The developmental origins of adipose tissue

Development (Cambridge)

Volumn 140, Issue 19, 2013, Pages 3939-3949

  Berry, Daniel C ^a   Stenesen, Drew ^a   Zeve, Daniel ^a   Graff, Jonathan M ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Adipocyte; Adipose; Development; Niche; Stem cells; Vascular niche

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; ANGIOTENSINOGEN; CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; CCAAT ENHANCER BINDING PROTEIN DELTA; FIBROBLAST GROWTH FACTOR 2; GLYCOGEN SYNTHASE; INSULIN RECEPTOR; INTERLEUKIN 6; KRUPPEL LIKE FACTOR 4; KRUPPEL LIKE FACTOR 5; LEPTIN; OSTEOGENIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; STAT5A PROTEIN; UNCOUPLING PROTEIN 1; VASCULOTROPIN;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ADIPOSE TISSUE; BROWN ADIPOSE TISSUE; CARCINOGENESIS; CELL DIFFERENTIATION; CYTOLOGY; DEVELOPMENTAL BIOLOGY; DIABETES MELLITUS; ENERGY BALANCE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HYPERGLYCEMIA; HYPERLIPIDEMIA; HYPERTENSION; INTRAABDOMINAL FAT; LIPID STORAGE; LIPOGENESIS; LIVER DISEASE; MICROENVIRONMENT; NONHUMAN; OBESITY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SUBCUTANEOUS FAT; WHITE ADIPOSE TISSUE; WNT SIGNALING PATHWAY;

ADIPOCYTE; ADIPOSE; DEVELOPMENT; NICHE; STEM CELLS; VASCULAR NICHE;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; HUMANS; STEM CELL NICHE; STEM CELLS;

EID: 84884273954     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.080549     Document Type: Review

References (116)

1. Akazawa, S., Sun, F., Ito, M., Kawasaki, E. and Eguchi, K. (2000). Efficacy of troglitazone on body fat distribution in type 2 diabetes. Diabetes Care 23, 1067-1071.
2. Atit, R., Sgaier, S. K., Mohamed, O. A., Taketo, M. M., Dufort, D., Joyner, A. L., Niswander, L. and Conlon, R. A. (2006). Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev. Biol. 296, 164-176.
3. Baglioni, S., Cantini, G., Poli, G., Francalanci, M., Squecco, R., Di Franco, A., Borgogni, E., Frontera, S., Nesi, G., Liotta, F. et al. (2012). Functional differences in visceral and subcutaneous fat pads originate from differences in the adipose stem cell. PLoS ONE 7, e36569.
4. Barak, Y., Nelson, M. C., Ong, E. S., Jones, Y. Z., Ruiz-Lozano, P., Chien, K. R., Koder, A. and Evans, R. M. (1999). PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell 4, 585-595.
5. Berry, R. and Rodeheffer, M. S. (2013). Characterization of the adipocyte cellular lineage in vivo. Nat. Cell Biol. 15, 302-308.
6. Berry, D. C., DeSantis, D., Soltanian, H., Croniger, C. M. and Noy, N. (2012). Retinoic acid upregulates preadipocyte genes to block adipogenesis and suppress diet-induced obesity. Diabetes 61, 1112-1121.
7. Billon, N., Iannarelli, P., Monteiro, M. C., Glavieux-Pardanaud, C., Richardson, W. D., Kessaris, N., Dani, C. and Dupin, E. (2007). The generation of adipocytes by the neural crest. Development 134, 2283-2292.
8. Björntorp, P., Bengtsson, C., Blohmé, G., Jonsson, A., Sjöström, L., Tibblin, E., Tibblin, G. and Wilhelmsen, L. (1971). Adipose tissue fat cell size and number in relation to metabolism in randomly selected middle-aged men and women. Metabolism 20, 927-935.
9. Brun, R. P., Tontonoz, P., Forman, B. M., Ellis, R., Chen, J., Evans, R. M. and Spiegelman, B. M. (1996). Differential activation of adipogenesis by multiple PPAR isoforms. Genes Dev. 10, 974-984.
10. Bueno, A. A., Habitante, C. A., Oyama, L. M., Estadella, D., Ribeiro, E. B. and Oller do Nascimento, C. M. (2011). White adipose tissue re-growth after partial lipectomy in high fat diet induced obese wistar rats. J. Physiol. Sci. 61, 55-63.
11. Cannon, B. and Nedergaard, J. (2004). Brown adipose tissue: function and physiological significance. Physiol. Rev. 84, 277-359.
12. Cao, Y. (2007). Angiogenesis modulates adipogenesis and obesity. J. Clin. Invest. 117, 2362-2368.
13. Cawthorn, W. P., Heyd, F., Hegyi, K. and Sethi, J. K. (2007). Tumour necrosis factor-alpha inhibits adipogenesis via a beta-catenin/TCF4(TCF7L2)-dependent pathway. Cell Death Differ. 14, 1361-1373.
14. Cawthorn, W. P., Scheller, E. L. and MacDougald, O. A. (2012). Adipose tissue stem cells meet preadipocyte commitment: going back to the future. J. Lipid Res. 53, 227-246.
15. Chapman, A. B., Knight, D. M. and Ringold, G. M. (1985). Glucocorticoid regulation of adipocyte differentiation: hormonal triggering of the developmental program and induction of a differentiation-dependent gene. J. Cell Biol. 101, 1227-1235.
16. Chawla, A., Schwarz, E. J., Dimaculangan, D. D. and Lazar, M. A. (1994). Peroxisome proliferator-activated receptor (PPAR) gamma: adiposepredominant expression and induction early in adipocyte differentiation. Endocrinology 135, 798-800.
17. Clark, E. R. and Clark., E. L. (1940). Microscopic studies of the new formation of fat in living adult rabbits. Am. J. Anat. 67, 255-285.
18. Crandall, D. L., Hausman, G. J. and Kral, J. G. (1997). A review of the microcirculation of adipose tissue: anatomic, metabolic, and angiogenic perspectives. Microcirculation 4, 211-232.
19. Cristancho, A. G. and Lazar, M. A. (2011). Forming functional fat: a growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol. 12, 722-734.
20. Crossno, J. T., Jr, Majka, S. M., Grazia, T., Gill, R. G. and Klemm, D. J. (2006). Rosiglitazone promotes development of a novel adipocyte population from bone marrow-derived circulating progenitor cells. J. Clin. Invest. 116, 3220-3228.
21. Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y. H., Doria, A. et al. (2009). Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360, 1509-1517.
22. Cypess, A. M., White, A. P., Vernochet, C., Schulz, T. J., Xue, R., Sass, C. A., Huang, T. L., Roberts-Toler, C., Weiner, L. S., Sze, C. et al. (2013). Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat. Med. 19, 635-639.
23. de Souza, C. J., Eckhardt, M., Gagen, K., Dong, M., Chen, W., Laurent, D. and Burkey, B. F. (2001). Effects of pioglitazone on adipose tissue remodeling within the setting of obesity and insulin resistance. Diabetes 50, 1863-1871.
24. Duan, S. Z., Ivashchenko, C. Y., Whitesall, S. E., D'Alecy, L. G., Duquaine, D. C., Brosius, F. C., 3rd, Gonzalez, F. J., Vinson, C., Pierre, M. A., Milstone, D. S. et al. (2007). Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J. Clin. Invest. 117, 812-822.
25. Fisher, R. M., Thörne, A., Hamsten, A. and Arner, P. (2002). Fatty acid binding protein expression in different human adipose tissue depots in relation to rates of lipolysis and insulin concentration in obese individuals. Mol. Cell. Biochem. 239, 95-100.
26. Flores-Delgado, G., Marsch-Moreno, M. and Kuri-Harcuch, W. (1987). Thyroid hormone stimulates adipocyte differentiation of 3T3 cells. Mol. Cell. Biochem. 76, 35-43.
27. Fukumura, D., Ushiyama, A., Duda, D. G., Xu, L., Tam, J., Krishna, V., Chatterjee, K., Garkavtsev, I. and Jain, R. K. (2003). Paracrine regulation of angiogenesis and adipocyte differentiation during in vivo adipogenesis. Circ. Res. 93, e88-e97.
28. Gealekman, O., Burkart, A., Chouinard, M., Nicoloro, S. M., Straubhaar, J. and Corvera, S. (2008). Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production. Am. J. Physiol. 295, E1056-E1064.
29. Gesta, S., Blüher, M., Yamamoto, Y., Norris, A. W., Berndt, J., Kralisch, S., Boucher, J., Lewis, C. and Kahn, C. R. (2006). Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc. Natl. Acad. Sci. USA 103, 6676-6681.
30. Gesta, S., Tseng, Y. H. and Kahn, C. R. (2007). Developmental origin of fat: tracking obesity to its source. Cell 131, 242-256.
31. Gir, P., Oni, G., Brown, S. A., Mojallal, A. and Rohrich, R. J. (2012). Human adipose stem cells: current clinical applications. Plast. Reconstr. Surg. 129, 1277-1290.
32. Grauer, W. O., Moss, A. A., Cann, C. E. and Goldberg, H. I. (1984). Quantification of body fat distribution in the abdomen using computed tomography. Am. J. Clin. Nutr. 39, 631-637.
33. Green, H. and Kehinde, O. (1975). An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5, 19-27.
34. Gregoire, F. M., Smas, C. M. and Sul, H. S. (1998). Understanding adipocyte differentiation. Physiol. Rev. 78, 783-809.
35. Gupta, R. K., Mepani, R. J., Kleiner, S., Lo, J. C., Khandekar, M. J., Cohen, P., Frontini, A., Bhowmick, D. C., Ye, L., Cinti, S. et al. (2012). Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metab. 15, 230-239.
36. Han, J., Lee, J. E., Jin, J., Lim, J. S., Oh, N., Kim, K., Chang, S. I., Shibuya, M., Kim, H. and Koh, G. Y. (2011). The spatiotemporal development of adipose tissue. Development 138, 5027-5037.
37. He, W., Barak, Y., Hevener, A., Olson, P., Liao, D., Le, J., Nelson, M., Ong, E., Olefsky, J. M. and Evans, R. M. (2003). Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. USA 100, 15712-15717.
38. Hellman, B. and Hellerstrom, C. (1961). Cell renewal in the white and brown fat tissue of the rat. Acta Pathol. Microbiol. Scand. 51, 347-353.
39. Herbst, K. L. (2012). Rare adipose disorders (RADs) masquerading as obesity. Acta Pharmacol. Sin. 33, 155-172.
40. Hiragun, A., Sato, M. and Mitsui, H. (1988). Preadipocyte differentiation in vitro: identification of a highly active adipogenic agent. J. Cell. Physiol. 134, 124-130.
41. Hirsch, J. and Batchelor, B. (1976). Adipose tissue cellularity in human obesity. Clin. Endocrinol. Metab. 5, 299-311.
42. Hollenberg, C. H. and Vost, A. (1968). Regulation of DNA synthesis in fat cells and stromal elements from rat adipose tissue. J. Clin. Invest. 47, 2485-2498.
43. Hossain, P., Kawar, B. and El Nahas, M. (2007). Obesity and diabetes in the developing world-a growing challenge. N. Engl. J. Med. 356, 213-215.
44. Jernås, M., Palming, J., Sjöholm, K., Jennische, E., Svensson, P. A., Gabrielsson, B. G., Levin, M., Sjögren, A., Rudemo, M., Lystig, T. C. et al. (2006). Separation of human adipocytes by size: hypertrophic fat cells display distinct gene expression. FASEB J. 20, 1540-1542.
45. Joe, A. W., Yi, L., Even, Y., Vogl, A. W. and Rossi, F. M. (2009). Depot-specific differences in adipogenic progenitor abundance and proliferative response to high-fat diet. Stem Cells 27, 2563-2570.
46. Kajimura, S., Seale, P. and Spiegelman, B. M. (2010). Transcriptional control of brown fat development. Cell Metab. 11, 257-262.
47. Kanda, T., Brown, J. D., Orasanu, G., Vogel, S., Gonzalez, F. J., Sartoretto, J., Michel, T. and Plutzky, J. (2009). PPARgamma in the endothelium regulates metabolic responses to high-fat diet in mice. J. Clin. Invest. 119, 110-124.
48. Kelly, I. E., Han, T. S., Walsh, K. and Lean, M. E. (1999). Effects of a thiazolidinedione compound on body fat and fat distribution of patients with type 2 diabetes. Diabetes Care 22, 288-293.
49. Kersten, S., Mandard, S., Tan, N. S., Escher, P., Metzger, D., Chambon, P., Gonzalez, F. J., Desvergne, B. and Wahli, W. (2000). Characterization of the fasting-induced adipose factor FIAF, a novel peroxisome proliferator-activated receptor target gene. J. Biol. Chem. 275, 28488-28493.
50. Larson, K. A. and Anderson, D. B. (1978). The effects of lipectomy on remaining adipose tissue depots in the Sprague Dawley rat. Growth 42, 469-477.
51. Le Lièvre, C. S. and Le Douarin, N. M. (1975). Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J. Embryol. Exp. Morphol. 34, 125-154.
52. Lee, Y. H., Petkova, A. P., Mottillo, E. P. and Granneman, J. G. (2012). In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metab. 15, 480-491.
53. Lidell, M. E., Betz, M. J., Dahlqvist Leinhard, O., Heglind, M., Elander, L., Slawik, M., Mussack, T., Nilsson, D., Romu, T., Nuutila, P. et al. (2013). Evidence for two types of brown adipose tissue in humans. Nat. Med. 19, 631-634.
54. Longo, K. A., Wright, W. S., Kang, S., Gerin, I., Chiang, S. H., Lucas, P. C., Opp, M. R. and MacDougald, O. A. (2004). Wnt10b inhibits development of white and brown adipose tissues. J. Biol. Chem. 279, 35503-35509.
55. MacDougald, O. A. and Mandrup, S. (2002). Adipogenesis: forces that tip the scales. Trends Endocrinol. Metab. 13, 5-11.
56. Macotela, Y., Emanuelli, B., Mori, M. A., Gesta, S., Schulz, T. J., Tseng, Y. H. and Kahn, C. R. (2012). Intrinsic differences in adipocyte precursor cells from different white fat depots. Diabetes 61, 1691-1699.
57. Masuzaki, H., Paterson, J., Shinyama, H., Morton, N. M., Mullins, J. J., Seckl, J. R. and Flier, J. S. (2001). A transgenic model of visceral obesity and the metabolic syndrome. Science 294, 2166-2170.
58. Mauer, M. M., Harris, R. B. and Bartness, T. J. (2001). The regulation of total body fat: lessons learned from lipectomy studies. Neurosci. Biobehav. Rev. 25, 15-28.
59. McKay, R. M., McKay, J. P., Avery, L. and Graff, J. M. (2003). C elegans: a model for exploring the genetics of fat storage. Dev. Cell 4, 131-142.
60. Medici, D., Shore, E. M., Lounev, V. Y., Kaplan, F. S., Kalluri, R. and Olsen, B. R. (2010). Conversion of vascular endothelial cells into multipotent stem-like cells. Nat. Med. 16, 1400-1406.
61. Miles, P. D., Barak, Y., He, W., Evans, R. M. and Olefsky, J. M. (2000). Improved insulin-sensitivity in mice heterozygous for PPAR-gamma deficiency. J. Clin. Invest. 105, 287-292.
62. Monteiro, M. C., Wdziekonski, B., Villageois, P., Vernochet, C., Iehle, C., Billon, N. and Dani, C. (2009). Commitment of mouse embryonic stem cells to the adipocyte lineage requires retinoic acid receptor beta and active GSK3. Stem Cells Dev. 18, 457-463.
63. Muto, S., Miyata, Y., Imai, M. and Asano, Y. (2001). Troglitazone stimulates basolateral rheogenic Na+/HCO3-cotransport activity in rabbit proximal straight tubules. Exp. Nephrol. 9, 191-197.
64. Napolitano, L. (1963). The Differentiation of White Adipose Cells. An Electron Microscope Study. J. Cell Biol. 18, 663-679.
65. Napolitano, L. and Gagne, H. T. (1963). Lipid-depleted white adipose cells: an electronmicroscope study. Anat. Rec. 147, 273-293.
66. Nawrocki, A. R. and Scherer, P. E. (2004). The delicate balance between fat and muscle: adipokines in metabolic disease and musculoskeletal inflammation. Curr. Opin. Pharmacol. 4, 281-289.
67. Nishimura, S., Manabe, I., Nagasaki, M., Hosoya, Y., Yamashita, H., Fujita, H., Ohsugi, M., Tobe, K., Kadowaki, T., Nagai, R. et al. (2007). Adipogenesis in obesity requires close interplay between differentiating adipocytes, stromal cells, and blood vessels. Diabetes 56, 1517-1526.
68. Okuno, A., Tamemoto, H., Tobe, K., Ueki, K., Mori, Y., Iwamoto, K., Umesono, K., Akanuma, Y., Fujiwara, T., Horikoshi, H. et al. (1998). Troglitazone increases the number of small adipocytes without the change of white adipose tissue mass in obese Zucker rats. J. Clin. Invest. 101, 1354-1361.
69. Osborn, O. and Olefsky, J. M. (2012). The cellular and signaling networks linking the immune system and metabolism in disease. Nat. Med. 18, 363-374.
70. Reyne, Y., Nougues, J. and Vezinhet, A. (1983). Adipose tissue regeneration in 6-month-old and adult rabbits following lipectomy. Proc. Soc. Exp. Biol. Med. 174, 258-264.
71. Rigamonti, A., Brennand, K., Lau, F. and Cowan, C. A. (2011). Rapid cellular turnover in adipose tissue. PLoS ONE 6, e17637.
72. Rodeheffer, M. S., Birsoy, K. and Friedman, J. M. (2008). Identification of white adipocyte progenitor cells in vivo. Cell 135, 240-249.
73. Rosen, E. D. and Spiegelman, B. M. (2000). Molecular regulation of adipogenesis. Annu. Rev. Cell Dev. Biol. 16, 145-171.
74. Ross, S. E., Hemati, N., Longo, K. A., Bennett, C. N., Lucas, P. C., Erickson, R. L. and MacDougald, O. A. (2000). Inhibition of adipogenesis by Wnt signaling. Science 289, 950-953.
75. Salans, L. B., Cushman, S. W. and Weismann, R. E. (1973). Studies of human adipose tissue. Adipose cell size and number in nonobese and obese patients. J. Clin. Invest. 52, 929-941.
76. Sanchez-Gurmaches, J., Hung, C. M., Sparks, C. A., Tang, Y., Li, H. and Guertin, D. A. (2012). PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metab. 16, 348-362.
77. Sandouk, T., Reda, D. and Hofmann, C. (1993a). Antidiabetic agent pioglitazone enhances adipocyte differentiation of 3T3-F442A cells. Am. J. Physiol. 264, C1600-C1608.
78. Sandouk, T., Reda, D. and Hofmann, C. (1993b). The antidiabetic agent pioglitazone increases expression of glucose transporters in 3T3-F442A cells by increasing messenger ribonucleic acid transcript stability. Endocrinology 133, 352-359.
79. Satoor, S. N., Puranik, A. S., Kumar, S., Williams, M. D., Ghale, M., Rahalkar, A., Karandikar, M. S., Shouche, Y., Patole, M., Bhonde, R. et al. (2011). Location, location, location: Beneficial effects of autologous fat transplantation. Sci. Rep. 1, 81.
80. Seale, P., Bjork, B., Yang, W., Kajimura, S., Chin, S., Kuang, S., Scimè, A., Devarakonda, S., Conroe, H. M., Erdjument-Bromage, H. et al. (2008). PRDM16 controls a brown fat/skeletal muscle switch. Nature 454, 961-967.
81. Seale, P., Kajimura, S. and Spiegelman, B. M. (2009). Transcriptional control of brown adipocyte development and physiological function-of mice and men. Genes Dev. 23, 788-797.
82. Sera, Y., LaRue, A. C., Moussa, O., Mehrotra, M., Duncan, J. D., Williams, C. R., Nishimoto, E., Schulte, B. A., Watson, P. M., Watson, D. K. et al. (2009). Hematopoietic stem cell origin of adipocytes. Exp Hematol 37, 1108-1120, e1-e4.
83. Shi, H. and Clegg, D. J. (2009). Sex differences in the regulation of body weight. Physiol. Behav. 97, 199-204.
84. Shimizu, H., Tsuchiya, T., Sato, N., Shimomura, Y., Kobayashi, I. and Mori, M. (1998). Troglitazone reduces plasma leptin concentration but increases hunger in NIDDM patients. Diabetes Care 21, 1470-1474.
85. Siersbæk, R., Nielsen, R. and Mandrup, S. (2012). Transcriptional networks and chromatin remodeling controlling adipogenesis. Trends Endocrinol. Metab. 23, 56-64.
86. Snijder, M. B., Dekker, J. M., Visser, M., Bouter, L. M., Stehouwer, C. D., Kostense, P. J., Yudkin, J. S., Heine, R. J., Nijpels, G. and Seidell, J. C. (2003a). Associations of hip and thigh circumferences independent of waist circumference with the incidence of type 2 diabetes: the Hoorn Study. Am. J. Clin. Nutr. 77, 1192-1197.
87. Snijder, M. B., Dekker, J. M., Visser, M., Yudkin, J. S., Stehouwer, C. D., Bouter, L. M., Heine, R. J., Nijpels, G. and Seidell, J. C. (2003b). Larger thigh and hip circumferences are associated with better glucose tolerance: the Hoorn study. Obes. Res. 11, 104-111.
88. Spalding, K. L., Arner, E., Westermark, P. O., Bernard, S., Buchholz, B. A., Bergmann, O., Blomqvist, L., Hoffstedt, J., Näslund, E., Britton, T. et al. (2008). Dynamics of fat cell turnover in humans. Nature 453, 783-787.
89. Spiegelman, B. M. and Flier, J. S. (2001). Obesity and the regulation of energy balance. Cell 104, 531-543.
90. Sterodimas, A., Boriani, F., Magarakis, E., Nicaretta, B., Pereira, L. H. and Illouz, Y. G. (2012). Thirtyfour years of liposuction: past, present and future. Eur. Rev. Med. Pharmacol. Sci. 16, 393-406.
91. Strissel, K. J., Stancheva, Z., Miyoshi, H., Perfield, J. W., 2nd, DeFuria, J., Jick, Z., Greenberg, A. S. and Obin, M. S. (2007). Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 56, 2910-2918.
92. Suh, J. M., Gao, X., McKay, J., McKay, R., Salo, Z. and Graff, J. M. (2006). Hedgehog signaling plays a conserved role in inhibiting fat formation. Cell Metab. 3, 25-34.
93. Suh, J. M., Zeve, D., McKay, R., Seo, J., Salo, Z., Li, R., Wang, M. and Graff, J. M. (2007). Adipose is a conserved dosage-sensitive antiobesity gene. Cell Metab. 6, 195-207.
94. Suh, J. M., Stenesen, D., Peters, J. M., Inoue, A., Cade, A. and Graff, J. M. (2008). An RGS-containing sorting nexin controls Drosophila lifespan. PLoS ONE 3, e2152.
95. Sul, H. S. (2009). Minireview: Pref-1: role in adipogenesis and mesenchymal cell fate. Mol. Endocrinol. 23, 1717-1725.
96. Sun, K., Wernstedt Asterholm, I., Kusminski, C. M., Bueno, A. C., Wang, Z. V., Pollard, J. W., Brekken, R. A. and Scherer, P. E. (2012). Dichotomous effects of VEGF-A on adipose tissue dysfunction. Proc. Natl. Acad. Sci. USA 109, 5874-5879.
97. Tang, W., Zeve, D., Suh, J. M., Bosnakovski, D., Kyba, M., Hammer, R. E., Tallquist, M. D. and Graff, J. M. (2008). White fat progenitor cells reside in the adipose vasculature. Science 322, 583-586.
98. Tang, W., Zeve, D., Seo, J., Jo, A. Y. and Graff, J. M. (2011). Thiazolidinediones regulate adipose lineage dynamics. Cell Metab. 14, 116-122.
99. Tchernof, A., Bélanger, C., Morisset, A. S., Richard, C., Mailloux, J., Laberge, P. and Dupont, P. (2006). Regional differences in adipose tissue metabolism in women: minor effect of obesity and body fat distribution. Diabetes 55, 1353-1360.
100. Tchkonia, T., Giorgadze, N., Pirtskhalava, T., Tchoukalova, Y., Karagiannides, I., Forse, R. A., DePonte, M., Stevenson, M., Guo, W., Han, J. et al. (2002). Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am. J. Physiol. 282, R1286-R1296.
101. Tchkonia, T., Lenburg, M., Thomou, T., Giorgadze, N., Frampton, G., Pirtskhalava, T., Cartwright, A., Cartwright, M., Flanagan, J., Karagiannides, I. et al. (2007). Identification of depot-specific human fat cell progenitors through distinct expression profiles and developmental gene patterns. Am. J. Physiol. 292, E298-E307.
102. Tontonoz, P. and Spiegelman, B. M. (2008). Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 77, 289-312.
103. Tontonoz, P., Hu, E., Graves, R. A., Budavari, A. I. and Spiegelman, B. M. (1994). mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8, 1224-1234.
104. Traktuev, D. O., Prater, D. N., Merfeld-Clauss, S., Sanjeevaiah, A. R., Saadatzadeh, M. R., Murphy, M., Johnstone, B. H., Ingram, D. A. and March, K. L. (2009). Robust functional vascular network formation in vivo by cooperation of adipose progenitor and endothelial cells. Circ. Res. 104, 1410-1420.
105. Tran, T. T., Yamamoto, Y., Gesta, S. and Kahn, C. R. (2008). Beneficial effects of subcutaneous fat transplantation on metabolism. Cell Metab. 7, 410-420.
106. Tran, K. V., Gealekman, O., Frontini, A., Zingaretti, M. C., Morroni, M., Giordano, A., Smorlesi, A., Perugini, J., De Matteis, R., Sbarbati, A. et al. (2012). The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab. 15, 222-229.
107. Tseng, Y. H., Kokkotou, E., Schulz, T. J., Huang, T. L., Winnay, J. N., Taniguchi, C. M., Tran, T. T., Suzuki, R., Espinoza, D. O., Yamamoto, Y. et al. (2008). New role of bone morphogenetic protein 7 in brown adipogenesis and energy expenditure. Nature 454, 1000-1004.
108. Wang, Y., Kim, K. A., Kim, J. H. and Sul, H. S. (2006). Pref-1, a preadipocyte secreted factor that inhibits adipogenesis. J. Nutr. 136, 2953-2956.
109. Weyer, C., Foley, J. E., Bogardus, C., Tataranni, P. A. and Pratley, R. E. (2000). Enlarged subcutaneous abdominal adipocyte size, but not obesity itself, predicts type II diabetes independent of insulin resistance. Diabetologia 43, 1498-1506.
110. Whittle, A. J., López, M. and Vidal-Puig, A. (2011). Using brown adipose tissue to treat obesity-the central issue. Trends Mol. Med. 17, 405-411.
111. Wu, J., Boström, P., Sparks, L. M., Ye, L., Choi, J. H., Giang, A. H., Khandekar, M., Virtanen, K. A., Nuutila, P., Schaart, G. et al. (2012). Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366-376.
112. Yamamoto, N., Akamatsu, H., Hasegawa, S., Yamada, T., Nakata, S., Ohkuma, M., Miyachi, E., Marunouchi, T. and Matsunaga, K. (2007). Isolation of multipotent stem cells from mouse adipose tissue. J. Dermatol. Sci. 48, 43-52.
113. Yki-Järvinen, H. (2004). Thiazolidinediones. N. Engl. J. Med. 351, 1106-1118.
114. Zamani, N. and Brown, C. W. (2011). Emerging roles for the transforming growth factor-beta superfamily in regulating adiposity and energy expenditure. Endocr. Rev. 32, 387-403.
115. Zeve, D., Tang, W. and Graff, J. (2009). Fighting fat with fat: the expanding field of adipose stem cells. Cell Stem Cell 5, 472-481.
116. Zeve, D., Seo, J., Suh, J. M., Stenesen, D., Tang, W., Berglund, E. D., Wan, Y., Williams, L. J., Lim, A., Martinez, M. J. et al. (2012). Wnt signaling activation in adipose progenitors promotes insulin-independent muscle glucose uptake. Cell Metab. 15, 492-504.