White, brown, beige/brite: Different adipose cells for different functions?

Endocrinology

Volumn 154, Issue 9, 2013, Pages 2992-3000

  Giralt, Marta ^b   Villarroya, Francesc ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

TRIACYLGLYCEROL; UNCOUPLING PROTEIN 1;

ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE CELL; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINEAGE; CELL TRANSDIFFERENTIATION; COLD EXPOSURE; ENERGY EXPENDITURE; HUMAN; LIPID OXIDATION; MESENCHYMAL STEM CELL; MITOCHONDRIAL RESPIRATION; NONHUMAN; OBESITY; PHENOTYPE; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; RADIODIAGNOSIS; REVIEW; THERMOGENESIS; WHITE ADIPOSE TISSUE;

ADIPOCYTES, BROWN; ADIPOCYTES, WHITE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; HUMANS; OBESITY; THERMOGENESIS;

EID: 84883145789     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1403     Document Type: Review

References (87)

1. Cannon B, Nedergaard J. Brown adipose tissue: function and physiological significance. Physiol Rev. 2004;84:277-359.
2. Whittle AJ, López M, Vidal-Puig A. Using brown adipose tissue to treat obesity-the central issue. Trends Mol Med. 2011;17:405-411.
3. Wu J, Cohen P, Spiegelman BM. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev. 2013;27:234-250.
4. Townsend KL, Tseng YH. Brown adipose tissue: recent insights into development, metabolic function and therapeutic potential. Adipocyte. 2012;1:13-24.
5. Frontini A, Cinti S. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 2010; 11:253-256.
6. Cinti S. The adipose organ at a glance. Dis Model Mech. 2012;5: 588-594.
7. Farmer SR. Transcriptional control of adipocyte formation. Cell Metab. 2006;4:263-273.
8. Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: tracking obesity to its source. Cell 2007;131:242-256.
9. Barak Y, NelsonMC,Ong ES, et al. PPARγ is required for placental, cardiac, and adipose tissue development. Mol Cell. 1999;4:585-595.
10. Rosen ED, Sarraf P, Troy AE, et al. PPARγ is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell. 1999; 4:611-617.
11. Linhart HG, Ishimura-Oka K, DeMayo F, et al. C/EBPα is required for differentiation of white, but not brown, adipose tissue. Proc Natl Acad Sci USA. 2001;98:12532-12537.
12. CarmonaMC,Iglesias R, Obregón MJ, Darlington GJ, Villarroya F, Giralt M. Mitochondrial biogenesis and thyroid status maturation in brown fat require CCAAT/enhancer-binding protein α. J Biol Chem. 2002;277:21489-21498.
13. Seale P, Kajimura S, Yang W, et al. Transcriptional control of brown fat determination by PRDM16. Cell Metab. 2007;6:38-54.
14. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998;92:829-839.
15. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, Spiegelman BM. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 2006;3:333-341.
16. Seale P, Bjork B, Yang W, et al. PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008;454:961-967.
17. Kajimura S, Seale P, Kubota K, et al. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-β transcriptional complex. Nature. 2009;460:1154-1158.
18. Hondares E, Rosell M, Díaz-Delfín J, et al. Peroxisome proliferatoractivated receptor α (PPARα) induces PPARα coactivator 1α (PGC-1α) gene expression and contributes to thermogenic activation of brown fat: involvement of PRDM16. J Biol Chem. 2011;286: 43112-43122.
19. Barbera MJ, Schluter A, Pedraza N, Iglesias R, Villarroya F, Giralt M. Peroxisome proliferator-activated receptor alpha activates transcription of the brown fat uncoupling protein-1 gene.Alink between regulation of the thermogenic and lipid oxidation pathways in the brown fat cell. J Biol Chem. 2001;276:1486-1493.
20. Siersbæk MS, Loft A, AagaardMM,et al. Genome-wide profiling of peroxisome proliferator-activated receptor γ in primary epididymal, inguinal, and brown adipocytes reveals depot-selective binding correlated with gene expression. Mol Cell Biol. 2012;32:3452-3463.
21. Rajakumari S, Wu J, Ishibashi J, et al. EBF2 determines and maintains brown adipocyte identity. Cell Metab. 2013;17:562-574.
22. Villanueva CJ, Vergnes L, Wang J, et al. Adipose subtype-selective recruitment of TLE3 or Prdm16 by PPARγ specifies lipid storage versus thermogenic gene programs. Cell Metab. 2013;17:423-435.
23. Young P, Arch JR, Ashwell M. Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett. 1984;167:10-14.
24. Cousin B, Cinti S, Morroni M, et al. Occurrence of brown adipocytes in rat white adipose tissue: molecular and morphological characterization. J Cell Sci. 1992;103:931-942.
25. Timmons JA, Wennmalm K, Larsson O, et al. Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages. Proc Natl Acad Sci USA. 2007;104: 4401-4406.
26. Ishibashi J, Seale P. Medicine. Beige can be slimming. Science. 2010; 328:1113-1114.
27. Petrovic N, Walden TB, Shabalina IG, Timmons JA, Cannon B, Nedergaard J. Chronic peroxisome proliferator-activated receptorγ (PPARγ) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J Biol Chem. 2010;285:7153-7164.
28. 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.
29. Tseng YH, Kokkotou E, Schulz TJ, et al. New role of bone mor-phogenetic protein 7 in brown adipogenesis and energy expenditure. Nature. 2008;454:1000-1004.
30. Barbatelli G, Murano I, Madsen L, et al. The emergence of cold-induced brown adipocytes in mouse white fat depots is determined predominantly by white to brown adipocyte transdifferentiation. Am J Physiol Endocrinol Metab. 2010;298:E1244-E1153.
31. Barbatelli G, Morroni M, Vinesi P, Cinti S, Michetti F. S-100 protein in rat brown adipose tissue under different functional conditions: a morphological, immunocytochemical, and immunochemical study. Exp Cell Res. 1993;208:226-231.
32. Himms-Hagen J, Melnyk A, Zingaretti MC, Ceresi E, Barbatelli G, Cinti S. Multilocular fat cells in WAT of CL-316243-treated rats derive directly from white adipocytes. Am J Physiol Cell Physiol. 2000;279:C670-C681.
33. Rosenwald M, Perdikari A, Rülicke T, Wolfrum C. Bi-directional interconversion of brite and white adipocytes. Nat Cell Biol. 2013; 15:659-667.
34. Lee YH, Petkova AP, Mottillo EP, Granneman JG. In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metab. 2012;15:480-491.
35. Sanchez-Gurmaches J,HungCM,Sparks CA, Tang Y, Li H, Guertin DA.PTENloss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metab. 2012;16:348-362.
36. Schulz TJ, Huang P, Huang TL, et al. Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature. 2013;495:379-383.
37. Bukowiecki L, Collet AJ, Follea N,GuayG, Jahjah L.Brownadipose tissue hyperplasia: a fundamental mechanism of adaptation to cold and hyperphagia. Am J Physiol. 1982;242:E353-E359.
38. Bukowiecki LJ, Géloën A, Collet AJ. Proliferation and differentiation of brown adipocytes from interstitial cells during cold acclimation. Am J Physiol. 1986;250:C880-C887.
39. Nedergaard J, Cannon B. UCP1 mRNA does not produce heat. Biochim Biophys Acta. 2013;1831:943-949.
40. Waldén TB, Hansen IR, Timmons JA, Cannon B, Nedergaard J. Recruited vs. nonrecruited molecular signatures of brown, "brite," and white adipose tissues. Am J Physiol Endocrinol Metab. 2012; 302:E19-E31.
41. Sharp LZ, Shinoda K, Ohno H, et al. Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS One. 2012; 7:e49452.
42. Mitchell JR, Jacobsson A, Kirchgessner TG, Schotz MC, Cannon B, Nedergaard J. Regulation of expression of the lipoprotein lipase gene in brown adipose tissue. Am J Physiol. 1992;263:E500-E506.
43. Bartelt A, Bruns OT, Reimer R, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011;17:200-205.
44. Nedergaard J, Bengtsson T, Cannon B. New powers of brown fat: fighting the metabolic syndrome. Cell Metab. 2011;13:238-240.
45. Guerra C, Koza RA, Yamashita H, Walsh K, Kozak LP. Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J Clin Invest. 1998;102:412-420.
46. Xue B, Rim JS, Hogan JC, Coulter AA, Koza RA, Kozak LP. Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. J Lipid Res. 2007;48:41-51.
47. López-Soriano FJ, Fernández-López JA, Mampel T, Villarroya F, Iglesias R, AlemanyM.Amino acid and glucose uptake by rat brown adipose tissue. Effect of cold-exposure and acclimation. Biochem J. 1988;252:843-849.
48. Cawthorne MA. Does brown adipose tissue have a role to play in glucose homeostasis? Proc Nutr Soc. 1989;48:207-214.
49. Mory G, Bouillaud F, Combes-George M, Ricquier D. Noradrenaline controls the concentration of the uncoupling protein in brown adipose tissue. FEBS Lett. 1984;166:393-396.
50. Ghorbani M, Claus TH, Himms-Hagen J. Hypertrophy of brown adipocytes in brown and white adipose tissues and reversal of dietinduced obesity in rats treated with a β3-adrenoceptor agonist. Biochem Pharmacol. 1997;54:121-131.
51. Yen M, Ewald MB. Toxicity of weight loss agents. J Med Toxicol. 2012;8:145-152.
52. Fukui Y, Masui S, Osada S, Umesono K, Motojima K. A new thiazolidinedione, NC-2100, which is a weak PPAR-γ activator, exhibits potent antidiabetic effects and induces uncoupling protein 1 in white adipose tissue of KKAγ obese mice. Diabetes. 2000;49:759-767.
53. Pardo R, Enguix N, Lasheras J, Feliu JE, Kralli A, Villena JA. Rosiglitazone-induced mitochondrial biogenesis in white adipose tissue is independent of peroxisome proliferator-activated receptor γ coactivator-1α. PLoS One. 2011;6:e26989.
54. Ohno H, Shinoda K, Spiegelman BM, Kajimura S. PPARγ agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab. 2012;15:395-404.
55. Sell H, Berger JP, Samson P, Castriota G, Lalonde J, Deshaies Y, Richard D. Peroxisome proliferator-activated receptor γ agonism increases the capacity for sympathetically mediated thermogenesis in lean and ob/ob mice. Endocrinology. 2004;145:3925-3934.
56. Villarroya F, Vidal-Puig A. Beyond the sympathetic tone: the new brown fat activators. Cell Metab. 2013;17:638-643.
57. Hondares E, Rosell M, Gonzalez FJ, Giralt M, Iglesias R, Villarroya F. Hepatic FGF21 expression is induced at birth via PPARγ in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab. 2010;11:206-212.
58. Fisher FM, Kleiner S, Douris N, et al. FGF21 regulates PGC-1α and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 2012;26:271-281.
59. BordicchiaM,Liu D, Amri EZ, et al. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes. J Clin Invest. 2012;122:1022-1036.
60. Boström P, Wu J, Jedrychowski MP, et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481:463-468.
61. Vegiopoulos A, Müller-Decker K, Strzoda D, et al. Cyclooxygenase-2 controls energy homeostasis in mice by de novo recruitment of brown adipocytes. Science. 2010;328:1158-1161.
62. Whittle AJ, Carobbio S, Martins L, et al. BMP8B increases brown adipose tissue thermogenesis through both central and peripheral actions. Cell. 2012;149:871-885.
63. Lean ME. Brown adipose tissue in humans. Proc Nutr Soc. 1989; 48:243-256.
64. Enerbäck S. Human brown adipose tissue. Cell Metab. 2010;11: 248-252.
65. Nedergaard J, Bengtsson T, Cannon B. Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2007;293:E444-E452.
66. van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360:1500-1508.
67. Virtanen KA, Lidell ME, Orava J, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518-1525.
68. Cypess AM, Lehman S, Williams G, et al. Identification and importance of brown adipose tissue in adult humans.NEngl J Med. 2009; 360:1509-1517.
69. Heaton JM. The distribution of brown adipose tissue in the human. J Anat. 1972;112:35-39.
70. Zingaretti MC, Crosta F, Vitali A, et al. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009; 23:3113-3120.
71. 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.
72. 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.
73. Söderlund 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;34:1018-1022.
74. Carey AL, Formosa MF, Van Every B, et al. Ephedrine activates brown adipose tissue in lean but not obese humans. Diabetologia. 2013;56:147-155.
75. Vosselman MJ, van der Lans AA, Brans B, et al. Systemic β-adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes. 2012;61:3106-3113.
76. Cypess AM, Chen YC, Sze C, et al. Cold but not sympathomimetics activates human brown adipose tissue in vivo. Proc Natl Acad Sci USA. 2012;109:10001-10005.
77. Lee P, Swarbrick MM, Ho KK. Brown adipose tissue in adult humans: a metabolic renaissance. Endocr Rev. 2013;34:413-438.
78. Vijgen GH, Bouvy ND, Teule GJ, et al. Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab. 2012;97:E1229-E1233.
79. Ricquier D, Nechad M, Mory G. Ultrastructural and biochemical characterization of human brown adipose tissue in pheochromocytoma. J Clin Endocrinol Metab. 1982;54:803-807.
80. Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue in patients with phaeochromocytoma. Int J Obes. 1986;10:219-227.
81. Bouillaud F, Villarroya F, Hentz E, Raimbault S, Cassard AM, Ricquier D. Detection of brown adipose tissue uncoupling protein mRNAin adult patients by a human genomic probe. Clin Sci (Lond). 1988;75:21-27.
82. Lidell ME, Betz MJ, Leinhard OD, et al. Evidence for two types of brown adipose tissue in humans. Nat Med. 2013;19:631-634.
83. Cypess AM, White AP, Vernochet C, et al. Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat Med. 2013;19:635-639.
84. Jespersen NZ, Larsen TJ, Peijs L, et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab. 2013;17:798-805.
85. Hondares E, Iglesias R, Giralt A, et al. Thermogenic activation induces FGF21 expression and release in brown adipose tissue. J Biol Chem. 2011;286:12983-12990.
86. Gunawardana SC, PistonDW.Reversal of type 1 diabetes in mice by brown adipose tissue transplant. Diabetes. 2012;61:674-682.
87. Stanford KI, Middelbeek RJ, Townsend KL, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013;123:215-223.