Depot- and obesity-related differences in adipogenesis

Clinical Lipidology

Volumn 7, Issue 5, 2012, Pages 587-596

  Lessard, Julie ^a   Tchernof, André ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

adipocyte; adipogenesis; hyperplasia; obesity; PPAR

Indexed keywords

PROTEIN;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; CELL COUNT; CELL HYPERPLASIA; CELL HYPERTROPHY; CELL SIZE; DIET; GENE IDENTIFICATION; GENE INTERACTION; GENETIC VARIABILITY; HUMAN; HYPERPLASIA; HYPERTROPHY; INTRAABDOMINAL FAT; LIPID STORAGE; NONHUMAN; OBESITY; PHENOTYPE; PRIORITY JOURNAL; PROADIPOCYTE; REVIEW; SUBCUTANEOUS FAT; TISSUE HYPERPLASIA;

EID: 84869446871     PISSN: 17584299     EISSN: 17584302     Source Type: Journal    
DOI: 10.2217/clp.12.49     Document Type: Review

References (101)

1. Cristancho AG, Lazar MA. Forming functional fat: A growing understanding of adipocyte differentiation. Nat. Rev. Mol. Cell Biol. 12(11), 722-734 (2011).
2. Lowe CE, O'Rahilly S, Rochford JJ. Adipogenesis at a glance. J. Cell Sci. 124(Pt 16), 2681-2686 (2011).
3. Gregoire FM, Smas CM, Sul HS. Understanding adipocyte differentiation. Physiol Rev. 78(3), 783-809 (1998). (Pubitemid 28340604)
4. Hausman DB, Digirolamo M, Bartness TJ, Hausman GJ, Martin RJ. The biology of white adipocyte proliferation. Obes. Rev. 2(4), 239-254 (2001). (Pubitemid 33755900)
5. Fajas L. Adipogenesis: A cross-talk between cell proliferation and cell differentiation. Ann. Med. 35(2), 79-85 (2003). (Pubitemid 36638210)
6. Avram MM, Avram AS, James WD. Subcutaneous fat in normal and diseased states 3. Adipogenesis: From stem cell to fat cell. J. Am. Acad. Dermatol. 56(3), 472-492 (2007). (Pubitemid 46273833)
7. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev. 14(11), 1293-1307 (2000). (Pubitemid 30397073)
8. Rosen ED, MacDougald OA. Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 7(12), 885-896 (2006). (Pubitemid 44871415)
9. Gregoire FM. Adipocyte differentiation: From fibroblast to endocrine cell. Exp. Biol. Med(Maywood) 226(11), 997-1002 (2001).
10. Rosen ED, Sarraf P, Troy AE et al. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell 4(4), 611-617 (1999). (Pubitemid 29531140)
11. Kubota N, Terauchi Y, Miki H et al. PPAR gamma mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol. Cell 4(4), 597-609 (1999). (Pubitemid 29531139)
12. Barak Y, Nelson MC, Ong ES et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell 4(4), 585-595 (1999). (Pubitemid 29531138)
13. Finucane MM, Stevens GA, Cowan MJ et al. National, regional, and global trends in body-mass index since 1980: Systematic analysis of health examination surveys and epidemiological studies with 960 countryyears and 9.1 million participants. Lancet 377(9765), 557-567 (2011).
14. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999-2010. JAMA 307(5), 483-490 (2012).
15. Shields M, Carroll MD, Ogden CL. Adult obesity prevalence in Canada and the United States. NCHS Data Brief (56), 1-8 (2011).
16. Katzmarzyk PT, Mason C. Prevalence of class I, II and III obesity in Canada. CMAJ 174(2), 156-157 (2006). (Pubitemid 43166264)
17. Williamson DF. Descriptive epidemiology of body weight and weight change in U.S. adults. Ann. Intern. Med. 119(7 Pt 2), 646-649 (1993). (Pubitemid 23313682)
18. Bergman RN, Stefanovski D, Buchanan TA et al. A better index of body adiposity. Obesity (Silver Spring) 19(5), 1083-1089 (2011).
19. Arsenault BJ, Beaumont EP, Despres JP, Larose E. Mapping body fat distribution: A key step towards the identification of the vulnerable patient? Ann. Med. doi:10.3109/0 .2011.605387 (2011) (Epub ahead of print).
20. Despres JP, Lemieux I. Abdominal obesity and metabolic syndrome. Nature 444(7121), 881-887 (2006). (Pubitemid 46024995)
21. Furnsinn C, Waldhausl W. Thiazolidinediones: Metabolic actions in vitro. Diabetologia 45(9), 1211-1223 (2002).
22. Gray SL, Vidal-Puig AJ. Adipose tissue expandability in the maintenance of metabolic homeostasis. Nutr. Rev. 65(6 Pt 2), S7-S12 (2007).
23. Medina-Gomez G, Virtue S, Lelliott C et al. The link between nutritional status and insulin sensitivity is dependent on the adipocyte-specific peroxisome proliferatoractivated receptor-gamma2 isoform. Diabetes 54(6), 1706-1716 (2005). (Pubitemid 40770761)
24. Zhang J, Fu M, Cui T et al. Selective disruption of PPARgamma 2 impairs the development of adipose tissue and insulin sensitivity. Proc. Natl Acad. Sci. USA 101(29), 10703-10708 (2004). (Pubitemid 38955806)
25. Giannini S, Serio M, Galli A. Pleiotropic effects of thiazolidinediones: Taking a look beyond antidiabetic activity. J. Endocrinol. Invest. 27(10), 982-991 (2004). (Pubitemid 40124199)
26. Semple RK, Chatterjee VK, O'Rahilly S. PPAR gamma and human metabolic disease. J. Clin. Invest. 116(3), 581-589 (2006). (Pubitemid 43326862)
27. Frayn KN. Adipose tissue as a buffer for daily lipid flux. Diabetologia 45(9), 1201-1210 (2002).
28. Reitman ML, Mason MM, Moitra J et al. Transgenic mice lacking white fat: Models for understanding human lipoatrophic diabetes. Ann. N Y Acad. Sci. 892, 289-296 (1999).
29. Veilleux A, Tchernof, A. Sex differences in body fat distribution. In: Adipose Tissue Biology. Symonds ME (Ed.). Springer, NY, USA, 123-166 (2012).
30. Spalding KL, Arner E, Westermark PO et al. Dynamics of fat cell turnover in humans. Nature 453(7196), 783-787 (2008). (Pubitemid 351793777)
31. Arner E, Westermark PO, Spalding KL et al. Adipocyte turnover: Relevance to human adipose tissue morphology. Diabetes 59(1), 105-109 (2010).
32. Arner P, Bernard S, Salehpour M et al. Dynamics of human adipose lipid turnover in health and metabolic disease. Nature 478(7367), 110-113 (2011).
33. Hauner H, Skurk T, Wabitsch M. Cultures of human adipose precursor cells. In: Adipose Tissue Protocols. Ailhaud G (Ed.). Humana Press, NY, USA, 239-247 (2001).
34. Bakker AH, van Dielen FM, Greve JW, Adam JA, Buurman WA. Preadipocyte number in omental and subcutaneous adipose tissue of obese individuals. Obes. Res. 12(3), 488-498 (2004). (Pubitemid 41132528)
35. Tchoukalova Y, Koutsari C, Jensen M. Committed subcutaneous preadipocytes are reduced in human obesity. Diabetologia 50(1), 151-157 (2007). (Pubitemid 46035863)
36. Roldan M, Macias-Gonzalez M, Garcia R, Tinahones FJ, Martin M. Obesity shortcircuits stemness red O network in human adipose multipotent stem cells. FASEB J. 25(12), 4111-4126 (2011).
37. Permana PA, Nair S, Lee YH, Luczy-Bachman G, Vozarova de Courten B, Tataranni PA. Subcutaneous abdominal preadipocyte differentiation in vitro inversely correlates with central obesity. Am. J. Physiol. Endocrinol. Metab. 286(6), e958-e962 (2004). (Pubitemid 38668818)
38. Isakson P, Hammarstedt A, Gustafson B, Smith U. Impaired preadipocyte differentiation in human abdominal obesity: Role of Wnt, tumor necrosis factor-alpha, and inflammation. Diabetes 58(7), 1550-1557 (2009).
39. van Harmelen V, Skurk T, Rohrig K et al. Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. Int. J. Obes. Relat. Metab. Disord. 27(8), 889-895 (2003). (Pubitemid 36918609)
40. Black MA, Begin-Heick N. Growth and maturation of primary-cultured adipocytes from lean and ob/ob mice. J. Cell. Biochem. 58(4), 455-463 (1995).
41. Shillabeer G, Forden JM, Russell JC, Lau DC. Paradoxically slow preadipocyte replication and differentiation in corpulent rats. Am. J. Physiol. 258(2 Pt 1), e368-e376 (1990). (Pubitemid 20094653)
42. Vohl MC, Sladek R, Robitaille J et al. A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. Obes. Res. 12(8), 1217-1222 (2004). (Pubitemid 41137463)
43. Tchernof A. Visceral adipocytes and the metabolic syndrome. Nutr. Rev. 65(6 Pt 2), S24-S29 (2007).
44. Tchernof A, Belanger C, Morisset AS et al. Regional differences in adipose tissue metabolism in women: Minor effect of obesity and body fat distribution. Diabetes 55(5), 1353-1360 (2006). (Pubitemid 44195374)
45. Drolet R, Richard C, Sniderman AD et al. Hypertrophy and hyperplasia of abdominal adipose tissues in women. Int. J. Obes. (Lond.) 32(2), 283-291 (2008). (Pubitemid 351271776)
46. Villaret A, Galitzky J, Decaunes P et al. Adipose tissue endothelial cells from obese human subjects: Differences among depots in angiogenic, metabolic, and inflammatory red O expression and cellular senescence. Diabetes 59(11), 2755-2763 (2010).
47. Veilleux A, Caron-Jobin M, Noel S, Laberge PY, Tchernof A. Visceral adipocyte hypertrophy is associated with dyslipidemia independent of body composition and fat distribution in women. Diabetes 60(5), 1504-1511 (2011).
48. Joe AW, Yi L, Even Y, Vogl AW, Rossi FM. Depot-specific differences in adipogenic progenitor abundance and proliferative response to high-fat diet. Stem Cells 27(10), 2563-2570 (2009).
49. Tchkonia T, Giorgadze N, Pirtskhalava T et al. Fat depot origin affects adipogenesis in primary cultured and cloned human preadipocytes. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282(5), R1286-R1296 (2002). (Pubitemid 34664512)
50. Baglioni S, Cantini G, Poli G et al. Functional differences in visceral and subcutaneous fat pads originate from differences in the adipose stem cell. PLoS ONE 7(5), e36569 (2012).
51. Blouin K, Nadeau M, Mailloux J et al. Pathways of adipose tissue androgen metabolism in women: Depot differences and modulation by adipogenesis. Am. J. Physiol. Endocrinol. Metab. 296(2), e244-e255 (2009).
52. Shahparaki A, Grunder L, Sorisky A. Comparison of human abdominal subcutaneous versus omental preadipocyte differentiation in primary culture. Metabolism 51(9), 1211-1215 (2002).
53. Tchoukalova YD, Koutsari C, Votruba SB et al. Sex- and depot-dependent differences in adipogenesis in normal-weight humans. Obesity (Silver Spring) 18(10), 1875-1880 (2010).
54. Tchoukalova YD, Votruba SB, Tchkonia T, Giorgadze N, Kirkland JL, Jensen MD. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc. Natl Acad. Sci. USA 107(42), 18226-18231 (2010).
55. Yang X, Jansson PA, Nagaev I et al. Evidence of impaired adipogenesis in insulin resistance. Biochem. Biophys. Res. Commun. 317(4), 1045-1051 (2004). (Pubitemid 38496415)
56. van Tienen FH, van der Kallen CJ, Lindsey PJ, Wanders RJ, van Greevenbroek MM, Smeets HJ. Preadipocytes of Type 2 diabetes subjects display an intrinsic red O expression profile of decreased differentiation capacity. Int. J. Obes. (Lond.) 35(9), 1154-1164 (2011).
57. Jansson PA, Pellme F, Hammarstedt A et al. A novel cellular marker of insulin resistance and early atherosclerosis in humans is related to impaired fat cell differentiation and low adiponectin. FASEB J. 17(11), 1434-1440 (2003). (Pubitemid 36935658)
58. Goedecke JH, Evans J, Keswell D et al. Reduced gluteal expression of adipogenic and lipogenic genes in Black South African women is associated with obesity-related insulin resistance. J. Clin. Endocrinol. Metab. 96(12), e2029-e2033 (2011).
59. Arner P, Arner E, Hammarstedt A, Smith U. Genetic predisposition for Type 2 diabetes, but not for overweight/obesity, is associated with a restricted adipogenesis. PLoS ONE 6(4), e18284 (2011).
60. Park HT, Lee ES, Cheon YP et al. The relationship between fat depot-specific preadipocyte differentiation and metabolic syndrome in obese women. Clin. Endocrinol. (Oxf.) 76(1), 59-66 (2012).
61. Shackleton S, Lloyd DJ, Jackson SN et al. LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat. Genet. 24(2), 153-156 (2000). (Pubitemid 30094715)
62. Dunnigan MG, Cochrane MA, Kelly A, Scott JW. Familial lipoatrophic diabetes with dominant transmission. A new syndrome. Q. J. Med. 43(169), 33-48 (1974).
63. Garg A, Peshock RM, Fleckenstein JL. Adipose tissue distribution pattern in patients with familial partial lipodystrophy (Dunnigan variety). J. Clin. Endocrinol. Metab. 84(1), 170-174 (1999). (Pubitemid 29036696)
64. Verstraeten VL, Renes J, Ramaekers FC et al. Reorganization of the nuclear lamina and cytoskeleton in adipogenesis. Histochem. Cell Biol. 135(3), 251-261 (2011).
65. Lelliott CJ, Logie L, Sewter CP et al. Lamin expression in human adipose cells in relation to anatomical site and differentiation state. J. Clin. Endocrinol. Metab. 87(2), 728-734 (2002). (Pubitemid 34158244)
66. Boguslavsky RL, Stewart CL, Worman HJ. Nuclear lamin A inhibits adipocyte differentiation: Implications for Dunnigantype familial partial lipodystrophy. Hum. Mol. Genet. 15(4), 653-663 (2006). (Pubitemid 43205428)
67. Kudlow BA, Jameson SA, Kennedy BK. HIV protease inhibitors block adipocyte differentiation independently of lamin A/C. AIDS 19(15), 1565-1573 (2005). (Pubitemid 41502668)
68. Nadeau M, Noel S, Laberge PY, Hurtubise J, Tchernof A. Adipose tissue lamin A/C messenger RNA expression in women. Metabolism 59(8), 1106-1114 (2010).
69. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferatoractivated receptor gamma (PPAR gamma). J. Biol Chem. 270(22), 12953-12956 (1995).
70. Kletzien RF, Clarke SD, Ulrich RG. Enhancement of adipocyte differentiation by an insulin-sensitizing agent. Mol. Pharmacol. 41(2), 393-398 (1992).
71. Deeb SS, Fajas L, Nemoto M et al. A Pro12Ala substitution in PPARgamma2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nat. Genet. 20(3), 284-287 (1998). (Pubitemid 28507675)
72. He W. PPARgamma2 polymorphism and human health. PPAR Res. 849538 (2009) (2009).
73. Gouda HN, Sagoo GS, Harding AH, Yates J, Sandhu MS, Higgins JP. The association between the peroxisome proliferator-activated receptor-gamma2 (PPARG2) Pro12Ala red O variant and Type 2 diabetes mellitus: A HuGE review and meta-analysis. Am. J. Epidemiol. 171(6), 645-655 (2010).
74. Altshuler D, Hirschhorn JN, Klannemark M et al. The common PPARgamma Pro12Ala polymorphism is associated with decreased risk of Type 2 diabetes. Nat. Genet. 26(1), 76-80 (2000).
75. Memisoglu A, Hu FB, Hankinson SE et al. Interaction between a peroxisome proliferatoractivated receptor gamma red O polymorphism and dietary fat intake in relation to body mass. Hum. Mol. Genet. 12(22), 2923-2929 (2003). (Pubitemid 37442020)
76. Robitaille J, Perusse L, Bouchard C, Vohl MC. Genes, fat intake, and cardiovascular disease risk factors in the Quebec Family Study. Obesity (Silver Spring) 15(9), 2336-2347 (2007). (Pubitemid 350004102)
77. Ruchat SM, Weisnagel SJ, Vohl MC, Rankinen T, Bouchard C, Perusse L. Evidence for interaction between PPARG Pro12Ala and PPARGC1A Gly482Ser polymorphisms in determining Type 2 diabetes intermediate phenotypes in overweight subjects. Exp. Clin. Endocrinol. Diabetes 117(9), 455-459 (2009).
78. Bouchard-Mercier A, Paradis AM, Perusse L, Vohl MC. Associations between polymorphisms in genes involved in fatty acid metabolism and dietary fat intakes. J. Nutrigenet. Nutrigenomics 5(1), 1-12 (2012).
79. Abella A, Dubus P, Malumbres M et al. Cdk4 promotes adipogenesis through PPARgamma activation. Cell Metab. 2(4), 239-249 (2005).
80. Tsutsui T, Hesabi B, Moons DS et al. Targeted disruption of CDK4 delays cell cycle entry with enhanced p27(Kip1) activity. Mol. Cell Biol. 19(10), 7011-7019 (1999). (Pubitemid 29441883)
81. Meenakshisundaram R, Gragnoli C. CDK4 IVS4-nt40 AA genotype and obesityassociated tumors/cancer in Italians - A case-control study. J. Exp. Clin. Cancer Res. 28, 42 (2009).
82. Meenakshisundaram R, Gragnoli C. CDK4 IVS4-nt40G->A and T2D-associated obesity in Italians. J. Cell. Physiol. 221(2), 273-275 (2009).
83. Laudes M. Role of WNT signalling in the determination of human mesenchymal stem cells into preadipocytes. J. Mol. Endocrinol. 46(2), R65-R72 (2011).
84. Kanazawa A, Tsukada S, Sekine A et al. Association of the red O encoding wingless-type mammary tumor virus integration-site family member 5B (WNT5B) with Type 2 diabetes. Am. J. Hum. Genet. 75(5), 832-843 (2004). (Pubitemid 39390490)
85. Salpea KD, Gable DR, Cooper JA et al. The effect of WNT5B IVS3C>G on the susceptibility to Type 2 diabetes in UK caucasian subjects. Nutr. Metab. Cardiovasc. Dis 19(2), 140-145 (2009).
86. Kanazawa A, Kawamura Y, Sekine A et al. Single nucleotide polymorphisms in the red O encoding Kruppel-like factor 7 are associated with Type 2 diabetes. Diabetologia 48(7), 1315-1322 (2005). (Pubitemid 41186096)
87. Zobel DP, Andreasen CH, Burgdorf KS et al. Variation in the red O encoding Kruppel factor 7 influences body fat: Studies of 14 818 Danes. Eur. J. Endocrinol. 160(4), 603-609 (2009).
88. Hegele RA, Anderson C, Young TK, Connelly PW. G-protein beta3 subunit red O splice variant and body fat distribution in Nunavut Inuit. Genome Res. 9(10), 972-977 (1999). (Pubitemid 29525205)
89. Nishizuka M, Honda K, Tsuchiya T, Nishihara T, Imagawa M. RGS2 promotes adipocyte differentiation in the presence of ligand for peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 276(32), 29625-29627 (2001).
90. Freson K, Stolarz K, Aerts R et al. -391 C to G substitution in the regulator of G-protein signalling-2 promoter increases susceptibility to the metabolic syndrome in white European men: Consistency between molecular and epidemiological studies. J. Hypertens. 25(1), 117-125 (2007). (Pubitemid 44885672)
91. Neels JG, Olefsky JM. Inflamed fat: What starts the fire? J. Clin. Invest. 116(1), 33-35 (2006). (Pubitemid 43121788)
92. Tilg H, Moschen AR. Adipocytokines: Mediators linking adipose tissue, inflammation and immunity. Nat. Rev. Immunol. 6(10), 772-783 (2006). (Pubitemid 44453463)
93. Winkler G, Kiss S, Keszthelyi L et al. Expression of tumor necrosis factor (TNF)-alpha protein in the subcutaneous and visceral adipose tissue in correlation with adipocyte cell volume, serum TNF-alpha, soluble serum TNF-receptor-2 concentrations and C-peptide level. Eur. J. Endocrinol. 149(2), 129-135 (2003). (Pubitemid 36987155)
94. Chavey C, Mari B, Monthouel MN et al. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J. Biol. Chem. 278(14), 11888-11896 (2003). (Pubitemid 36800160)
95. Lijnen HR, Maquoi E, Hansen LB, Van Hoef B, Frederix L, Collen D. Matrix metalloproteinase inhibition impairs adipose tissue development in mice. Arterioscler. Thromb. Vasc. Biol. 22(3), 374-379 (2002). (Pubitemid 34218741)
96. Poulain-Godefroy O, Lecoeur C, Pattou F, Fruhbeck G, Froguel P. Inflammation is associated with a decrease of lipogenic factors in omental fat in women. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295(1), R1-R7 (2008).
97. Quinkler M, Bujalska IJ, Tomlinson JW, Smith DM, Stewart PM. Depot-specific prostaglandin synthesis in human adipose tissue: A novel possible mechanism of adipogenesis. Gene 380(2), 137-143 (2006). (Pubitemid 44363149)
98. Sewter CP, Blows F, Vidal-Puig A, O'Rahilly S. Regional differences in the response of human pre-adipocytes to PPARgamma and RXRalpha agonists. Diabetes 51(3), 718-723 (2002). (Pubitemid 34760181)
99. Kolehmainen M, Uusitupa MIJ, Alhava E, Laakso M, Vidal H. Effect of the Pro12Ala polymorphism in the peroxisome proliferator-activated receptor (PPAR) g2 red O on the expression of PPARg target genes in adipose tissue of massively obese subjects. J. Clin. Endocrinol. Metab. 88(4), 1717-1722 (2003). (Pubitemid 36623394)
100. Montague CT, Prins JB, Sanders L et al. Depot-related red O expression in human subcutaneous and omental adipocytes. Diabetes 47(9), 1384-1391 (1998). (Pubitemid 28396940)
101. Ruschke K, Fishbein L, Dietrich A et al. Red O expression of PPARgamma and PGC-1alpha in human omental and subcutaneous adipose tissues is related to insulin resistance markers and mediates beneficial effects of physical training. Eur. J. Endocrinol. 162(3), 515-523 (2010).