler, C. Cochran, J. Solomon, C. Chen, and P. Gorden Thyroid hormone induced brown adipose tissue and amelioration of diabetes in a patient with extreme insulin resistance J. Clin. Endocrinol. Metab. 95 2010 256 262
46. M.E. Symonds, K. Henderson, L. Elvidge, C. Bosman, D. Sharkey, A.C. Perkins, and H. Budge 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. 161 2012 892 898
47. E. Szentirmai, and L. Kapás Intact brown adipose tissue thermogenesis is required for restorative sleep responses after sleep loss Eur. J. Neurosci. 39 2014 984 998
48. A.A. van der Lans, J. Hoeks, B. Brans, G.H. Vijgen, M.G. Visser, M.J. Vosselman, J. Hansen, J.A. Jörgensen, J. Wu, and F.M. Mottaghy et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis J. Clin. Invest. 123 2013 3395 3403
49. A.A. van der Lans, R. Wierts, M.J. Vosselman, P. Schrauwen, B. Brans, and W.D. van Marken Lichtenbelt Cold-activated brown adipose tissue in human adults - methodological issues Am. J. Physiol. Regul. Integr. Comp. Physiol. 2014 10.1152/ajpregu.00021.2014
50. B.D. van Rooijen, A.A. van der Lans, B. Brans, J.E. Wildberger, F.M. Mottaghy, P. Schrauwen, W.H. Backes, and W.D. van Marken Lichtenbelt 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. 48 2013 708 714
51. J. Villarroya, R. Cereijo, and F. Villarroya An endocrine role for brown adipose tissue? Am. J. Physiol. Endocrinol. Metab. 305 2013 E567 E572
52. K.A. Virtanen, M.E. Lidell, J. Orava, M. Heglind, R. Westergren, T. Niemi, M. Taittonen, J. Laine, N.J. Savisto, S. Enerbäck, and P. Nuutila Functional brown adipose tissue in healthy adults N. Engl. J. Med. 360 2009 1518 1525
53. J. Wu, P. Boström, L.M. Sparks, L. Ye, J.H. Choi, A.H. Giang, M. Khandekar, K.A. Virtanen, P. Nuutila, and G. Schaart et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human Cell 150 2012 366 376
54. T. Yoneshiro, S. Aita, M. Matsushita, T. Kameya, K. Nakada, Y. Kawai, and M. Saito Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men Obesity (Silver Spring) 19 2011 13 16
55. P. Young, J.R. Arch, and M. Ashwell Brown adipose tissue in the parametrial fat pad of the mouse FEBS Lett. 167 1984 10 14