Temperature-acclimated brown adipose tissue modulates insulin sensitivity in humans

Diabetes

Volumn 63, Issue 11, 2014, Pages 3686-3698

  Lee, Paul ^a   Smith, Sheila ^a   Linderman, Joyce ^a   Courville, Amber B ^b   Brychta, Robert J ^a   Dieckmann, William ^b   Werner, Charlotte D ^a   Chen, Kong Y ^a   Celi, Francesco S ^a,c  

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

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; GLUCOSE; INSULIN; LEPTIN;

ADULT; ARTICLE; BROWN ADIPOSE TISSUE; COLD ACCLIMATIZATION; CONTROLLED STUDY; CROSSOVER PROCEDURE; ENERGY BALANCE; ENERGY METABOLISM; GLUCOSE METABOLISM; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; INSULIN SENSITIVITY; MALE; METABOLIC REGULATION; NORMAL HUMAN; PROTEIN EXPRESSION; SEASONAL VARIATION; TEMPERATURE ACCLIMATIZATION; ACCLIMATIZATION; ADIPOSE TISSUE; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY; PROSPECTIVE STUDY; SKELETAL MUSCLE; TEMPERATURE; THERMOGENESIS; YOUNG ADULT;

ACCLIMATIZATION; ADIPOSE TISSUE; ADIPOSE TISSUE, BROWN; ADULT; CROSS-OVER STUDIES; ENERGY METABOLISM; HUMANS; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; PROSPECTIVE STUDIES; TEMPERATURE; THERMOGENESIS; YOUNG ADULT;

EID: 84907973405     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0513     Document Type: Article

References (50)

1. Keith SW, Redden DT, Katzmarzyk PT, et al. Putative contributors to the secular increase in obesity: exploring the roads less traveled. Int J Obes (Lond) 2006;30:1585-1594
2. Lowell BB, Bachman ES. Beta-adrenergic receptors, diet-induced thermogenesis, and obesity. J Biol Chem 2003;278:29385-29388
3. Saito M. Brown adipose tissue as a regulator of energy expenditure and body fat in humans. Diabetes Metab J 2013;37:22-29
4. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev 2004;84:277-359
5. Petrovic N, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. Thermogenically competent nonadrenergic recruitment in brown preadipocytes by a PPARgamma agonist. Am J Physiol Endocrinol Metab 2008;295:E287-E296
6. Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev 2013;27:234-250
7. Stanford KI, Middelbeek RJ, Townsend KL, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest 2013;123: 215-223
8. Seale P, Bjork B, Yang W, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature 2008;454:961-967
9. Boström P, Wu J, Jedrychowski MP, et al. A PGC1-a-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 2012;481:463-468
10. Heaton JM. The distribution of brown adipose tissue in the human. J Anat 1972;112:35-39
11. Bouillaud F, Combes-George M, Ricquier D. Mitochondria of adult human brown adipose tissue contain a 32 000-Mr uncoupling protein. Biosci Rep 1983; 3:775-780
12. Tanuma Y, Tamamoto M, Ito T, Yokochi C. The occurrence of brown adipose tissue in perirenal fat in Japanese. Arch Histol Jpn 1975;38:43-70
13. Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med 2009;360:1509-1517
14. Lee P, Zhao JT, Swarbrick MM, et al. High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab 2011;96:2450-2455
15. Saito M, Okamatsu-Ogura Y, Matsushita M, et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 2009;58:1526-1531
16. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Coldactivated brown adipose tissue in healthy men. N Engl J Med 2009;360:1500-1508
17. Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med 2009;360:1518-1525
18. Lee P, Swarbrick MM, Zhao JT, Ho KK. Inducible brown adipogenesis of supraclavicular fat in adult humans. Endocrinology 2011;152:3597-3602
19. Lee P, Werner CD, Kebebew E, Celi FS. Functional thermogenic beige adipogenesis is inducible in human neck fat. Int J Obes (Lond) 2014;38:170-176
20. Ouellet V, Labbé SM, Blondin DP, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest 2012;122:545-552
21. Sharp LZ, Shinoda K, Ohno H, et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS ONE 2012;7:e49452
22. Wu J, Boström P, Sparks LM, et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012;150:366-376
23. Lee P, Swarbrick MM, Ho KK. Brown adipose tissue in adult humans: a metabolic renaissance. Endocr Rev 2013;34:413-438
24. Chen KY, Brychta RJ, Linderman JD, 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-E1223
25. van der Lans AA, Hoeks J, Brans B, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 2013;123: 3395-3403
26. Yoneshiro T, Aita S, Matsushita M, et al. Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest 2013;123:3404-3408
27. Saito M. Human brown adipose tissue: regulation and anti-obesity potential [Review]. Endocr J 2014;61:409-416
28. Lee P, Greenfield JR, Ho KK, Fulham MJ. A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 2010;299:E601-E606
29. Matsushita M, Yoneshiro T, Aita S, Kameya T, Sugie H, Saito M. Impact of brown adipose tissue on body fatness and glucose metabolism in healthy humans. Int J Obes (Lond) 2014;38:812-817
30. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 2009;9:203-209
31. Celi FS, Brychta RJ, Linderman JD, et al. Minimal changes in environmental temperature result in a significant increase in energy expenditure and changes in the hormonal homeostasis in healthy adults. Eur J Endocrinol 2010;163:863-872
32. Lee P, Linderman JD, Smith S, et al. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab 2014;19:302-309
33. Cobelli C, Dalla Man C, Toffolo G, Basu R, Vella A, Rizza R. The oral minimal model method. Diabetes 2014;63:1203-1213
34. Maia AL, Kim BW, Huang SA, Harney JW, Larsen PR. Type 2 iodothyronine deiodinase is the major source of plasma T3 in euthyroid humans. J Clin Invest 2005;115:2524-2533
35. Lee P, Brychta RJ, Linderman J, Smith S, Chen KY, Celi FS. Mild cold exposure modulates fibroblast growth factor 21 (FGF21) diurnal rhythm in humans: relationship between FGF21 levels, lipolysis, and cold-induced thermogenesis. J Clin Endocrinol Metab 2013;98:E98-E102
36. Barneda D, Frontini A, Cinti S, Christian M. Dynamic changes in lipid droplet-associated proteins in the "browning" of white adipose tissues. Biochim Biophys Acta 2013;1831:924-933
37. Celi FS. Brown adipose tissue-when it pays to be inefficient. N Engl J Med 2009;360:1553-1556
38. Skarulis MC, Celi FS, Mueller E, et al. Thyroid hormone induced brown adipose tissue and amelioration of diabetes in a patient with extreme insulin resistance. J Clin Endocrinol Metab 2010;95:256-262
39. Andersen S, Kleinschmidt K, Hvingel B, Laurberg P. Thyroid hyperactivity with high thyroglobulin in serum despite sufficient iodine intake in chronic cold adaptation in an Arctic Inuit hunter population. Eur J Endocrinol 2012;166:433-440
40. Orava J, Nuutila P, Lidell ME, et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab 2011;14:272-279
41. Holland WL, Adams AC, Brozinick JT, et al. An FGF21-adiponectin-ceramide axis controls energy expenditure and insulin action in mice. Cell Metab 2013;17: 790-797
42. Hu HH, Wu TW, Yin L, et al. MRI detection of brown adipose tissue with low fat content in newborns with hypothermia. Magn Reson Imaging 2014;32:107-117
43. Hu HH, Smith DL Jr, Nayak KS, Goran MI, Nagy TR. Identification of brown adipose tissue in mice with fat-water IDEAL-MRI. J Magn Reson Imaging 2010; 31:1195-1202
44. Ye L, Wu J, Cohen P, et al. Fat cells directly sense temperature to activate thermogenesis. Proc Natl Acad Sci U S A 2013;110:12480-12485
45. Nordström EA, Rydén M, Backlund EC, et al. A human-specific role of cell death-inducing DFFA (DNA fragmentation factor-alpha)-like effector A (CIDEA) in adipocyte lipolysis and obesity. Diabetes 2005;54:1726-1734
46. Wu L, Zhou L, Chen C, et al. Cidea controls lipid droplet fusion and lipid storage in brown and white adipose tissue. Sci China Life Sci 2014;57:107-116
47. Johnson F, Mavrogianni A, Ucci M, Vidal-Puig A, Wardle J. Could increased time spent in a thermal comfort zone contribute to population increases in obesity? Obes Rev 2011;12:543-551
48. Glucose tolerance and mortality: comparison of WHO and American Diabetes Association diagnostic criteria. The DECODE study group. European Diabetes Epidemiology Group. Diabetes Epidemiology: Collaborative analysis Of Diagnostic criteria in Europe. Lancet 1999;354:617-621
49. Seale P, Conroe HM, Estall J, et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 2011;121: 96-105
50. Rosen ED, Spiegelman BM. What we talk about when we talk about fat. Cell 2014;156:20-44