Structural and biochemical characteristics of various white adipose tissue depots

Acta Physiologica

Volumn 205, Issue 2, 2012, Pages 194-208

  Wronska, A ^a   Kmiec, Z ^a  

^a MEDICAL UNIVERSITY OF GDANSK   (Poland)

Author keywords

Adipocyte; Fat depots; Subcutaneous; Visceral; White adipose tissue

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADIPOCYTOKINE; ADIPONECTIN; CARNITINE PALMITOYLTRANSFERASE; CATECHOLAMINE; CD36 ANTIGEN; DIACYLGLYCEROL ACYLTRANSFERASE; FAT DROPLET; FATTY ACID; FATTY ACID TRANSPORTER; GLUCOCORTICOID; GLUCOSE TRANSPORTER 4; GROWTH HORMONE RECEPTOR; HORMONE SENSITIVE LIPASE; LEPTIN; LIPOPROTEIN LIPASE; NEUROPEPTIDE Y; NORADRENALIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; TUMOR NECROSIS FACTOR ALPHA; VERY LOW DENSITY LIPOPROTEIN;

ADIPOCYTE; ANGIOGENESIS; BLOOD CLOTTING; BLOOD PRESSURE REGULATION; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL COUNT; CELL FUNCTION; CELL SIZE; CELL STRUCTURE; EPICARDIUM; FATTY ACID OXIDATION; GLUCOSE METABOLISM; GLUCOSE OXIDATION; GLUCOSE TRANSPORT; HORMONAL REGULATION; HUMAN; IMMUNITY; INSULIN RESISTANCE; INTRAABDOMINAL FAT; LIPID BLOOD LEVEL; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LIPOLYSIS; NONHUMAN; NUTRIENT AVAILABILITY; OBESITY; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; SUBCUTANEOUS FAT; TISSUE SPECIFICITY; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ADIPOSITY; BODY FAT DISTRIBUTION; HUMANS; OBESITY;

EID: 84860256182     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2012.02409.x     Document Type: Review

References (107)

1. Aghamohammadzadeh, R., Withers, S., Lynch, F., Greenstein, A., Malik, R. & Heagerty, A. 2011. Perivascular adipose tissue from human systemic and coronary vessels: the emergence of a new pharmacotherapeutic target. Br J Pharmacol 13, 1476-5381.
2. Ahmadian, M., Wang, Y. & Sul, H. 2010. Lipolysis in adipocytes. Int J Biochem Cell Biol 42, 555-559.
3. Alligier, M., Meugnier, E., Debard, C., Lambert-Porcheron, S., Chanseaume, E., Sothier, M., Loizon, E., Ait Hssain, A., Brozek, J., Scoazec, J.Y., Morio, B., Vidal, H. & Laville, M. 2011. Subcutaneous adipose tissue remodeling during the initial phase of weight gain induced by overfeeding in humans. J Clin Endocrinol Metab doi: 10.1210/jc.2011-2314. [Epub ahead of print].
4. Anderson, E., Gutierrez, D. & Hasty, A. 2010. Adipose tissue recruitment of leukocytes. Curr Opin Lipidol 21, 172-177.
5. Arner, P. 2005. Human fat cell lipolysis: biochemistry, regulation and clinical role. Best Pract Res Clin Endocrinol Metab 19, 471-482.
6. Arner, P., Bernard, S., Salehpour, M., Possnert, G., Liebl, J., Steier, P., Buchholz, B., Eriksson, M., Arner, E., Hauner, H., Skurk, T., Rydén, M., Frayn, K. & Spalding, K. 2011. Dynamics of human adipose lipid turnover in health and metabolic disease. Nature 478, 110-113.
7. Balamatsias, D., Kong, A., Waters, J., Sriratana, A., Gurung, R., Bailey, C., Rasko, J., Tiganis, T., Macaulay, S. & Mitchell, C. 2011. Identification of P-Rex1 as a novel Rac1-guanine nucleotide exchange factor (GEF) that promotes actin remodeling and GLUT4 protein trafficking in adipocytes. J Biol Chem 286, 43229-43240.
8. Bartness, T.J. & Song, C.K. 2007. Brain-adipose tissue neural crosstalk. Physiol Behav 91, 343-351.
9. Bartness, T., Shrestha, Y., Vaughan, C., Schwartz, G. & Song, C. 2010. Sensory and sympathetic nervous system control of white adipose tissue lipolysis. Mol Cell Endocrinol 318, 34-43.
10. Bergman, B., Perreault, L., Hunerdosse, D., Koehler, M., Samek, A. & Eckel, R. 2010. Increased intramuscular lipid synthesis and low saturation relate to insulin sensitivity in endurance-trained athletes. J Appl Physiol 108, 1134-1141.
11. Billon, N. & Dani, C. 2011. Developmental origins of the adipocyte lineage: new insights from genetics and genomics studies. Stem Cell Rev doi: 10.1007/s12015-011-9242-x. [Epub ahead of print].
12. Bjørndal, B., Burri, L., Stalesen, V., Skorve, J. & Berge, R. 2011. Different adipose depots: their role in the development of metabolic syndrome and mitochondrial response to hypolipidemic agents. J Obes doi: 10.1155/2011/490650. [Epub ahead of print].
13. Boettcher, M., Machann, J., Stefan, N., Thamer, C., Häring, H., Claussen, C., Fritsche, A. & Schick, F. 2009. Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging 29, 1340-1345.
14. Bonen, A., Tandon, N., Glatz, J., Luiken, J. & Heigenhauser, G. 2006. The fatty acid transporter FAT/CD36 is upregulated in subcutaneous and visceral adipose tissues in human obesity and type 2 diabetes. Int J Obes 30, 877-883.
15. Buemann, B., Astrup, A., Pedersen, O., Black, E., Holst, C., Toubro, S., Echwald, S., Holst, J., Rasmussen, C. & Sørensen, T. 2006. Possible role of adiponectin and insulin sensitivity in mediating the favorable effects of lower body fat mass on blood lipids. J Clin Endocrinol Metab 91, 1698-1704.
16. Cancello, R., Tordjman, J., Poitou, C., Guilhem, G., Bouillot, J., Hugol, D., Coussieu, C., Basdevant, A., Bar Hen, A., Bedossa, P., Guerre-Millo, M. & Clement, K. 2006. Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 55, 1554-1561.
17. Canoy, D. 2008. Distribution of body fat and risk of coronary heart disease in men and women. Curr Opin Cardiol 23, 591-600.
18. Ceddia, R. 2005. Direct metabolic regulation in skeletal muscle and fat tissue by leptin: implications for glucose and fatty acids homeostasis. Int J Obes 29, 1175-1183.
19. Cypess, A. & Kahn, C. 2010. Brown fat as a therapy for obesity and diabetes. Curr Opin Endocrinol Diabetes Obes 17, 143-149.
20. Deveaud, C., Beauvoit, B., Salin, B., Schaeffer, J. & Rigoulet, M. 2004. Regional differences in oxidative capacity of rat white adipose tissue are linked to the mitochondrial content of mature adipocytes. Mol Cell Biochem 267, 157-166.
21. Dicker, A., Aström, G., Wåhlén, K., Hoffstedt, J., Näslund, E., Wirén, M., Rydén, M., Arner, P. & van Harmelen, V. 2009. Primary differences in lipolysis between human omental and subcutaneous adipose tissue observed using in vitro differentiated adipocytes. Horm Metab Res 41, 350-355.
22. Divoux, A. & Clément, K. 2011. Architecture and the extracellular matrix: the still unappreciated components of the adipose tissue. Obes Rev 12, e494-e503.
23. Drolet, R., Bélanger, C., Fortier, M., Huot, C., Mailloux, J., Légaré, D. & Tchernof, A. 2009. Fat depot-specific impact of visceral obesity on adipocyte adiponectin release in women. Obesity (Silver Spring) 17, 424-430.
24. Erman, A., Veilleux, A., Tchernof, A. & Goodyer, C. 2011. Human growth hormone receptor (GHR) expression in obesity: I. GHR mRNA expression in omental and subcutaneous adipose tissues of obese women. Int J Obes 35, 1511-1519.
25. Fain, J., Madan, A., Hiler, M., Cheema, P. & Bahouth, S. 2004. Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology 145, 2273-2282.
26. Fontana, L., Eagon, J., Trujillo, M., Scherer, P. & Klein, S. 2007. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 56, 1010-1013.
27. Foster, M. & Bartness, T. 2006. Sympathetic but not sensory denervation stimulates white adipocyte proliferation. Am J Physiol Regul Integr Comp Physiol 291, R1630-R1637.
28. Fried, S., Russell, C., Grauso, N. & Brolin, R. 1993. Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men. J Clin Invest 92, 2191-2198.
29. Garg, A. & Agarwal, A. 2009. Lipodystrophies: disorders of adipose tissue biology. Biochim Biophys Acta 1791, 507-513.
30. Gealekman, O., Guseva, N., Hartigan, C., Apotheker, S., Gorgoglione, M., Gurav, K., Tran, K., Straubhaar, J., Nicoloro, S., Czech, M., Thompson, M., Perugini, R. & Corvera, S. 2011. Depot-specific differences and insufficient subcutaneous adipose tissue angiogenesis in human obesity. Circulation 123, 186-194.
31. Hannukainen, J., Kalliokoski, K., Borra, R., Viljanen, A., Janatuinen, T., Kujala, U., Kaprio, J., Heinonen, O., Viljanen, T., Haaparanta, M., Iozzo, P., Parkkola, R. & Nuutila, P. 2010. Higher free fatty acid uptake in visceral than in abdominal subcutaneous fat tissue in men. Obesity (Silver Spring) 18, 261-265.
32. Heilbronn, L., Smith, S. & Ravussin, E. 2004. Failure of fat cell proliferation, mitochondrial function and fat oxidation results in ectopic fat storage, insulin resistance and type II diabetes mellitus. Int J Obes Relat Metab Disord 28, S12-S21.
33. Hoffman, N. & Elmendorf, J. 2011. Signaling, cytoskeletal and membrane mechanisms regulating GLUT4 exocytosis. Trends Endocrinol Metab 22, 110-116.
34. Hoffstedt, J., Amer, P., Hellers, G. & Lonnqvist, F. 1997. Variation in adrenergic regulation of lipolysis between omental and subcutaneous adipocytes from obese and non-obese men. J Lipid Res 38, 795-804.
35. Hou, X., Moser, S., Sarr, M., Thompson, G., Que, F. & Jensen, M. 2009. Visceral and subcutaneous adipose tissue diacylglycerol acyltransferase activity in humans. Obesity (Silver Spring) 17, 1129-1134.
36. Hovey, R. & Aimo, L. 2010. Diverse and active roles for adipocytes during mammary gland growth and function. J Mammary Gland Biol Neoplasia 15, 279-290.
37. Iozzo, P. 2011. Myocardial, perivascular, and epicardial fat. Diabetes Care 34, S371-S379.
38. Joyner, J., Hutley, J. & Cameron, D. 2000. Glucocorticoid receptors in human preadipocytes: regional and gender differences. Endocrinol Metab 284, E1140-E1148.
39. Karamanlidis, G., Karamitri, A., Docherty, K., Hazlerigg, D. & Lomax, M. 2007. C/EBPbeta reprograms white 3T3-L1 preadipocytes to a brown adipocyte pattern of gene expression. J Biol Chem 282, 24660-24669.
40. Khan, T., Muise, E., Iyengar, P., Wang, Z., Chandalia, M., Abate, N., Zhang, B., Bonaldo, P., Chua, S. & Scherer, P. 2009. Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol Cell Biol 29, 1575-1591.
41. Kraunsoe, R., Boushel, R., Neigaard Hansen, C., Schjerling, P., Qvortrup, K., Støckel, M., Mikines, K. & Dela, F. 2010. Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity. J Physiol 588, 2023-2032.
42. Kreier, F., Fliers, E., Voshol, P., Van Eden, C., Havekes, L., Kalsbeek, A., Van Heijningen, C., Sluiter, A., Mettenleiter, T., Romijn, J., Sauerwein, H. & Buijs, R. 2002. Selective parasympathetic innervation of subcutaneous and intra-abdominal fat-functional implications. J Clin Invest 110, 1243-1250.
43. Lafontan, M. & Langin, D. 2009. Lipolysis and lipid mobilization in human adipose tissue. Prog Lipid Res 48, 275-297.
44. Ledoux, S., Queguiner, I., Msika, S., Calderari, S., Rufat, P., Gasc, J., Corvol, P. & Larger, E. 2008. Angiogenesis associated with visceral and subcutaneous adipose tissue in severe human obesity. Diabetes 57, 3247-3257.
45. Lee, M.-J., Wu, Y. & Fried, S. 2010. Adipose tissue remodeling in pathophysiology of obesity. Curr Opin Clin Nutr Metab Care 13, 371-376.
46. Li, F., Cheng, K., Lam, K., Vanhoutte, P. & Xu, A. 2011. Cross-talk between adipose tissue and vasculature: role of adiponectin. Acta Physiol (Oxf) 203, 167-180.
47. Macfarlane, D., Forbes, S. & Walker, B. 2008. Glucocorticoids and fatty acid metabolism in humans: fuelling fat redistribution in the metabolic syndrome. J Endocrinol 197, 189-204.
48. Marcus, R., Addison, O., Kidde, J., Dibble, L. & Lastayo, P. 2010. Skeletal muscle fat infiltration: impact of age, inactivity, and exercise. J Nutr Health Aging 14, 362-366.
49. Mariman, E. & Wang, P. 2010. Adipocyte extracellular matrix composition, dynamics and role in obesity. Cell Mol Life Sci 67, 1277-1292.
50. Mazur, A., Ostanski, M., Telega, G. & Malecka-Tendera, E. 2010. Is epicardial fat tissue a marker of metabolic syndrome in obese children? Atherosclerosis 211, 596-600.
51. McQuaid, S., Humphreys, S., Hodson, L., Fielding, B., Karpe, F. & Frayn, K. 2010. Femoral adipose tissue may accumulate the fat that has been recycled as VLDL and nonesterified fatty acids. Diabetes 59, 2465-2473.
52. McQuaid, S., Hodson, L., Neville, M., Dennis, A., Cheeseman, J., Humphreys, S., Ruge, T., Gilbert, M., Fielding, B., Frayn, K. & Karpe, F. 2011. Downregulation of adipose tissue fatty acid trafficking in obesity: a driver for ectopic fat deposition? Diabetes 60, 47-55.
53. Miller, N.E., Michel, C.C., Nanjee, M.N., Olszewski, W.L., Miller, I.P., Hazell, M., Olivecrona, G., Sutton, P., Humphreys, S.M. & Frayn, K.N. 2011. Secretion of adipokines by human adipose tissue in vivo: partitioning between capillary and lymphatic transport. Am J Physiol Endocrinol Metab 301, E659-E667.
54. Miyazaki, Y., Glass, L., Triplitt, C., Wajcberg, E., Mandarino, L. & DeFronzo, R. 2002. Abdominal fat distribution and peripheral and hepatic insulin resistance in type 2 diabetes mellitus. Am J Physiol 283, E1135-E1143.
55. Miyazawa-Hoshimoto, S., Takahashi, K., Bujo, H., Hashimoto, N., Yagui, K. & Saito, Y. 2005. Roles of degree of fat deposition and its localization on VEGF expression in adipocytes. Am J Physiol Endocrinol Metab 288, E1128-E1136.
56. Natale, F., Tedesco, M., Mocerino, R., de Simone, V., Di Marco, G., Aronne, L., Credendino, M., Siniscalchi, C., Calabrò, P., Cotrufo, M. & Calabrò, R. 2009. Visceral adiposity and arterial stiffness: echocardiographic epicardial fat thickness reflects, better than waist circumference, carotid arterial stiffness in a large population of hypertensives. Eur J Echocardiogr 10, 549-555.
57. Ohsaki, Y., Cheng, J., Suzuki, M., Shinohara, Y., Fujita, A. & Fujimoto, T. 2009. Biogenesis of cytoplasmic lipid droplets: from the lipid ester globule in the membrane to the visible structure. Biochim Biophys Acta 1791, 399-407.
58. Ortega, F., Moreno-Navarrete, J., Ribas, V., Esteve, E., Rodriguez-Hermosa, J., Ruiz, B., Peral, B., Ricart, W., Zorzano, A. & Fernández-Real, J. 2009. Subcutaneous fat shows higher thyroid hormone receptor-α1 gene expression than omental fat. Obesity 17, 2134-2141.
59. Ouchi, N., Parker, J., Lugus, J. & Walsh, K. 2010. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 11, 85-97.
60. Palou, M., Priego, T., Sánchez, J., Rodriguez, A., Palou, A. & Pico, C. 2009. Gene expression patterns in visceral and subcutaneous adipose depots in rats are linked to their morphologic features. Cell Physiol Biochem 24, 547-556.
61. Palou, M., Sanchez, J., Priego, T., Rodriguez, A., Pico, C. & Palou, A. 2010. Regional differences in the expression of genes involved in lipid metabolism in adipose tissue in response to short- and medium-term fasting and refeeding. J Nutr Biochem 21, 23-33.
62. Panarotto, D., Poisson, J., Devroede, G. & Maheux, P. 2000. Lipoprotein lipase steady-state mRNA levels are lower in human omental versus subcutaneous abdominal adipose tissue. Metabolism 49, 1224-1227.
63. Perreault, L., Bergman, B., Hunerdosse, D. & Eckel, R. 2010. Altered intramuscular lipid metabolism relates to diminished insulin action in men, but not women, in progression to diabetes. Obesity (Silver Spring) 18, 2093-2100.
64. Pijl, H. 2011. Obesity: evolution of a symptom of affluence. Neth J Med 69, 159-166.
65. Rasmussen, M., Lihn, A., Pedersen, S., Bruun, J., Rasmussen, M. & Richelsen, B. 2006. Adiponectin receptors in human adipose tissue: effects of obesity, weight loss, and fat depots. Obesity 14, 28-35.
66. Ray, H., Pinteur, C., Frering, V., Beylot, M. & Large, V. 2009. Depot-specific differences in perilipin and hormone-sensitive lipase expression in lean and obese. Lipids Health Dis 18, 8-58.
67. Ruge, T., Sukonina, V., Myrnäs, T., Lundgren, M., Eriksson, J. & Olivecrona, G. 2006. Lipoprotein lipase activity/mass ratio is higher in omental than in subcutaneous adipose tissue. Eur J Clin Invest 36, 16-21.
68. Sacks, H., Fain, J., Holman, B., Cheema, P., Chary, A., Parks, F., Karas, J., Optican, R., Bahouth, S., Garrett, E., Wolf, R., Carter, R., Robbins, T., Wolford, D. & Samaha, J. 2009. Uncoupling protein-1 and related messenger ribonucleic acids in human epicardial and other adipose tissues: epicardial fat functioning as brown fat. J Clin Endocrinol Metab 94, 3611-3615.
69. Samuel, V., Petersen, K. & Shulman, G. 2010. Lipid-induced insulin resistance: unravelling the mechanism. Lancet 375, 2267-2277.
70. Sato, K., Umeno, H. & Nakashima, T. 2005. Histological investigation of liposuctioned fat for injection laryngoplasty. Otolaryngol Head Neck Surg 26, 219-225.
71. Sbarbati, A., Accorsi, D., Benati, D., Marchetti, L., Orsini, G., Rigotti, G. & Panettiere, P. 2010. Subcutaneous adipose tissue classification. Eur J Histochem 54, e48.
72. Schrauwen-Hinderling, V., Hesselink, M., Schrauwen, P. & Kooi, M. 2006. Intramyocellular lipid content in human skeletal muscle. Obesity (Silver Spring) 14, 357-367.
73. Schulz, T.J., Huang, T.L., Tran, T.T., Zhang, H., Townsend, K.L., Shadrach, J.L., Cerletti, M., McDougall, L.E., Giorgadze, N., Tchkonia, T., Schrier, D., Falb, D., Kirkland, J.L., Wagers, A.J. & Tseng, Y.H. 2011. Identification of inducible brown adipocyte progenitors residing in skeletal muscle and white fat. Proc Natl Acad Sci U S A 108, 143-148.
74. Sell, H. & Eckel, J. 2010. Adipose tissue inflammation: novel insight into the role of macrophages and lymphocytes. Curr Opin Clin Nutr Metab Care 13, 366-370.
75. Sepe, A., Tchkonia, T., Thumou, T., Zamboni, M. & Kirkland, J.L. 2011. Aging and regional differences in fat cell progenitors - a mini-review. Gerontology 57, 66-75.
76. Sethi, J. & Vidal-Puig, A. 2007. Thematic review series: adipocyte biology. Adipose tissue function and plasticity orchestrate nutritional adaptation. J Lipid Res 48, 1253-1262.
77. Shay, C., Secrest, A., Goodpaster, B., Kelsey, S., Strotmeyer, E. & Orchard, T. 2010. Regional adiposity and risk for coronary artery disease in type 1 diabetes: does having greater amounts of gluteal-femoral adiposity lower the risk? Diabetes Res Clin Pract 89, 288-295.
78. Skurk, T., Alberti-Huber, C., Herder, C. & Hauner, H. 2007. Relationship between adipocyte size and adipokine expression and secretion. J Clin Endocrinol Metab 92, 1023-1033.
79. Smith, S., Lovejoy, J., Greenway, F., Ryan, D., de Jonge, L., de la Bretonne, J., Volafova, J. & Bray, G. 2001. Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity. Metabolism 50, 425-435.
80. Snijder, M., Visser, M., Dekker, J., Goodpaster, B., Harris, T., Kritchevsky, S., De Rekeneire, N., Kanaya, A., Newman, A., Tylavsky, F., Seidell, J.; Health ABC Study. 2005. Low subcutaneous thigh fat is a risk factor for unfavourable glucose and lipid levels, independently of high abdominal fat. The Health ABC Study. Diabetologia 48, 301-308.
81. Song, C.K., Schwartz, G.J. & Bartness, T.J. 2009. Anterograde transneuronal viral tract tracing reveals central sensory circuits from white adipose tissue. Am J Physiol Regul Integr Comp Physiol 296, R501-R511.
82. Spalding, K., Arner, E., Westermark, P., Bernard, S., Buchholz, B., Bergmann, O., Blomqvist, L., Hoffstedt, J., Näslund, E., Britton, T., Concha, H., Hassan, M., Rydén, M., Frisén, J. & Arner, P. 2008. Dynamics of fat cell turnover in humans. Nature 453, 783-787.
83. Spencer, M., Unal, R., Zhu, B., Rasouli, N., McGehee, R., Peterson, C. & Kern, P. 2011. Adipose tissue extracellular matrix and vascular abnormalities in obesity and insulin resistance. J Clin Endocrinol Metab 96, E1990-E1998.
84. Suganami, T. & Ogawa, Y. 2010. Adipose tissue macrophages: their role in adipose tissue remodeling. J Leukoc Biol 88, 33-39.
85. Szendroedi, J. & Roden, M. 2009. Ectopic lipids and organ function. Curr Opin Lipidol 20, 50-56.
86. Tchernof, A., Bélanger, C., Morisset, A., Richard, C., Mailloux, J., Laberge, P. & Dupont, P. 2006. Regional differences in adipose tissue metabolism in women: minor effect of obesity and body fat distribution. Diabetes 55, 1353-1360.
87. Tchkonia, T., Giorgadze, N., Pirtskhalava, T., Tchoukalova, Y., Karagiannides, I., Forse, R., DePonte, M., Stevenson, M., Guo, W., Han, J., Waloga, G., Lash, T., Jensen, M. & Kirkland, J. 2002. Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am J Physiol Regul Integr Comp Physiol 282, R1286-R1296.
88. Tchkonia, T., Tchoukalova, Y.D., Giorgadze, N., Pirtskhalava, T., Karagiannides, I., Forse, R.A., Koo, A., Stevenson, M., Chinnappan, D., Cartwright, A., Jensen, M. & Kirkland, J. 2005. Abundance of two human preadipocyte subtypes with distinct capacities for replication, adipogenesis, and apoptosis varies among fat depots. Am J Physiol 288, E267-E277.
89. 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.
90. Toh, S., Gong, J., Du, G., Li, J., Yang, S., Ye, J., Yao, H., Zhang, Y., Xue, B., Li, Q., Yang, H., Wen, Z. & Li, P. 2008. Up-regulation of mitochondrial activity and acquirement of brown adipose tissue-like property in the white adipose tissue of Fsp27 deficient mice. PLoS ONE 3, e2890.
91. Torres-Leal, F.L., Fonseca-Alaniz, M.H., Rogero, M.M. & Tirapegui, J. 2010. The role of inflamed adipose tissue in the insulin resistance. Cell Biochem Funct 28, 623-631.
92. Van Harmelen, V., Reynisdottir, S., Eriksson, P., Thorne, A., Hoffstedt, J., Lonnqvist, F. & Arner, P. 1998. Leptin secretion from subcutaneous and visceral adipose tissue in women. Diabetes 47, 913-917.
93. Veilleux, A., Blouin, K., Rhéaume, C., Daris, M., Marette, A. & Tchernof, A. 2009. Glucose transporter 4 and insulin receptor substrate-1 messenger RNA expression in omental and subcutaneous adipose tissue in women. Metabolism 58, 624-631.
94. Verstraeten, V., Renes, J., Ramaekers, F., Kamps, M., Kuijpers, H., Verheyen, F., Wabitsch, M., Steijlen, P., van Steensel, M. & Broer, J. 2011. Reorganization of the nuclear lamina and cytoskeleton in adipogenesis. Histochem Cell Biol 135, 251-261.
95. Virtanen, K., Lonnroth, P., Parkkola, R., Peltoniemi, P., Asola, M., Viljanen, T., Tolvanen, T., Knuuti, J., Ronnemaa, T., Huupponen, R. & Nuutila, P. 2002. Glucose uptake and perfusion in subcutaneous and visceral adipose tissue during insulin stimulation in nonobese and obese humans. J Clin Endocrinol Metab 87, 3902-3910.
96. Virtue, S. & Vidal-Puig, A. 2010. Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome - an allostatic perspective. Biochim Biophys Acta 1801, 338-349.
97. Vlasova, M., Purhonen, A., Jarvelin, M., Rodilla, E., Pascual, J. & Herzig, K. 2010. Role of adipokines in obesity-associated hypertension. Acta Physiol (Oxf) 200, 107-127.
98. Walker, G., Verti, B., Marzullo, P., Savia, G., Mencarelli, M., Zurleni, F., Liuzi, A. & Di Blasio, A. 2007. Cellular and molecular deep subcutaneous adipose tissue: a distinct abdominal adipose depot. Obesity 15, 1933-1943.
99. Walker, G., Marzullo, P., Verti, B., Guzzaloni, G., Maestrini, S., Zurleni, F., Liuzzi, A. & Di Blasio, A. 2008. Subcutaneous abdominal adipose tissue subcompartments: potential role in rosiglitazone effects. Obesity 16, 1983-1991.
100. Wolfs, M., Rensen, S., Bruin-Van Dijk, E., Verdam, F., Greve, J., Sanjabi, B., Bruinenberg, M., Wijmenga, C., van Haeften, T., Buurman, W., Franke, L. & Hofker, M. 2010. Co-expressed immune and metabolic genes in visceral and subcutaneous adipose tissue from severely obese individuals are associated with plasma HDL and glucose levels: a microarray study. BMC Med Genomics 5, 3-34.
101. Xu, A., Wang, Y., Lam, K. & Vanhoutte, P. 2010. Vascular actions of adipokines: molecular mechanisms and therapeutic implications. Adv Pharmacol 60, 229-255.
102. Yamamoto, Y., Gesta, S., Lee, K., Tran, T., Saadatirad, P. & Kahn, C. 2010. Adipose depots possess unique developmental gene signatures. Obesity (Silver Spring) 18, 872-878.
103. Yang, Y., Chen, M., Clements, R., Abrams, J., Aprahamian, C. & Harmon, C. 2008. Human mesenteric adipose tissue plays unique role versus subcutaneous and omental fat in obesity related diabetes. Cell Physiol Biochem 22, 531-538.
104. Yang, K., Guan, H., Arany, E., Hill, D. & CaoYarak, X. 2010. Neuropeptide Y is produced in visceral adipose tissue and promotes proliferation of adipocyte precursor cells via the Y1 receptor. FASEB J 22, 2452-2464.
105. Yarak, S. & Okamoto, O. 2010. Human adipose-derived stem cells: current challenges and clinical perspectives. An Bras Dermatol 85, 647-656.
106. Ye, J. 2011. Adipose tissue vascularization: its role in chronic inflammation. Curr Diab Rep 11, 203-210.
107. Yim, J., Heshka, S., Albu, J., Heymsfield, S., Kuznia, P., Harris, T. & Gallagher, D. 2007. Intermuscular adipose tissue rivals visceral adipose tissue in independent associations with cardiovascular risk. Int J Obes 31, 1400-1405.