Experimental hyperglycemia induces an increase of monocyte and T-lymphocyte content in adipose tissue of healthy obese women

. 2015 ; 10 (3) : e0122872. [epub] 20150420

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu klinická studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25894202

BACKGROUND/OBJECTIVES: Hyperglycemia represents one of possible mediators for activation of immune system and may contribute to worsening of inflammatory state associated with obesity. The aim of our study was to investigate the effect of a short-term hyperglycemia (HG) on the phenotype and relative content of immune cells in circulation and subcutaneous abdominal adipose tissue (SAAT) in obese women without metabolic complications. SUBJECTS/METHODS: Three hour HG clamp with infusion of octreotide and control investigations with infusion of octreotide or saline were performed in three groups of obese women (Group1: HG, Group 2: Octreotide, Group 3: Saline, n=10 per group). Before and at the end of the interventions, samples of SAAT and blood were obtained. The relative content of immune cells in blood and SAAT was determined by flow cytometry. Gene expression analysis of immunity-related markers in SAAT was performed by quantitative real-time PCR. RESULTS: In blood, no changes in analysed immune cell population were observed in response to HG. In SAAT, HG induced an increase in the content of CD206 negative monocytes/macrophages (p<0.05) and T lymphocytes (both T helper and T cytotoxic lymphocytes, p<0.01). Further, HG promoted an increase of mRNA levels of immune response markers (CCL2, TLR4, TNFα) and lymphocyte markers (CD3g, CD4, CD8a, TBX21, GATA3, FoxP3) in SAAT (p<0.05 and 0.01). Under both control infusions, none of these changes were observed. CONCLUSIONS: Acute HG significantly increased the content of monocytes and lymphocytes in SAAT of healthy obese women. This result suggests that the short-term HG can modulate an immune status of AT in obese subjects.

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Heilbronn LK, Campbell LV (2008) Adipose tissue macrophages, low grade inflammation and insulin resistance in human obesity. Curr Pharm Des 14: 1225–1230. PubMed

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. 10.1097/MCO.0b013e32833aab7f PubMed DOI

Cancello R, Tordjman J, Poitou C, Guilhem G, Bouillot JL, Hugol D, et al. (2006) Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 55: 1554–1561. PubMed

Klimcakova E, Roussel B, Kovacova Z, Kovacikova M, Siklova-Vitkova M, Combes M, et al. (2011) Macrophage gene expression is related to obesity and the metabolic syndrome in human subcutaneous fat as well as in visceral fat. Diabetologia 54: 876–887. 10.1007/s00125-010-2014-3 PubMed DOI

Elbein SC, Kern PA, Rasouli N, Yao-Borengasser A, Sharma NK, Das SK (2011) Global gene expression profiles of subcutaneous adipose and muscle from glucose-tolerant, insulin-sensitive, and insulin-resistant individuals matched for BMI. Diabetes 60: 1019–1029. 10.2337/db10-1270 PubMed DOI PMC

Hardy OT, Perugini RA, Nicoloro SM, Gallagher-Dorval K, Puri V, Straubhaar J, et al. (2011) Body mass index-independent inflammation in omental adipose tissue associated with insulin resistance in morbid obesity. Surg Obes Relat Dis 7: 60–67. 10.1016/j.soard.2010.05.013 PubMed DOI PMC

McLaughlin T, Deng A, Gonzales O, Aillaud M, Yee G, Lamendola C, et al. (2008) Insulin resistance is associated with a modest increase in inflammation in subcutaneous adipose tissue of moderately obese women. Diabetologia 51: 2303–2308. 10.1007/s00125-008-1148-z PubMed DOI PMC

Knowler WC, Barrett-Connor E, Fowler SE, Hamman RF, Lachin JM, Walker EA, et al. (2002) Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 346: 393–403. PubMed PMC

Weyer C, Bogardus C, Mott DM, Pratley RE (1999) The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J Clin Invest 104: 787–794. PubMed PMC

Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, et al. (2006) Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA 295: 1681–1687. PubMed

Marfella R, Quagliaro L, Nappo F, Ceriello A, Giugliano D (2001) Acute hyperglycemia induces an oxidative stress in healthy subjects. J Clin Invest 108: 635–636. PubMed PMC

Hofmann MA, Schiekofer S, Kanitz M, Klevesath MS, Joswig M, Lee V, et al. (1998) Insufficient glycemic control increases nuclear factor-kappa B binding activity in peripheral blood mononuclear cells isolated from patients with type 1 diabetes. Diabetes Care 21: 1310–1316. PubMed

Chen H (2006) Cellular inflammatory responses: novel insights for obesity and insulin resistance. Pharmacol Res 53: 469–477. PubMed

Faraj M, Beauregard G, Tardif A, Loizon E, Godbout A, Cianflone K, et al. (2008) Regulation of leptin, adiponectin and acylation-stimulating protein by hyperinsulinaemia and hyperglycaemia in vivo in healthy lean young men. Diabetes Metab 34: 334–342. 10.1016/j.diabet.2008.01.014 PubMed DOI

Dasu MR, Devaraj S, Park S, Jialal I (2010) Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care 33: 861–868. 10.2337/dc09-1799 PubMed DOI PMC

Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366: 1059–1062. PubMed

Klimcakova E, Polak J, Moro C, Hejnova J, Majercik M, Viguerie N, et al. (2006) Dynamic strength training improves insulin sensitivity without altering plasma levels and gene expression of adipokines in subcutaneous adipose tissue in obese men. J Clin Endocrinol Metab 91: 5107–5112. PubMed

Kovacikova M, Sengenes C, Kovacova Z, Siklova-Vitkova M, Klimcakova E, Polak J, et al. (2011) Dietary intervention-induced weight loss decreases macrophage content in adipose tissue of obese women. Int J Obes (Lond) 35: 91–98. 10.1038/ijo.2010.112 PubMed DOI

Curat CA, Miranville A, Sengenes C, Diehl M, Tonus C, Busse R, et al. (2004) From blood monocytes to adipose tissue-resident macrophages: induction of diapedesis by human mature adipocytes. Diabetes 53: 1285–1292. PubMed

Esposito K, Nappo F, Marfella R, Giugliano G, Giugliano F, Ciotola M, et al. (2002) Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 106: 2067–2072. PubMed

Dasu MR, Devaraj S, Zhao L, Hwang DH, Jialal I (2008) High glucose induces toll-like receptor expression in human monocytes: mechanism of activation. Diabetes 57: 3090–3098. 10.2337/db08-0564 PubMed DOI PMC

Jones BW, Heldwein KA, Means TK, Saukkonen JJ, Fenton MJ (2001) Differential roles of Toll-like receptors in the elicitation of proinflammatory responses by macrophages. Ann Rheum Dis 60 Suppl 3: iii6–12. PubMed PMC

Parker LC, Whyte MK, Vogel SN, Dower SK, Sabroe I (2004) Toll-like receptor (TLR)2 and TLR4 agonists regulate CCR expression in human monocytic cells. J Immunol 172: 4977–4986. PubMed

Kashiwagi M, Imanishi T, Ozaki Y, Satogami K, Masuno T, Wada T, et al. (2012) Differential expression of Toll-like receptor 4 and human monocyte subsets in acute myocardial infarction. Atherosclerosis 221: 249–253. 10.1016/j.atherosclerosis.2011.12.030 PubMed DOI

Wentworth JM, Naselli G, Brown WA, Doyle L, Phipson B, Smyth GK, et al. (2010) Pro-inflammatory CD11c+CD206+ adipose tissue macrophages are associated with insulin resistance in human obesity. Diabetes 59: 1648–1656. 10.2337/db09-0287 PubMed DOI PMC

Aron-Wisnewsky J, Tordjman J, Poitou C, Darakhshan F, Hugol D, Basdevant A, et al. (2009) Human adipose tissue macrophages: m1 and m2 cell surface markers in subcutaneous and omental depots and after weight loss. J Clin Endocrinol Metab 94: 4619–4623. 10.1210/jc.2009-0925 PubMed DOI

Kintscher U, Hartge M, Hess K, Foryst-Ludwig A, Clemenz M, Wabitsch M, et al. (2008) T-lymphocyte infiltration in visceral adipose tissue: a primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Arterioscler Thromb Vasc Biol 28: 1304–1310. 10.1161/ATVBAHA.108.165100 PubMed DOI

Nishimura S, Manabe I, Nagasaki M, Eto K, Yamashita H, Ohsugi M, et al. (2009) CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat Med 15: 914–920. 10.1038/nm.1964 PubMed DOI

Rocha VZ, Folco EJ, Sukhova G, Shimizu K, Gotsman I, Vernon AH, et al. (2008) Interferon-gamma, a Th1 cytokine, regulates fat inflammation: a role for adaptive immunity in obesity. Circ Res 103: 467–476. 10.1161/CIRCRESAHA.108.177105 PubMed DOI PMC

Dong C (2006) Diversification of T-helper-cell lineages: finding the family root of IL-17-producing cells. Nat Rev Immunol 6: 329–333. PubMed

Winer S, Chan Y, Paltser G, Truong D, Tsui H, Bahrami J, et al. (2009) Normalization of obesity-associated insulin resistance through immunotherapy. Nat Med 15: 921–929. 10.1038/nm.2001 PubMed DOI PMC

Fabbrini E, Cella M, McCartney SA, Fuchs A, Abumrad NA, Pietka TA, et al. (2013) Association between specific adipose tissue CD4+ T-cell populations and insulin resistance in obese individuals. Gastroenterology 145: 366–374 e361–363. 10.1053/j.gastro.2013.04.010 PubMed DOI PMC

Meugnier E, Faraj M, Rome S, Beauregard G, Michaut A, Pelloux V, et al. (2007) Acute hyperglycemia induces a global downregulation of gene expression in adipose tissue and skeletal muscle of healthy subjects. Diabetes 56: 992–999. PubMed

Bes-Houtmann S, Roche R, Hoareau L, Gonthier MP, Festy F, Caillens H, et al. (2007) Presence of functional TLR2 and TLR4 on human adipocytes. Histochem Cell Biol 127: 131–137. PubMed

Mudaliar H, Pollock C, Ma J, Wu H, Chadban S, Panchapakesan U (2014) The Role of TLR2 and 4-Mediated Inflammatory Pathways in Endothelial Cells Exposed to High Glucose. PLoS One 9: e108844 10.1371/journal.pone.0108844 PubMed DOI PMC

Amano SU, Cohen JL, Vangala P, Tencerova M, Nicoloro SM, Yawe JC, et al. (2014) Local proliferation of macrophages contributes to obesity-associated adipose tissue inflammation. Cell Metab 19: 162–171. 10.1016/j.cmet.2013.11.017 PubMed DOI PMC

Duffaut C, Zakaroff-Girard A, Bourlier V, Decaunes P, Maumus M, Chiotasso P, et al. (2009) Interplay Between Human Adipocytes and T Lymphocytes in Obesity: CCL20 as an Adipochemokine and T Lymphocytes as Lipogenic Modulators. Arteriosclerosis, Thrombosis, and Vascular Biology 29: 1608–1614. 10.1161/ATVBAHA.109.192583 PubMed DOI

Stentz FB, Kitabchi AE (2003) Activated T lymphocytes in Type 2 diabetes: implications from in vitro studies. Curr Drug Targets 4: 493–503. PubMed

Elgazar-Carmon V, Rudich A, Hadad N, Levy R (2008) Neutrophils transiently infiltrate intra-abdominal fat early in the course of high-fat feeding. J Lipid Res 49: 1894–1903. 10.1194/jlr.M800132-JLR200 PubMed DOI

Goossens GH, Blaak EE, Theunissen R, Duijvestijn AM, Clement K, Tervaert JW, et al. (2012) Expression of NLRP3 inflammasome and T cell population markers in adipose tissue are associated with insulin resistance and impaired glucose metabolism in humans. Mol Immunol 50: 142–149. 10.1016/j.molimm.2012.01.005 PubMed DOI

Snyder-Cappione JE, Nikolajczyk BS (2013) When diet and exercise are not enough, think immunomodulation. Mol Aspects Med 34: 30–38. 10.1016/j.mam.2012.10.003 PubMed DOI

Duffaut C, Galitzky J, Lafontan M, Bouloumié A (2009) Unexpected trafficking of immune cells within the adipose tissue during the onset of obesity. Biochemical and Biophysical Research Communications 384: 482–485. 10.1016/j.bbrc.2009.05.002 PubMed DOI

Sultan A, Strodthoff D, Robertson AK, Paulsson-Berne G, Fauconnier J, Parini P, et al. (2009) T cell-mediated inflammation in adipose tissue does not cause insulin resistance in hyperlipidemic mice. Circ Res 104: 961–968. 10.1161/CIRCRESAHA.108.190280 PubMed DOI

Murdolo G, Hammarstedt A, Sandqvist M, Schmelz M, Herder C, Smith U, et al. (2007) Monocyte chemoattractant protein-1 in subcutaneous abdominal adipose tissue: characterization of interstitial concentration and regulation of gene expression by insulin. J Clin Endocrinol Metab 92: 2688–2695. PubMed

Zhang WY, Schwartz EA, Permana PA, Reaven PD (2008) Pioglitazone inhibits the expression of inflammatory cytokines from both monocytes and lymphocytes in patients with impaired glucose tolerance. Arterioscler Thromb Vasc Biol 28: 2312–2318. 10.1161/ATVBAHA.108.175687 PubMed DOI

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