Sex differences during the course of diet-induced obesity in mice: Adipose tissue expandability and glycemic control

International Journal of Obesity

Volumn 36, Issue 2, 2012, Pages 262-272

  Medrikova, D ^a   Jilkova, Z M ^a   Bardova, K ^a   Janovska, P ^a   Rossmeisl, M ^a   Kopecky, J ^a  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

Author keywords

adipose tissue expandability; inflammation; insulin sensitivity; mice; sex differences

Indexed keywords

ADIPONECTIN; GLUCOSE; LIPID;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL INFILTRATION; CELL SIZE; CONTROLLED STUDY; DIET; FATTY LIVER; FEMALE; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; GLYCEMIC CONTROL; INFLAMMATION; LIPID BLOOD LEVEL; LIPID DIET; LIPID STORAGE; MACROPHAGE; MALE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SEX DIFFERENCE; TISSUE EXPANSION; TISSUE STRUCTURE; WEIGHT GAIN;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL MARKERS; BLOOD GLUCOSE; DIET, HIGH-FAT; ELASTICITY; FEMALE; GLUCOSE TOLERANCE TEST; IMMUNOHISTOCHEMISTRY; LIPIDS; MALE; MICE; MICE, INBRED C57BL; OBESITY; SEX FACTORS; WEIGHT GAIN;

MUS;

EID: 84857051608     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2011.87     Document Type: Article

References (60)

1. Krotkiewski M, Bjorntorp P, Sjostrom L, Smith U. Impact of obesity on metabolism in men and women. Importance of regional adipose tissue distribution. J Clin Invest 1983; 72: 1150-1162. (Pubitemid 14212633)
2. Frias JP, Macaraeg GB, Ofrecio J, Yu JG, Olefsky JM, Kruszynska YT. Decreased susceptibility to fatty acid-induced peripheral tissue insulin resistance in women. Diabetes 2001; 50: 1344-1350. (Pubitemid 32500167)
3. Priego T, Sanchez J, Pico C, Palou A. Sex-differential expression of metabolism-related genes in response to a high-fat diet. Obesity (Silver Spring) 2008; 16: 819-826. (Pubitemid 351465638)
4. Guerre-Millo M, Leturque A, Girard J, Lavau M. Increased insulin sensitivity and responsiveness of glucose metabolism in adipocytes from female versus male rats. J Clin Invest 1985; 76: 109-116. (Pubitemid 15240424)
5. Hevener A, Reichart D, Janez A, Olefsky J. Female rats do not exhibit free fatty acid-induced insulin resistance. Diabetes 2002; 51: 1907-1912. (Pubitemid 34564305)
6. Trevaskis JL, Meyer EA, Galgani JE, Butler AA. Counterintuitive effects of double-heterozygous null melanocortin-4 receptor and leptin genes on diet-induced obesity and insulin resistance in C57BL/6J mice. Endocrinology 2008; 149: 174-184.
7. Macotela Y, Boucher J, Tran TT, Kahn CR. Sex and depot differences in adipocyte insulin sensitivity and glucose metabolism. Diabetes 2009; 58: 803-812.
8. Wajchenberg BL. Subcutaneous and visceral adipose tissue: Their relation to the metabolic syndrome. Endocr Rev 2000; 21: 697-738. (Pubitemid 32113289)
9. Cnop M, Landchild MJ, Vidal J, Havel PJ, Knowles NG, Carr DR et al. The concurrent accumulation of intra-Abdominal and subcutaneous fat explains the association between insulin resistance and plasma leptin concentrations: Distinct metabolic effects of two fat compartments. Diabetes 2002; 51: 1005-1015. (Pubitemid 34438343)
10. Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, Zurlo F. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 1986; 44: 739-746. (Pubitemid 17208993)
11. Clegg DJ, Brown LM, Woods SC, Benoit SC. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 2006; 55: 978-987. (Pubitemid 44100172)
12. Arner E,Westermark PO, Spalding KL, Britton T, Ryden M, Frisen J et al. Adipocyte turnover: Relevance to human adipose tissue morphology. Diabetes 2010; 59: 105-109.
13. Okuno A, Tamemoto H, Tobe K, Ueki K, Mori Y, Iwamoto K et al. Troglitazone increases the number of small adipocytes without the change of white adipose tissue mass in obese zucker rats. J Clin Invest 1998; 101: 1354-1361. (Pubitemid 28145252)
14. Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, Komeda K et al. PPAR gamma mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 1999; 4: 597-609. (Pubitemid 29531139)
15. Danforth Jr. E. Failure of adipocyte differentiation causes type II diabetes mellitus? Nat Genet 2000; 26: 13.
16. Virtue S, Vidal-Puig A. It's not how fat you are, it's what you do with it that counts. PLoS Biol 2008; 6: E237.
17. Khan T, Muise ES, Iyengar P,Wang ZV, ChandaliaM, Abate N et al. Metabolic dysregulation and adipose tissue fibrosis: Role of collagen VI. Mol Cell Biol 2009; 29: 1575-1591.
18. Halberg N, Khan T, Trujillo ME, Wernstedt-Asterholm I, Attie AD, Sherwani S et al. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol 2009; 29: 4467-4483.
19. Grove KL, Fried SK, Greenberg AS, Xiao XQ, Clegg DJ. A microarray analysis of sexual dimorphism of adipose tissues in high-fat-diet-induced obese mice. Int J Obes (Lond) 2010; 34: 989-1000.
20. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R et al. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 2006; 116: 1494-1505.
21. Kamei N, Tobe K, Suzuki R, Ohsugi M,Watanabe T, Kubota N et al. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 2006; 281: 26602-26614. (Pubitemid 44401869)
22. Anderson EK, Gutierrez DA, Hasty AH. Adipose tissue recruitment of leukocytes. Curr Opin Lipidol 2010; 21: 172-177.
23. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117: 175-184. (Pubitemid 46048464)
24. Lumeng CN, Delproposto JB, Westcott DJ, Saltiel AR. Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 2008; 57: 3239-3246.
25. Hotamisligil GS, Murray DL, Choy LN, Spiegelman BM. Tumor necrosis factor alpha inhibits signaling from the insulin receptor. Proc Natl Acad Sci USA 1994; 91: 4854-4858. (Pubitemid 24177748)
26. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112: 1821-1830. (Pubitemid 38063705)
27. de Luca C, Olefsky JM. Inflammation and insulin resistance. FEBS Lett 2008; 582: 97-105. (Pubitemid 50010731)
28. Strissel KJ, Stancheva Z, Miyoshi H, Perfield JW, DeFuria J, Jick Z et al. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes 2007; 56: 2910-2918. (Pubitemid 350223625)
29. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 2005; 46: 2347-2355. (Pubitemid 41532523)
30. Monteiro R, de Castro PMST, Calhau C, Azevedo I. Adipocyte size and liability to cell death. Obesity Surgery 2006; 16: 804-806. (Pubitemid 43874842)
31. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S et al. Adiponectin stimulates glucose utilization and fatty-Acid oxidation by activating AMP-Activated protein kinase. Nat Med 2002; 8: 1288-1295. (Pubitemid 35373562)
32. Carling D. The AMP-Activated protein kinase cascade-A unifying system for energy control. Trends Biochem Sci 2004; 29: 18-24. (Pubitemid 38068476)
33. Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y et al. Plasma concentrations of a novel, adiposespecific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol 2000; 20: 1595-1599. (Pubitemid 30353893)
34. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 2001; 7: 947-953. (Pubitemid 32756433)
35. Yamauchi T, Kamon J,Waki H, Terauchi Y, Kubota N, Hara K et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 2001; 7: 941-946. (Pubitemid 32756432)
36. Kim JY, van de WE, Laplante M, Azzara A, Trujillo ME, Hofmann SM et al. Obesity-Associated improvements in metabolic profile through expansion of adipose tissue. J Clin Invest 2007; 117: 2621-2637. (Pubitemid 47494363)
37. Okamoto Y, Kihara S, Ouchi N, Nishida M, Arita Y, Kumada M et al. Adiponectin reduces atherosclerosis in apolipoprotein E-deficient mice. Circulation 2002; 106: 2767-2770. (Pubitemid 35396973)
38. Cancello R, Tordjman J, Poitou C, Guilhem G, Bouillot JL, Hugol D et al. Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 2006; 55: 1554-1561. (Pubitemid 44324107)
39. Tordjman J, Guerre-Millo M, Clement K. Adipose tissue inflammation and liver pathology in human obesity. Diabetes Metab 2008; 34: 658-663.
40. Hou XG, Moser S, Sarr MG, Thompson GB, Que FG, Jensen MD. Visceral and subcutaneous adipose tissue diacylglycerol acyltransferase activity in humans. Obesity (Silver Spring) 2009; 17: 1129-1134.
41. Kuda O, Jelenik T, Jilkova Z, Flachs P, Rossmeisl M, Hensler M et al. n-3 Fatty acids and rosiglitazone improve insulin sensitivity through additive stimulatory effects on muscle glycogen synthesis in mice fed a high-fat diet. Diabetologia 2009; 52: 941-951.
42. Cinti S. The Adipose Organ. Editrice Kurtis: Milano, Italy, 1999.
43. Polak J, Kovacova Z, Jacek M, Klimcakova E, Kovacikova M, Vitkova M et al. An increase in plasma adiponectin multimeric complexes follows hypocaloric diet-induced weight loss in obese and overweight pre-menopausal women. Clin Sci (Lond) 2007; 112: 557-565. (Pubitemid 46849546)
44. Rossmeisl M, Jelenik T, Jilkova Z, Slamova K, Kus V, Hensler M et al. Prevention and reversal of obesity and glucose intolerance in mice by DHA-derivatives. Obesity (Silver Spring) 2009; 17: 1023-1031.
45. Ruzickova J, Rossmeisl M, Prazak T, Flachs P, Sponarova J, Vecka M et al. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids 2004; 39: 1177-1185.
46. Viollet B, Andreelli F, Jorgensen SB, Perrin C, Geloen A, Flamez D et al. The AMP-Activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J Clin Invest 2003; 111: 91-98. (Pubitemid 36134852)
47. Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S, Kita S et al. Impaired multimerization of human adiponectin mutants associated with diabetes -Molecular structure and multimer formation of adiponectin. J Biol Chem 2003; 278: 40352-40363. (Pubitemid 37248604)
48. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2006; 116: 115-124. (Pubitemid 43121796)
49. Law IK, Xu A, Lam KS, Berger T, Mak TW, Vanhoutte PM et al. Lipocalin-2 deficiency attenuates insulin resistance associated with aging and obesity. Diabetes 2010; 59: 872-882.
50. Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-Alpha: Direct role in obesity-linked insulin resistance. Science 1993; 259: 87-91. (Pubitemid 23036092)
51. Takahashi K, Mizuarai S, Araki H, Mashiko S, Ishihara A, Kanatani A et al. Adiposity elevates plasma MCP-1 levels leading to the increased CD11b-positive monocytes in mice. J Biol Chem 2003; 278: 46654-46660. (Pubitemid 37452242)
52. Inouye KE, Shi H, Howard JK, Daly CH, Lord GM, Rollins BJ et al. Absence of CC chemokine ligand 2 does not limit obesityassociated infiltration of macrophages into adipose tissue. Diabetes 2007; 56: 2242-2250. (Pubitemid 47358231)
53. Ghisletti S, Meda C, Maggi A, Vegeto E. 17beta-estradiol inhibits inflammatory gene expression by controlling NF-kappaB intracellular localization. Mol Cell Biol 2005; 25: 2957-2968. (Pubitemid 40464301)
54. Vegeto E, Belcredito S, Etteri S, Ghisletti S, Brusadelli A, Meda C et al. Estrogen receptor-Alpha mediates the brain antiinflammatory activity of estradiol. Proc Natl Acad Sci USA 2003; 100: 9614-9619. (Pubitemid 37033976)
55. Combs TP, Berg AH, Rajala MW, Klebanov S, Iyengar P, Jimenez-Chillaron JC et al. Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 2003; 52: 268-276. (Pubitemid 36173178)
56. Combs TP, Pajvani UB, Berg AH, Lin Y, Jelicks LA, Laplante M et al. A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology 2004; 145: 367-383. (Pubitemid 38094532)
57. Spranger J, Kroke A, Mohlig M, Bergmann MM, Ristow M, Boeing H et al. Adiponectin and protection against type 2 diabetes mellitus. Lancet 2003; 361: 226-228. (Pubitemid 36126226)
58. Snijder MB, Heine RJ, Seidell JC, Bouter LM, Stehouwer CD, Nijpels G et al. Associations of adiponectin levels with incident impaired glucose metabolism and type 2 diabetes in older men and women: The hoorn study. Diabetes Care 2006; 29: 2498-2503. (Pubitemid 44912259)
59. Ohashi K, Parker JL, Ouchi N, Higuchi A, Vita JA, Gokce N et al. Adiponectin promotes macrophage polarization toward an antiinflammatory phenotype. J Biol Chem 2010; 285: 6153-6160.
60. Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O et al. Dynamics of fat cell turnover in humans. Nature 2008; 453: 783-787. (Pubitemid 351793777)