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The Effect of Very-Low-Calorie Diet on Mrna Expression of Inflammation

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The Effect of Very-Low-Calorie Diet on Mrna Expression of Inflammation JCEM ONLINE Hot Topics in Translational Endocrinology—Endocrine Research The Effect of Very-Low-Calorie Diet on mRNA Expression of Inflammation-Related Genes in Subcutaneous Adipose Tissue and Peripheral Monocytes of Obese Patients with Type 2 Diabetes Mellitus Downloaded from https://academic.oup.com/jcem/article/96/4/E606/2720876 by guest on 26 September 2021 M. Mraz, Z. Lacinova, J. Drapalova, D. Haluzikova, A. Horinek, M. Matoulek, P. Trachta, P. Kavalkova, S. Svacina, and M. Haluzik Third Department of Medicine (M.Mr., Z.L., J.D., D.H., A.H., M.Ma., P.T., P.K., S.S., M.H.) and Department of Sports Medicine (D.H.), General University Hospital and First Medical Faculty, Charles University, 128 08 Prague 2, Czech Republic Context: Low-grade inflammation links obesity, type 2 diabetes mellitus (T2DM), and cardiovas- cular diseases. Objective: To explore the expression profile of genes involved in inflammatory pathways in adipose tissue and peripheral monocytes (PM) of obese patients with and without T2DM at baseline and after dietary intervention. Design: Two-week intervention study with very-low-calorie diet (VLCD). Setting: University hospital. Patients: Twelve obese females with T2DM, 8 obese nondiabetic females (OB) and 15 healthy age-matched females. Intervention: Two weeks of VLCD (2500 kJ/d). Main Outcome Measures: Metabolic parameters, circulating cytokines, hormones, and mRNA expression of 39 genes in sc adipose tissue (SCAT) and PM. Results: Both T2DM and OB group had significantly increased serum concentrations of circulating proinflammatory factors (C-reactive protein, TNF␣, IL-6, IL-8), mRNA expression of macrophage antigen CD68 and proinflammatory chemokines (CCL-2, -3, -7, -8, -17, -22) in SCAT and comple- mentary chemokine receptors (CCR-1, -2, -3, -5) and other proinflammatory receptors (toll-like receptor 2 and 4, TNF receptor superfamily 1A and 1B, IL-6R) in PM, with OB group showing less pronounced chemoattracting and proinflammatory profile compared to T2DM group. In T2DM patients VLCD decreased body weight, improved metabolic profile, and decreased mRNA expres- sion of up-regulated CCRs in PM and chemokines [CCL 8, chemokine (C-X-C motif) ligand 10] in SCAT. VLCD markedly increased mRNA expression of T-lymphocyte attracting chemokine CCL-17 in SCAT. Conclusion: Obese patients with and without T2DM have increased mRNA expression of chemot- actic and proinflammatory factors in SCAT and expression of corresponding receptors in PM. Two weeks of VLCD significantly improved this profile in T2DM patients. (J Clin Endocrinol Metab 96: E606–E613, 2011) ISSN Print 0021-972X ISSN Online 1945-7197 Abbreviations: ATM, Adipose tissue macrophage; BMI, body mass index; CCL, chemokine Printed in U.S.A. (C-C motif) ligand; CCR, chemokine (C-C motif) receptor; CRP, C-reactive protein; CXCL, Copyright © 2011 by The Endocrine Society chemokine (C-X-C motif) ligand; OB, obese nondiabetic; PM, peripheral monocyte; PPAR, doi: 10.1210/jc.2010-1858 Received August 9, 2010. Accepted January 3, 2011. peroxisome proliferator-activated receptor; SCAT, sc adipose tissue; T2DM, type 2 diabetes First Published Online February 2, 2011 mellitus; TH, T helper lymphocyte; TLR, toll-like receptor; TNFRSF, TNF receptor superfamily; VLCD, very-low-calorie diet. E606 jcem.endojournals.org J Clin Endocrinol Metab, April 2011, 96(4):E606–E613 J Clin Endocrinol Metab, April 2011, 96(4):E606–E613 jcem.endojournals.org E607 ubclinical inflammation is one of the key mecha- Materials and Methods S nisms linking obesity, insulin resistance, and other components of the metabolic syndrome (1–3). The piv- Study subjects Twelve obese women with T2DM (T2DM group), eight otal role in the development of this chronic low-grade obese nondiabetic females (OB group), and fifteen healthy nor- proinflammatory state is now attributed to adipose tis- mal-weight age-matched women (C group) were included in the sue and its endocrine factors (1, 4–6). Obesity is char- study. Eight of 12 T2DM patients had been treated either with acterized by elevated circulating levels of acute phase oral antidiabetic drugs (metformin, sulfonylurea derivates, or proteins, proinflammatory cytokines, and chemokines thiazolidindiones), insulin, or its combination. The rest of T2DM patients were treated by diet only. All diabetic patients such as TNF␣, IL-6, IL-8, and chemokine C-C motif were on antihypertensive treatment, four patients were treated ligand 2 (CCL-2), leptin, resistin, and many others (1, by statins, one by fibrate. None of the patients had malignant 5). These factors induce insulin resistance by interfer- tumor, thyroid disease, or acute infectious disease. In the OB Downloaded from https://academic.oup.com/jcem/article/96/4/E606/2720876 by guest on 26 September 2021 ence with postreceptor insulin signaling cascade (7) and group one patient was treated with antihypertensives and none accelerate the development of endothelial dysfunction/ of them was on hypolipidemic medication. Control subjects had atherosclerosis (5). no history of obesity and/or diabetes mellitus, arterial hyperten- sion, or lipid metabolism disturbances and received no medica- A number of studies have shown that both adipocytes tion. Blood tests confirmed normal blood count, biochemical (8) as well as immunocompetent cells residing in adipose and hormonal parameters. tissue contribute to this inflammatory process (2, 9). Ex- All T2DM patients underwent a 2-week VLCD with energy cessive accumulation of adipose tissue is associated with intake of 2500 kJ/d (600 kcal/d). During this program, all pa- elevated number of adipose tissue macrophages (ATMs) tients were hospitalized in the Third Department of Medicine, General University Hospital, Prague. (2, 10, 11) and increased expression of proinflammatory The body weight of all study participants remained stable for factors in fat (2, 9). Accumulation of ATMs in fat is linked at least 3 months before the beginning of the study. Written to insulin resistance and endothelial dysfunction in obese informed consent was signed by all participants before being subjects (12). enrolled in the study. The study was approved by Human Ethical It has been demonstrated that most of the ATMs in Review Committee, First Faculty of Medicine and General Uni- versity Hospital, Prague, Czech Republic and was performed in fat are derived from circulating mononuclear cells out- accordance with the guidelines proposed in Declaration of side the adipose tissue (9–11). Peripheral blood mono- Helsinki. cytes are recruited into adipose tissue by various che- moattractants produced by hypertrophic adipocytes as Anthropometric examination, blood, and adipose well as resident stromal macrophages and T-lympho- tissue sampling cytes. Their products subsequently act on adipocytes in All patients with T2DM were examined twice: at basal state a paracrine manner promoting the production of pro- before the beginning of any intervention and after 2 wk of VLCD, inflammatory factors. This cross-talk between ATMs while OB and normal-weight healthy women were examined and adipocytes generates a vicious circle of increased only once. All subjects were measured and weighed, and their adipose tissue inflammation that contributes to the low- body mass index (BMI) was calculated. Blood samples for cyto- kines, C-reactive protein (CRP), insulin, and biochemical pa- grade systemic inflammation (13, 14). rameters measurement were withdrawn between 0700 h and At present, very little is known about interactions be- 0800 h after 12 h of overnight fasting. Blood samples were sep- tween circulating monocytes and adipose tissue, although arated by centrifugation for 10 min at 1000 ϫ g within 30 min this interplay may be critically important in the develop- from blood collection. Serum was subsequently stored in ali- Ϫ ment of systemic subclinical inflammation, type 2 diabetes quots at 80 C until further analysis. Blood samples for monocyte isolation were collected in mellitus (T2DM), and its atherosclerotic complications. Na-EDTA anticoagulant from all subjects and processed We hypothesized that this interplay is driven by adipose within 1–2 h. tissue production of factors associated with the recruit- Samples of SCAT for mRNA expression analysis were ob- ment of peripheral monocytes (PM) into adipose tissue, tained from the abdominal region as described previously else- such as chemokines and chemokine receptors. Further- where (6). more, we tested the hypothesis that metabolic improve- ments after short-term very-low-calorie diet (VLCD) Hormonal and biochemical assays could be mediated by improved inflammatory profile and Serum adiponectin, CRP, leptin, resistin, and insulin concen- decreased expression of chemotactic factors in both PM trations were measured by commercial ELISA and RIA kits as and sc adipose tissue (SCAT). To this end, we evaluated described previously (8). Serum concentrations of IL-6, IL-8, CCL-2, and TNF␣ were measured using Human serum adipo- the expression of a selected panel of inflammation-related kine panel B LINCOplex Kit on Luminex200 instrument (Linco factors in SCAT and PM of patients with obesity and Research, St. Charles, MO). Sensitivity was 1.6 pg/ml for IL-6, T2DM. 0.2 pg/ml for IL-8, 0.14 pg/ml for CCL-2, and 0.22 pg/ml TNF␣. E608 Mraz et al. Effect of VLCD on Gene Expression in T2DM J Clin Endocrinol Metab, April 2011, 96(4):E606–E613 The intra- and interassay variabilities were less than 10% and monal results are expressed as means Ϯ SEM. Differences of gene 15%, respectively.
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