Female Mice are Protected against High-Fat Diet Induced Metabolic Syndrome and Increase the Regulatory T Cell Population in Adipose Tissue

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Pettersson, Ulrika S ^a   Waldén, Tomas B ^a   Carlsson, Per Ola ^a   Jansson, Leif ^a   Phillipson, Mia ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; GLUCOSE; INSULIN; INTERLEUKIN 10; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; MESSENGER RNA; TRANSCRIPTION FACTOR FOXP3; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; BODY FAT DISTRIBUTION; BODY WEIGHT; CELL POPULATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INTRAABDOMINAL FAT; LIPID DIET; LYMPHOCYTE COUNT; MALE; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PANCREAS ISLET CELL FUNCTION; PANCREAS ISLET DISEASE; PANCREAS ISLET HYPERTROPHY; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; SEX DIFFERENCE; SOFT TISSUE INFLAMMATION; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN;

ADIPOSE TISSUE; ANIMALS; DIET, HIGH-FAT; FEMALE; MACROPHAGES; MALE; METABOLIC SYNDROME X; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES, REGULATORY;

MUS;

EID: 84866706026     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046057     Document Type: Article

References (56)

1. Dandona P, Aljada A, Bandyopadhyay A, (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25: 4-7.
2. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, et al. (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881-885.
3. Reaven G, (2002) Metabolic syndrome: pathophysiology and implications for management of cardiovascular disease. Circulation 106: 286-288.
4. Wellen KE, Hotamisligil GS, (2005) Inflammation, stress, and diabetes. J Clin Invest 115: 1111-1119.
5. Straczkowski M, Dzienis-Straczkowska S, Stepien A, Kowalska I, Szelachowska M, et al. (2002) Plasma interleukin-8 concentrations are increased in obese subjects and related to fat mass and tumor necrosis factor-alpha system. J Clin Endocrinol Metab 87: 4602-4606.
6. Popko K, Gorska E, Stelmaszczyk-Emmel A, Plywaczewski R, Stoklosa A, et al. (2010) Proinflammatory cytokines Il-6 and TNF-alpha and the development of inflammation in obese subjects. Eur J Med Res 15Suppl 2: 120-122.
7. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
8. Lumeng CN, Bodzin JL, Saltiel AR, (2007) Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 117: 175-184.
9. Carlsson PO, Andersson A, Jansson L, (1996) Pancreatic islet blood flow in normal and obese-hyperglycemic (ob/ob) mice. Am J Physiol 271: E990-995.
10. Pettersson US, Henriksnas J, Jansson L, (2009) Reversal of high pancreatic islet and white adipose tissue blood flow in type 2 diabetic GK rats by administration of the beta3-adrenoceptor inhibitor SR-59230A. Am J Physiol Endocrinol Metab 297: E490-494.
11. Carlsson PO, Jansson L, Ostenson CG, Kallskog O, (1997) Islet capillary blood pressure increase mediated by hyperglycemia in NIDDM GK rats. Diabetes 46: 947-952.
12. Lammert E, (2008) The vascular trigger of type II diabetes mellitus. Exp Clin Endocrinol Diabetes 116Suppl 1: S21-25.
13. Carlsson PO, Andersson A, Jansson L, (1998) Influence of age, hyperglycemia, leptin, and NPY on islet blood flow in obese-hyperglycemic mice. Am J Physiol 275: E594-601.
14. Svensson AM, Hellerstrom C, Jansson L, (1996) Diet-induced obesity and pancreatic islet blood flow in the rat: a preferential increase in islet blood perfusion persists after withdrawal of the diet and normalization of body weight. J Endocrinol 151: 507-511.
15. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, et al. (2003) Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52: 102-110.
16. Butler AE, Cao-Minh L, Galasso R, Rizza RA, Corradin A, et al. (2010) Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 53: 2167-2176.
17. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC, (2008) Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 10Suppl 4: 32-42.
18. Rhodes CJ, (2005) Type 2 diabetes-a matter of beta-cell life and death? Science 307: 380-384.
19. Shi H, Clegg DJ, (2009) Sex differences in the regulation of body weight. Physiol Behav 97: 199-204.
20. Chan JC, Cheung JC, Stehouwer CD, Emeis JJ, Tong PC, et al. (2002) The central roles of obesity-associated dyslipidaemia, endothelial activation and cytokines in the Metabolic Syndrome-an analysis by structural equation modelling. Int J Obes Relat Metab Disord 26: 994-1008.
21. Kocak H, Oner-Iyidogan Y, Gurdol F, Oner P, Suzme R, et al. (2007) Advanced oxidation protein products in obese women: its relation to insulin resistance and resistin. Clin Exp Med 7: 173-178.
22. Nilsson BO, (2007) Modulation of the inflammatory response by estrogens with focus on the endothelium and its interactions with leukocytes. Inflamm Res 56: 269-273.
23. Cushman M, Legault C, Barrett-Connor E, Stefanick ML, Kessler C, et al. (1999) Effect of postmenopausal hormones on inflammation-sensitive proteins: the Postmenopausal Estrogen/Progestin Interventions (PEPI) Study. Circulation 100: 717-722.
24. Payette C, Blackburn P, Lamarche B, Tremblay A, Bergeron J, et al. (2009) Sex differences in postprandial plasma tumor necrosis factor-alpha, interleukin-6, and C-reactive protein concentrations. Metabolism 58: 1593-1601.
25. Register TC, Cann JA, Kaplan JR, Williams JK, Adams MR, et al. (2005) Effects of soy isoflavones and conjugated equine estrogens on inflammatory markers in atherosclerotic, ovariectomized monkeys. J Clin Endocrinol Metab 90: 1734-1740.
26. Kampf C, Bodin B, Kallskog O, Carlsson C, Jansson L, (2005) Marked increase in white adipose tissue blood perfusion in the type 2 diabetic GK rat. Diabetes 54: 2620-2627.
27. Jansson L, Hellerstrom C, (1981) A rapid method of visualizing the pancreatic islets for studies of islet capillary blood flow using non-radioactive microspheres. Acta Physiol Scand 113: 371-374.
28. Andersson A, (1978) Isolated mouse pancreatic islets in culture: effects of serum and different culture media on the insulin production of the islets. Diabetologia 14: 397-404.
29. Bastard JP, Jardel C, Bruckert E, Blondy P, Capeau J, et al. (2000) Elevated levels of interleukin 6 are reduced in serum and subcutaneous adipose tissue of obese women after weight loss. J Clin Endocrinol Metab 85: 3338-3342.
30. Hotamisligil GS, Shargill NS, Spiegelman BM, (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259: 87-91.
31. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, et al. (2005) Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res 46: 2347-2355.
32. Deiuliis J, Shah Z, Shah N, Needleman B, Mikami D, et al. (2011) Visceral adipose inflammation in obesity is associated with critical alterations in tregulatory cell numbers. PLoS One 6: e16376.
33. Louet JF, LeMay C, Mauvais-Jarvis F, (2004) Antidiabetic actions of estrogen: insight from human and genetic mouse models. Curr Atheroscler Rep 6: 180-185.
34. Lundholm L, Bryzgalova G, Gao H, Portwood N, Falt S, et al. (2008) The estrogen receptor {alpha}-selective agonist propyl pyrazole triol improves glucose tolerance in ob/ob mice; potential molecular mechanisms. J Endocrinol 199: 275-286.
35. Riant E, Waget A, Cogo H, Arnal JF, Burcelin R, et al. (2009) Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150: 2109-2117.
36. Tesone M, Chazenbalk GD, Ballejos G, Charreau EH, (1979) Estrogen receptor in rat pancreatic islets. J Steroid Biochem 11: 1309-1314.
37. SutterDub MT, (1976) Preliminary report: effects of female sex hormones on insulin secretion by the perfused rat pancreas. J Physiol (Paris) 72: 795-800.
38. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, et al. (2007) Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317: 121-124.
39. Pickup JC, Mattock MB, Chusney GD, Burt D, (1997) NIDDM as a disease of the innate immune system: association of acute-phase reactants and interleukin-6 with metabolic syndrome X. Diabetologia. 40: 1286-1292.
40. Akira S, Taga T, Kishimoto T, (1993) Interleukin-6 in biology and medicine. Adv Immunol 54: 1-78.
41. Vozarova B, Weyer C, Hanson K, Tataranni PA, Bogardus C, et al. (2001) Circulating interleukin-6 in relation to adiposity, insulin action, and insulin secretion. Obes Res 9: 414-417.
42. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM, (2001) C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286: 327-334.
43. Bastard JP, Maachi M, Van Nhieu JT, Jardel C, Bruckert E, et al. (2002) Adipose tissue IL-6 content correlates with resistance to insulin activation of glucose uptake both in vivo and in vitro. J Clin Endocrinol Metab 87: 2084-2089.
44. Tsigos C, Papanicolaou DA, Kyrou I, Defensor R, Mitsiadis CS, et al. (1997) Dose-dependent effects of recombinant human interleukin-6 on glucose regulation. J Clin Endocrinol Metab 82: 4167-4170.
45. Fenton JI, Nunez NP, Yakar S, Perkins SN, Hord NG, et al. (2009) Diet-induced adiposity alters the serum profile of inflammation in C57BL/6N mice as measured by antibody array. Diabetes Obes Metab 11: 343-354.
46. Neels JG, Badeanlou L, Hester KD, Samad F, (2009) Keratinocyte-derived chemokine in obesity: expression, regulation, and role in adipose macrophage infiltration and glucose homeostasis. J Biol Chem 284: 20692-20698.
47. Galli SJ, Borregaard N, Wynn TA, (2011) Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol 12: 1035-1044.
48. Chawla A, Nguyen KD, Goh YP (2011) Macrophage-mediated inflammation in metabolic disease. Nat Rev Immunol.
49. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, et al. (2009) Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 15: 930-939.
50. De Rosa V, Procaccini C, Cali G, Pirozzi G, Fontana S, et al. (2007) A key role of leptin in the control of regulatory T cell proliferation. Immunity 26: 241-255.
51. Winer S, Chan Y, Paltser G, Truong D, Tsui H, et al. (2009) Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15: 921-929.
52. van der Weerd K, Dik WA, Schrijver B, Schweitzer DH, Langerak AW, et al. (2012) Morbidly obese human subjects have increased peripheral blood CD4+ T cells with skewing toward a Treg- and Th2-dominated phenotype. Diabetes 61: 401-408.
53. Eller K, Kirsch A, Wolf AM, Sopper S, Tagwerker A, et al. (2011) Potential role of regulatory T cells in reversing obesity-linked insulin resistance and diabetic nephropathy. Diabetes 60: 2954-2962.
54. Tschen SI, Dhawan S, Gurlo T, Bhushan A, (2009) Age-dependent decline in beta-cell proliferation restricts the capacity of beta-cell regeneration in mice. Diabetes 58: 1312-1320.
55. Skau M, Pakkenberg B, Buschard K, Bock T, (2001) Linear correlation between the total islet mass and the volume-weighted mean islet volume. Diabetes 50: 1763-1770.
56. Dor Y, Brown J, Martinez OI, Melton DA, (2004) Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-46.