Brown adipose tissue and novel therapeutic approaches to treat metabolic disorders

Translational Research

Volumn 165, Issue 4, 2015, Pages 464-479

  Roman, Sabiniano ^a   Agil, Ahmad ^a   Peran, Macarena ^a   Alvaro Galue, Eduardo ^a   Ruiz Ojeda, Francisco J ^a   Fernández Vázquez, Gumersindo ^a   Marchal, Juan A ^a,b  

^a UNIVERSITY OF GRANADA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

18F FDG PET; 18F fluorodeoxyglucose positron emission tomography; adenosine 3', 5' cyclic monophosphate; adipocyte fatty acid binding protein; adipose derived stem cells; adrenergic receptor; ADSCs; adult stem cells; aP2; AR; ASCs; BAT; BMI; BMP; body mass index; bone morphogenic protein; brown adipose tissue; C EBP; cAMP; cAMP dependent protein kinase A; central nervous system; CNS; coactivator 1 of PPAR; computed tomography; CT; cytosine enhancer binding protein; embryogenic signaling pathway; embryonic stem cells; ESCs; FAs; fatty acids; FFAs; fibronectin type III domain containing protein 5; FNDC5; free FAs; HP; hypothalamus; MEL; melatonin; melatonin receptor; mesenchymal stem cell; MSC; MT; NE; Necdin; norepinephrine; osteogeneic key transcriptional factor; p107; peroxisome proliferator activated receptor ; PGC 1 ; PKA; PKA cAMP response element binding; PKA CREB; positive regulatory domain 16; postmitotic neuron specific growth suppressor; PPAR ; PRDM16; Rb; retinoblastoma protein; retinoblastoma like protein 1; retinoid X receptor; Runx2; RXR; SCs; SNS; SRC; stem cells; steroid receptor coactivators 1, 2 and 3; sympathetic nervous system; T2DM; TGs; triglycerides; type 2 diabetes mellitus; UCP1; uncoupling protein 1; WAT; white adipose tissue; Wnt

Indexed keywords

CATECHOLAMINE; MELATONIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ARTICLE; BROWN ADIPOCYTE; BROWN ADIPOSE TISSUE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CITRIC ACID CYCLE; HUMAN; LIPID METABOLISM; METABOLIC DISORDER; MITOCHONDRIAL MEMBRANE; NONHUMAN; NONSHIVERING THERMOGENESIS; OBESITY; PHENOTYPE; PHOTOPERIODICITY; PRIORITY JOURNAL; PROADIPOCYTE; STEM CELL; TISSUE ENGINEERING; WHITE ADIPOSE TISSUE; ANIMAL; CARDIOVASCULAR DISEASE; COMPLICATION; DIABETES MELLITUS, TYPE 2; METABOLISM; PHYSIOLOGY;

ADIPOCYTES, BROWN; ADIPOSE TISSUE, BROWN; ANIMALS; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; HUMANS; OBESITY;

EID: 84925086314     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2014.11.002     Document Type: Review

References (166)

1. L.P. Kozak, and R. Anunciado-Koza UCP1. Its involvement and utility in obesity Int J Obes 32 suppl 7 2008 S32 S38
2. B.M. Spiegelman, and J.S. Flier Obesity and the regulation of energy balance Cell 104 2001 531 543
3. D. Langin Recruitment of brown fat and conversion of white into brown adipocytes: strategies to fight the metabolic complications of obesity Biochim Biophys Acta 1801 2010 372 376
4. P. Seale, S. Kajimura, and B.M. Spiegelman Transcriptional control of brown adipocyte development and physiological function-of mice and men Genes Dev 23 2009 788 797
5. V.J. Carey, E.E. Walters, and G.A. Colditz et al. Body fat distribution and risk of non-insulin-dependent diabetes mellitus in women. The Nurses' Health Study Am J Epidemiol 145 1997 614 619
6. I. Baik, A. Ascherio, and E.B. Rimm et al. Adiposity and mortality in men Am J Epidemiol 152 2000 264 271
7. T. Pischon, H. Boeing, and K. Hoffmann et al. General and abdominal adiposity and risk of death in Europe N Engl J Med 359 2008 2105 2120
8. C. Zhang, K.M. Rexrode, R.M. van Dam, T.Y. Li, and F.B. Hu Abdominal obesity and the risk of all-cause, cardiovascular, and cancer mortality: sixteen years of follow-up in US women Circulation 117 2008 1658 1667
9. A.R. Saltiel, and C.R. Kahn Insulin signalling and the regulation of glucose and lipid metabolism Nature 414 2001 799 806
10. S.L. Wijers, W.H. Saris, and W.D. van Marken Lichtenbelt Recent advances in adaptive thermogenesis: potential implications for the treatment of obesity Obes Rev 10 2009 218 226
11. S. Gesta, Y.H. Tseng, and C.R. Kahn Developmental origin of fat: tracking obesity to its source Cell 131 2007 242 256
12. J.A. Timmons, K. Wennmalm, and O. Larsson et al. Myogenic gene expression signature establishes that brown and white adipocytes originate from distinct cell lineages Proc Natl Acad Sci U S A 104 2007 4401 4406
13. T.B. Walden, J.A. Timmons, P. Keller, J. Nedergaard, and B. Cannon Distinct expression of muscle-specific microRNAs (myomirs) in brown adipocytes J Cell Physiol 218 2009 444 449
14. R. Atit, S.K. Sgaier, and O.A. Mohamed et al. Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse Dev Biol 296 2006 164 176
15. G. Fruhbeck, P. Sesma, and M.A. Burrell PRDM16: the interconvertible adipo-myocyte switch Trends Cell Biol 19 2009 141 146
16. S. Klaus, M. Ely, D. Encke, and G. Heldmaier Functional assessment of white and brown adipocyte development and energy metabolism in cell culture. Dissociation of terminal differentiation and thermogenesis in brown adipocytes J Cell Sci 108 1995 3171 3180
17. T.J. Schulz, T.L. Huang, and T.T. Tran et al. Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat Proc Natl Acad Sci U S A 108 2011 143 148
18. M. Jastroch, K.W. Withers, and S. Taudien et al. Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis Physiol Genomics 32 2008 161 169
19. N.A. Ducharme, and P.E. Bickel Lipid droplets in lipogenesis and lipolysis Endocrinology 149 2009 942 949
20. T. Pulinilkunnil, H. He, and D. Kong et al. Adrenergic regulation of AMP-activated protein kinase in brown adipose tissue in vivo J Biol Chem 286 2011 8798 8809
21. S. Rousset, M.C. Alves-Guerra, and J. Mozo et al. The biology of mitochondrial uncoupling proteins Diabetes 53 suppl 1 2004 S130 S135
22. M. Klingenberg Uncoupling protein - a useful energy dissipator J Bioenerg Biomembr 31 1999 419 430
23. A. Bartelt, O.T. Bruns, and R. Reimer et al. Brown adipose tissue activity controls triglyceride clearance Nat Med 17 2011 200 205
24. D. Sramkova, S. Krejbichova, and J. Vcelak et al. The UCP1 gene polymorphism A-3826G in relation to DM2 and body composition in Czech population Exp Clin Endocrinol Diabetes 115 2007 303 307
25. A.H. Kissebah, and G.R. Krakower Regional adiposity and morbidity Physiol Rev 74 1994 761 811
26. S. Enerback, A. Jacobsson, and E.M. Simpson et al. Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese Nature 387 1997 90 94
27. S.A. van den Berg, W. Van Marken-Lichtenbelt, K. Willems van Dijk, and P. Schrauwen Skeletal muscle mitochondrial uncoupling, adaptive thermogenesis and energy expenditure Curr Opin Clin Nutr Metab Care 14 2011 243 249
28. P. Tontonoz, E. Hu, and B.M. Spiegelman Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor Cell 79 1994 1147 1156
29. Y. Barak, M.C. Nelson, and E.S. Ong et al. PPAR gamma is required for placental, cardiac, and adipose tissue development Mol Cell 4 1999 585 595
30. E.D. Rosen, P. Sarraf, and A.E. Troy et al. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro Mol Cell 4 1999 611 617
31. J. Nedergaard, N. Petrovic, E.M. Lindgren, A. Jacobsson, and B. Cannon PPARgamma in the control of brown adipocyte differentiation Biochim Biophys Acta 1740 2005 293 304
32. S.L. Gray, E. Dalla Nora, and E.C. Backlund et al. Decreased brown adipocyte recruitment and thermogenic capacity in mice with impaired peroxisome proliferator-activated receptor (P465L PPARgamma) function Endocrinology 147 2007 5708 5714
33. Z. Wu, E.D. Rosen, and R. Brun et al. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity Mol Cell 3 1999 151 158
34. M.I. Lefterova, Y. Zhang, and D.J. Steger et al. PPARgamma and C/EBP factors orchestrate adipocyte biology via adjacent binding on a genome-wide scale Genes Dev 22 2008 2941 2952
35. R. Nielsen, T.A. Pedersen, and D. Hagenbeek et al. Genome-wide profiling of PPARgamma: RXR and RNA polymerase II occupancy reveals temporal activation of distinct metabolic pathways and changes in RXR dimer composition during adipogenesis Genes Dev 22 2008 2953 2967
36. E. Hondares, O. Mora, and P. Yubero et al. Thiazolidinediones and rexinoids induce peroxisome proliferator-activated receptor-coactivator (PGC)-1alpha gene transcription: an autoregulatory loop controls PGC-1alpha expression in adipocytes via peroxisome proliferator-activated receptor-gamma coactivation Endocrinology 147 2006 2829 2838
37. X. Yang, and U. Smith Adipose tissue distribution and risk of metabolic disease: does thiazolidinedione-induced adipose tissue redistribution provide a clue to the answer Diabetologia 50 2007 1127 1139
38. P. Seale, S. Kajimura, and W. Yang et al. Transcriptional control of brown fat determination by PRDM16 Cell Metab 6 2007 38 54
39. H. Chen, S. Kshirsagar, I. Jensen, K. Lau, C. Simonson, and S.F. Schluter Characterization of arrangement and expression of the beta-2 microglobulin locus in the sandbar and nurse shark Dev Comp Immunol 34 2010 189 195
40. S. Ramanan, M. Kooshki, W. Zhao, F.C. Hsu, and M.E. Robbins PPARalpha ligands inhibit radiation-induced microglial inflammatory responses by negatively regulating NF-kappaB and AP-1 pathways Free Radic Biol Med 45 2008 1695 1704
41. P. Puigserver, Z. Wu, C.W. Park, R. Graves, M. Wright, and B.M. Spiegelman A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis Cell 92 1998 829 839
42. S. Herzig, F. Long, and U.S. Jhala et al. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1 Nature 413 2001 179 183
43. W. Cao, K.W. Daniel, and J. Robidoux et al. p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene Mol Cell Biol 24 2004 3057 3067
44. B. Xue, A. Coulter, J.S. Rim, R.A. Koza, and L.P. Kozak Transcriptional synergy and the regulation of Ucp1 during brown adipocyte induction in white fat depots Mol Cell Biol 25 2005 8311 8322
45. C. Wang, Z. Huang, Y. Du, Y. Cheng, S. Chen, and F. Guo ATF4 regulates lipid metabolism and thermogenesis Cell Res 20 2005 174 184
46. D. Larrouy, H. Vidal, F. Andreelli, M. Laville, and D. Langin Cloning and mRNA tissue distribution of human PPARgamma coactivator-1 Int J Obes Relat Metab Disord 23 1999 1327 1332
47. C. Tiraby, G. Tavernier, and C. Lefort et al. Acquirement of brown fat cell features by human white adipocytes J Biol Chem 278 2003 33370 33376
48. A. Mazzucotelli, N. Viguerie, and C. Tiraby et al. The transcriptional coactivator peroxisome proliferator activated receptor (PPAR)gamma coactivator-1 alpha and the nuclear receptor PPAR alpha control the expression of glycerol kinase and metabolism genes independently of PPAR gamma activation in human white adipocytes Diabetes 56 2007 2467 2475
49. J. St-Pierre, S. Drori, and M. Uldry et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell 127 2006 397 408
50. F. Picard, M. Gehin, and J. Annicotte et al. SRC-1 and TIF2 control energy balance between white and brown adipose tissues Cell 111 2002 931 941
51. C. Lerin, J.T. Rodgers, D.E. Kalume, S.H. Kim, A. Pandey, and P. Puigserver GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1alpha Cell Metab 3 2006 429 438
52. A. Coste, J.F. Louet, and M. Lagouge et al. The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1{alpha} Proc Natl Acad Sci U S A 105 2008 17187 17192
53. J.F. Louet, and B.W. O'Malley Coregulators in adipogenesis: what could we learn from the SRC (p160) coactivator family Cell Cycle 6 2007 2448 2452
54. M.M. Del Mar Gonzalez-Barroso, D. Ricquier, and A.M. Cassard-Doulcier The human uncoupling protein-1 gene (UCP1): present status and perspectives in obesity research Obes Rev 1 2000 61 72
55. G. Leonardsson, J.H. Steel, and M. Christian et al. Nuclear receptor corepressor RIP140 regulates fat accumulation Proc Natl Acad Sci U S A 101 2004 8437 8442
56. M. Christian, E. Kiskinis, D. Debevec, G. Leonardsson, R. White, and M.G. Parker RIP140-targeted repression of gene expression in adipocytes Mol Cell Biol 25 2005 9383 9391
57. A. Seth, J.H. Steel, and D. Nichol et al. The transcriptional corepressor RIP140 regulates oxidative metabolism in skeletal muscle Cell Metab 6 2007 236 245
58. M. Hallberg, D.L. Morganstein, and E. Kiskinis et al. A functional interaction between RIP140 and PGC-1alpha regulates the expression of the lipid droplet protein CIDEA Mol Cell Biol 28 2008 6785 6795
59. J.B. Hansen, C. Jorgensen, and R.K. Petersen et al. Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation Proc Natl Acad Sci U S A 101 2004 4112 4117
60. S. Rea, F. Eisenhaber, and D. O'Carroll et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases Nature 406 2000 593 599
61. D.C. Schultz, K. Ayyanathan, D. Negorev, G.G. Maul, and F.J. Rauscher 3rd SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins Genes Dev 16 2002 919 932
62. R.C. Trievel, B.M. Beach, L.M. Dirk, R.L. Houtz, and J.H. Hurley Structure and catalytic mechanism of a SET domain protein methyltransferase Cell 111 2002 91 103
63. P. Seale, B. Bjork, and W. Yang et al. PRDM16 controls a brown fat/skeletal muscle switch Nature 454 2008 961 967
64. S. Kajimura, P. Seale, and T. Tomaru et al. Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex Genes Dev 22 2008 1397 1409
65. S. Kajimura, P. Seale, and K. Kubota et al. Initiation of myoblast to brown fat switch by a PRDM16-C/EBP-beta transcriptional complex Nature 460 2009 1154 1158
66. M.E. Lidell, E.L. Seifert, and R. Westergren et al. The adipocyte-expressed forkhead transcription factor Foxc2 regulates metabolism through altered mitochondrial function Diabetes 60 2011 427 435
67. Y.H. Tseng, E. Kokkotou, and T.J. Schulz et al. New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure Nature 454 2008 1000 1004
68. P. Ducy, R. Zhang, V. Geoffroy, A.L. Ridall, and G. Karsenty Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation Cell 89 1997 747 754
69. Y.H. Tseng, A.J. Butte, and E. Kokkotou et al. Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin Nat Cell Biol 7 2005 601 611
70. M. Manieri, I. Murano, A. Fianchini, A. Brunelli, and S. Cinti Morphological and immunohistochemical features of brown adipocytes and preadipocytes in a case of human hibernoma Nutr Metab Cardiovasc Dis 20 2010 567 574
71. I. Kuji, E. Imabayashi, A. Minagawa, H. Matsuda, and T. Miyauchi Brown adipose tissue demonstrating intense FDG uptake in a patient with mediastinal pheochromocytoma Ann Nucl Med 22 2008 231 235
72. A. Frontini, A. Vitali, and J. Perugini et al. White-to-brown transdifferentiation of omental adipocytes in patients affected by pheochromocytoma Biochim Biophys Acta 1831 2013 950 959
73. M.C. Zingaretti, F. Crosta, and A. Vitali 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 23 2009 3113 3120
74. W.D. van Marken Lichtenbelt, J.W. Vanhommerig, and N.M. Smulders et al. Cold-activated brown adipose tissue in healthy men N Engl J Med 360 2009 1500 1508
75. A.M. Cypess, S. Lehman, and G. Williams et al. Identification and importance of brown adipose tissue in adult humans N Engl J Med 360 2009 1509 1517
76. M.E. Lidell, and S. Enerbäck Brown adipose tissue-a new role in humans Nat Rev Endocrinol 6 2010 319 325
77. K.A. Virtanen, M.E. Lidell, and J. Orava et al. Functional brown adipose tissue in healthy adults N Engl J Med 360 2009 1518 1525
78. M.E. Lidell, M.J. Betz, and O. Dahlqvist Leinhard et al. Evidence for two types of brown adipose tissue in humans Nat Med 19 2013 631 634
79. N. Petrovic, T.B. Walden, I.G. Shabalina, J.A. Timmons, B. Cannon, and J. Nedergaard Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) 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 285 2010 7153 7164
80. J. Wu, P. Bostrom, and L.M. Sparks et al. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human Cell 150 2012 366 376
81. P. Trayhurn, and M. Ashwell Control of white and brown adipose tissues by the autonomic nervous system Proc Nutr Soc 46 1987 135 142
82. B. Cannon, and J. Nedergaard Brown adipose tissue: function and physiological significance Physiol Rev 84 2004 277 359
83. J.D. Bloom, M.D. Dutia, and B.D. Johnson et al. Disodium (R,R)-5-[2-[[2-(3-chlorophenyl)-2-hydroxyethyl]-amino] propyl]-1,benzodioxole-2,2-dicarboxylate (CL 316,243). A potent beta-adrenergic agonist virtually specific for beta 3 receptors. A promising antidiabetic and antiobesity agent J Med Chem 35 1992 3081 3084
84. B.R. Holloway, R. Howe, B.S. Rao, and D. Stribling ICI D7114: a novel selective adrenoceptor agonist of brown fat and thermogenesis Am J Clin Nutr 55 1 suppl 1992 262S 264S
85. D. Grujic, V.S. Susulic, and M.E. Harper et al. Beta3-adrenergic receptors on white and brown adipocytes mediate beta3-selective agonist-induced effects on energy expenditure, insulin secretion, and food intake. A study using transgenic and gene knockout mice J BiolChem 272 1997 17686 17693
86. A.C. Bianco, and J.E. Silva Intracellular conversion of thyroxine to triiodothyronine is required for the optimal thermogenic function of brown adipose tissue J Clin Invest 79 1997 295 300
87. M.O. Ribeiro, S.D. Carvalho, and J.J. Schultz et al. Thyroid hormone-sympathetic interaction and adaptive thermogenesis are thyroid hormone receptor isoform-specific J Clin Invest 108 2001 97 105
88. J.F. Tobin, and A.J. Celeste Bone morphogenetic proteins and growth differentiation factors as drug targets in cardiovascular and metabolic disease Drug Discov Today 11 2006 405 411
89. I. Bogacka, B. Ukropcova, M. McNeil, J.M. Gimble, and S.R. Smith Structural and functional consequences of mitochondrial biogenesis in human adipocytes in vitro J Clin Endocrinol Metab 90 2005 6650 6656
90. M.L. Bonet, P. Oliver, and A. Palou Pharmacological and nutritional agents promoting browning of white adipose tissue Biochim Biophys Acta 183 2013 969 985
91. G.H. Vijgen, N.D. Bouvy, and G.J. Teule et al. Brown adipose tissue in morbidly obese subjects PLoS One 6 2011 e17247
92. J. Orava, P. Nuutila, and T. Noponen et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans Obesity (Silver Spring) 21 2013 2279 2287
93. A.L. Carey, M.F. Formosa, and B. Van Every et al. Ephedrine activates brown adipose tissue in lean but not obese humans Diabetologia 56 2013 147 155
94. D. Langin Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome Pharmacol Res 53 2006 482 491
95. A.D. Strosberg Association of beta 3-adrenoceptor polymorphism with obesity and diabetes: current status Trends Pharmacol Sci 18 1997 449 454
96. S. Cinti The adipose organ Prostaglandins Leukot Essent Fatty Acids 73 2005 9 15
97. Q. Wang, M. Zhang, and G. Ning et al. Brown adipose tissue in humans is activated by elevated plasma catecholamines levels and is inversely related to central obesity PLoS One 6 2011 e21006
98. M.J. Vosselman, A.A. van der Lans, and B. Brans et al. Systemic β-adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans Diabetes 61 2012 3106 3113
99. C. Handschin, and B.M. Spiegelman The role of exercise and PGC-α in inflammation and chronic disease Nature 454 2008 463 469
100. T. Wenz, S.G. Rossi, R.L. Rotundo, B.M. Spiegelman, and C.T. Moraes Increased muscle PGC-1a expression protects from sarcopenia and metabolic disease during aging Proc Natl Acad Sci U S A 106 2009 20405 20410
101. P. Boström, J. Wu, and M.P. Jedrychowski et al. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis Nature 481 2012 463 468
102. M. Bordicchia, D. Liu, and E.Z. Amri et al. Cardiac natriuretic peptides act via p38 MAPK to induce the brown fat thermogenic program in mouse and human adipocytes J Clin Invest 122 2012 1022 1036
103. V. Ouellet, S.M. Labbé, and D.P. Blondin et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans J Clin Invest 122 2012 545 552
104. J.M. Moreno-Navarrete, F. Ortega, and M. Serrano et al. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance Clin Endocrinol Metab 98 2013 E769 E778
105. K.A. Iwen, O. Senyaman, and A. Schwartz et al. Melanocortin crosstalk with adipose functions: ACTH directly induces insulin resistance, promotes a pro-inflammatory adipokine profile and stimulates UCP-1 in adipocytes J Endocrinol 196 2008 465 472
106. R. Nogueiras, P. Wiedmer, and D. Perez-Tilve et al. The central melanocortin system directly controls peripheral lipid metabolism J Clin Invest 117 2007 3475 3488
107. T.J. Bartness, G.E. Demas, and C.K. Song Seasonal changes in adiposity: the roles of the photoperiod, melatonin and other hormones, and sympathetic nervous system Exp Biol Med 227 2002 363 376
108. C. Atgie, P. Sauvant, L. Ambid, and C. Carpéné Possible mechanisms of weight loss of Siberian hamsters (Phodopus sungorus sungorus) exposed to short photoperiod J Physiol Biochem 65 2009 377 386
109. L.C. Manchester, B. Poeggeler, F.L. Alvares, G.B. Ogden, and R.J. Reiter Melatonin immunoreactivity in the photosynthetic prokaryote Rhodospirillum rubrum: implications for an ancient antioxidant system Cell Mol Biol Res 41 1995 391 395
110. D.X. Tan, and L.C. Manchester Significance and application of melatonin in the regulation of brown adipose tissue metabolism: relation to human obesity Obes Rev 12 2011 167 188
111. H. Tan, C.M. Ramirez, N. Miljkovic, H. Li, J.P. Rubin, and K.G. Marra Thermosensitive injectable hyaluronic acid hydrogel for adipose tissue engineering Biomaterials 30 2009 6844 6853
112. R.J. Reiter Pineal melatonin: cell biology of its synthesis and of its physiological interactions Endocr Rev 12 1991 151 180
113. T. Wolden-Hanson, D.R. Mitton, and R.L. McCants et al. Daily melatonin administration to middle-aged male rats suppresses body weight, intraabdominal adiposity, and plasma leptin and insulin independent of food intake and total body fat Endocrinology 141 2000 487 497
114. H.A. Schmid, P.J. Requintina, G.F. Oxenkrug, and W. Sturner Calcium, calcification, and melatonin biosynthesis in the human pineal gland: a postmortem study into age-related factors J Pineal Res 16 1994 178 183
115. D.T. Glass, and G.R. Lynch Melatonin: identification of sites of antigonadal action in mouse brain Science 214 1981 821 823
116. M.L. Dubocovich, and J. Takahashi Melatonin receptors in central nervous system Proc Natl Acad Sci U S A 84 1987 3916 3920
117. R. Hardeland, B. Fuhrberg, and I. Balzer Melatonin in plants: a mechanism of action in a unicellular alga and some perspectives of its role in multicellular plants R. Hardeland, Actions and redox properties of melatonin and other aromatic amino acid metabolites 2001 Cuvillier Gottingen 70 79
118. M. Sanchez-Hidalgo, Z. Lu, D.X. Tan, M.D. Maldonado, R.J. Reiter, and R.I. Gregerman Melatonin inhibits fatty acid-induced triglyceride accumulation in ROS17/2.8 cells: implications for osteoblast differentiation and osteoporosis Am J Physiol Regul Integr Comp Physiol 292 2007 R2208 R2215
119. M.I. Alonso-Vale, S.B. Peres, C. Vernochet, S.R. Farmer, and F.B. Lima Adipocyte differentiation is inhibited by melatonin through the regulation of C/EBPbeta transcriptional activity J Pineal Res 47 2009 221 227
120. L. Zhang, P. Su, and C. Xu et al. Melatonin inhibits adipogenesis and enhances osteogenesis of human mesenchymal stem cells by suppressing PPARγ expression and enhancing Runx2 expression J Pineal Res 49 2010 364 372
121. M.I. Alonso-Vale, S. Andreotti, and S.B. Peres et al. Melatonin enhances leptin expression by rat adipocytes in the presence of insulin Am J Physiol Endocrinol Metab 288 2005 E805 E812
122. N. Mohan, K. Sadeghi, R.J. Reiter, and M.L. Meltz The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-kappa B Biochem Mol Biol Int 37 1995 1063 1070
123. G. Heldmaier, and S. Steinlechner Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopussungorus), living in natural photoperiod J Comp Physiol 142 1981 429 437
124. B. Prunet-Marcassus, L. Ambid, N. Viguerie-Bascands, L. Pénicaud, and L. Casteilla Evidence for a direct effect of melatonin on mitochondrial genome expression of Siberian hamster brown adipocytes J Pineal Res 30 2001 108 115
125. A. Agil, M. Navarro-Alarcón, R. Ruiz, S. Abuhamadah, M.Y. El-Mir, and G.F. Vázquez Beneficial effects of melatonin on obesity and lipid profile in young Zucker diabetic fatty rats J Pineal Res 50 2011 207 212
126. A. Agil, I. Rosado, R. Ruiz, A. Figueroa, N. Zen, and G. Fernández-Vázquez Melatonin improves glucose homeostasis in young Zucker diabetic fatty rats J Pineal Res 52 2011 203 210
127. A. Agil, R.J. Reiter, and A. Jiménez-Aranda et al. Melatonin ameliorates low-grade inflammation and oxidative stress in young Zucker diabetic fatty rats J Pineal Res 54 2013 381 388
128. A. Jiménez-Aranda, G. Fernández-Vázquez, and D. Campos et al. Melatonin induces browning of inguinal white adipose tissue in Zucker diabetic fatty rats J Pineal Res 55 2013 416 423
129. J.A. Martinez-Climent, E.J. Andreu, and F. Prosper Somatic stem cells and the origin of cancer Clin Transl Oncol 8 2006 647 663
130. J.A. Marchal, H. Boulaiz, and P. Macarena et al. Therapeutic potential of differentiation in cancer and normal stem cells Juan A. Marchal, Nova Science Publishers 2009 1 116 USA
131. J.A. Marchal, M. Picón, and M. Perán et al. Purification and long-term expansion of multipotent endothelial-like cells with potential cardiovascular regeneration Stem Cells Dev 21 2012 562 574
132. M. Perán, J.A. Marchal, and E. López et al. Human cardiac tissue induces transdifferentiation of adult stem cells towards cardiomyocytes Cytotyherapy 13 2011 193 200
133. M. Peran, S. Ruiz, and W. Kwiatkowski et al. Activin/BMP2 chimeric ligands direct adipose-derived stem cells to chondrogenic differentiation Stem Cell Res 10 2013 464 476
134. E. López-Ruiz, M. Perán, and J. Cobo-Molinos et al. Chondrocytes extract from patients with osteoarthritis induces chondrogenesis in infrapatellar fat pad-derived stem cells Osteoarthritis Cartilage 21 2013 246 258
135. M. Krampera, S. Marconi, and A. Pasini et al. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus Bone 40 2007 382 390
136. Y. Fukuchi, H. Nakajima, D. Sugiyama, I. Hirose, T. Kitamura, and K. Tsuji Human placenta-derived cells have mesenchymal stem/progenitor cell potential Stem Cells 22 2004 649 658
137. X. Lu, S. Alshemali, E.A. de Wynter, and A.M. Dickinson Mesenchymal stem cells from CD34 human umbilical cord blood Transfus Med 20 2010 178 184
138. M. Crisan, S. Yap, and L. Casteilla et al. A perivascular origin for mesenchymal stem cells in multiple human organs Cell Stem Cell 3 2008 301 313
139. C. Elabd, C. Chiellini, and M. Carmona et al. Human multipotent adipose-derived stem cells differentiate into functional brown adipocytes Stem Cells 27 2009 2753 2760
140. D. Garcia-Olmo, D. Herreros, and I. Pascual et al. Expanded adipose-derived stem cells for the treatment of complex perianal fistula: a phase II clinical trial Dis Colon Rectum 52 2009 79 86
141. R. Madonna, Y.J. Geng, and R. De Caterina Adipose tissue-derived stem cells: characterization and potential for cardiovascular repair Arterioscler Thromb Vasc Biol 29 2009 1723 1729
142. M. Jumabay, T. Matsumoto, and S. Yokoyama et al. Dedifferentiated fat cells convert to cardiomyocyte phenotype and repair infarcted cardiac tissue in rats J Mol Cell Cardiol 47 2009 565 575
143. R.L. Van, and D.A. Roncari Complete differentiation in vivo of implanted cultured adipocyte precursors from adult rats Cell Tissue Res 225 1982 557 566
144. B. Rieck, and S. Schlaak In vivo tracking of rat preadipocytes after autologous transplantation Ann Plast Surg 51 2003 294 300
145. K. Yagi, D. Kondo, Y. Okazaki, and K. Kano A novel preadipocyte cell line established from mouse adult mature adipocytes Biochem Biophys Res Commun 321 2004 967 974
146. A.W. Joe, L. Yi, Y. Even, A.W. Vogl, and F.M. Rossi Depot-specific differences in adipogenic progenitor abundance and proliferative response to high-fat diet Stem Cells 27 2009 2563 2570
147. E.A. Salisbury, Z.W. Lazard, E.E. Ubogu, A.R. Davis, and E.A. Olmsted-Davis Transient brown adipocyte-like cells derive from peripheral nerve progenitors in response to bone morphogenetic protein 2 Stem Cells Transl Med 1 2012 874 885
148. T. Ahfeldt, R.T. Schinzel, and Y.K. Lee et al. Programming human pluripotent stem cells into white and brown adipocytes Nat Cell Biol 14 2012 209 219
149. M. Nishio, T. Yoneshiro, and M. Nakahara et al. Production of functional classical brown adipocytes from human pluripotent stem cells using specific hemopoietin cocktail without gene transfer Cell Metab 16 2012 394 406
150. J. Smahel Experimental implantation of adipose tissue fragments Br J Plast Surg 42 1989 207 211
151. G. Dellagiacoma, A. Sbarbati, and M. Rossi et al. Brown adipose tissue: magnetic resonance imaging and ultrastructural studies after transplantation in syngeneic rats Transplant Proc 24 1992 2986
152. C.T. Gomillion, and K.J. Burg Stem cells and adipose tissue engineering Biomaterials 27 2006 6052 6063
153. S.W. Cho, K.W. Song, J.W. Rhie, M.H. Park, C.Y. Choi, and B.S. Kim Engineered adipose tissue formation enhanced by basic fibroblast growth factor and a mechanically stable environment Cell Transplant 16 2007 421 434
154. N. Torio-Padron, N. Baerlecken, A. Momeni, G.B. Stark, and J. Borges Engineering of adipose tissue by injection of human preadipocytes in fibrin Aesthetic Plast Surg 31 2007 285 293
155. M.C. Tanzi, and S. Fare Adipose tissue engineering: state of the art, recent advances and innovative approaches Expert Rev Med Devices 6 2009 533 551
156. N. Kawaguchi, K. Toriyama, E. Nicodemou-Lena, K. Inou, S. Torii, and Y. Kitagawa Reconstituted basement membrane potentiates in vivo adipogenesis of 3T3-F442A cells Cytotechnology 31 1999 215 220
157. C. Fischbach, T. Spruss, and B. Weiser et al. Generation of mature fat pads in vitro and in vivo utilizing 3-D long-term culture of 3T3-L1 preadipocytes Exp Cell Res 300 2004 54 56
158. S.C. Gunawardana, and D.W. Piston Reversal of type 1diabetes in mice by brown adipose tissue transplant Diabetes 61 2012 674 682
159. J. Mercader, A. Palou, and M.L. Bonet Induction of uncoupling protein-1 in mouse embryonic fibroblast-derived adipocytes by retinoic acid Obesity (Silver Spring) 18 2010 655 662
160. M. Scheideler, C. Elabd, and L.E. Zaragosi et al. Comparative transcriptomics of human multipotent stem cells during adipogenesis and osteoblastogenesis BMC Genomics 9 2008 340
161. M. Lamfers, S. Idema, and F. van Milligen et al. Homing properties of adipose-derived stem cells to intracerebral glioma and the effects of adenovirus infection Cancer Lett 274 2009 78 87
162. Y.S. Choi, S.N. Park, and H. Suh Adipose tissue engineering using mesenchymal stem cells attached to injectable PLGA spheres Biomaterials 26 2005 5855 5863
163. Y. Itoi, M. Takatori, H. Hyakusoku, and H. Mizuno Comparison of readily available scaffolds for adipose tissue engineering using adipose-derived stem cells J Plast Reconstr Aesthet Surg 63 2010 858 864
164. J. Rehman, D. Traktuev, and J. Li et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells Circulation 109 2004 1292 1298
165. S.H. Bhang, S.W. Cho, and J.M. Lim et al. Locally delivered growth factor enhances the angiogenic efficacy of adipose-derived stromal cells transplanted to ischemic limbs Stem Cells 27 2009 1976 1986
166. C.G. Yi, W. Xia, and L.X. Zhang et al. VEGF gene therapy for the survival of transplanted fat tissue in nude mice J Plast Reconstr Aesthet Surg 60 2007 272 278