Macadamia oil supplementation attenuates inflammation and adipocyte hypertrophy in obese mice

Edson A Lima, Loreana S Silveira, Laureane N Masi, Amanda R Crisma, Mariana R Davanso, Gabriel I G Souza, Aline B Santamarina, Renata G Moreira, Amanda Roque Martins, Luis Gustavo O de Sousa, Sandro M Hirabara, Jose C Rosa Neto, Edson A Lima, Loreana S Silveira, Laureane N Masi, Amanda R Crisma, Mariana R Davanso, Gabriel I G Souza, Aline B Santamarina, Renata G Moreira, Amanda Roque Martins, Luis Gustavo O de Sousa, Sandro M Hirabara, Jose C Rosa Neto

Abstract

Excess of saturated fatty acids in the diet has been associated with obesity, leading to systemic disruption of insulin signaling, glucose intolerance, and inflammation. Macadamia oil administration has been shown to improve lipid profile in humans. We evaluated the effect of macadamia oil supplementation on insulin sensitivity, inflammation, lipid profile, and adipocyte size in high-fat diet (HF) induced obesity in mice. C57BL/6 male mice (8 weeks) were divided into four groups: (a) control diet (CD), (b) HF, (c) CD supplemented with macadamia oil by gavage at 2 g/Kg of body weight, three times per week, for 12 weeks (CD + MO), and (d) HF diet supplemented with macadamia oil (HF + MO). CD and HF mice were supplemented with water. HF mice showed hypercholesterolemia and decreased insulin sensitivity as also previously shown. HF induced inflammation in adipose tissue and peritoneal macrophages, as well as adipocyte hypertrophy. Macadamia oil supplementation attenuated hypertrophy of adipocytes and inflammation in the adipose tissue and macrophages.

Figures

Figure 1
Figure 1
Effect of MO supplementation on adipose tissue histology. (a) Histological sections stained with H&E. (b) Area of adipocytes. CD = group of animals maintained on control diet; HF = group of animals fed high-fat diet; CD + MO = group of animals fed control diet supplemented with macadamia oil; HF + MO = group of animals fed high-fat diet supplemented with macadamia oil. The data are given as the means ± S.D. *P < 0.05 (n = 6).
Figure 2
Figure 2
Insulin sensitivity and triacylglycerol content in skeletal muscle after 12 weeks. (a) HOMA-IR: homeostatic model assessment of insulin resistance; (b) GLUT-4 gene expression; (c) triacylglycerol content in gastrocnemius muscle. The data are given as the means ± S.D. In all experiments the animals were previously fasted for 6 hours. CD = group of animals maintained on control diet; HF = group of animals fed high-fat diet; CD + MO = group of animals fed control diet supplemented with macadamia oil; HF + MO = group of animals fed high-fat diet supplemented with macadamia oil. A.U. = arbitrary unit. *P < 0.05; **P < 0.01 (n = 6).
Figure 3
Figure 3
Inflammatory parameters in adipose tissue homogenate and adipose tissue explant incubation medium. IL10 content in adipose tissue homogenate (a) and IL1-β in the adipose tissue explant incubation medium, after 24 hours measured by ELISA (b). The animals received water or macadamia oil orally, 2 g/kg b.w., with or without association with a high-fat diet. CD = group of animals maintained on control diet; HF = group of animals fed high-fat diet; CD + MO = group of animals fed control diet supplemented with macadamia oil; HF + MO = group of animals fed high-fat diet supplemented with macadamia oil. The data are given as the means ± S.D. *P < 0.05 (n = 5-6).
Figure 4
Figure 4
Nitric oxide and cytokine production by peritoneal macrophages. Peritoneal macrophages were collected and cultured for 24 h in the absence (white bars) or presence (black bars) of 2.5 μg/mL LPS. Nitric oxide (a), IL1-β (b), TNF-α (c), IL-6 (d), and IL-10 (e) were measured. CD = control diet; HF = high-fat diet; CD + MO = control diet + macadamia oil; HF + MO = high-fat diet + macadamia oil. The data are given as the means ± S.D. *P < 0.05; ***P < 0.001 (n = 5-6).

References

    1. Arapostathi C, Tzanetakou IP, Kokkinos AD, et al. A diet rich in monounsaturated fatty acids improves the lipid profile of mice previously on a diet rich in saturated fatty acids. Angiology. 2011;62(8):636–640.
    1. Hiraoka-Yamamoto J, Ikeda K, Negishi H, et al. Serum lipid effects of a monounsaturated (palmitoleic) fatty acid-rich diet based on macadamia nuts in healthy, young japanese women. Clinical and Experimental Pharmacology and Physiology. 2004;31(supplement 2):S37–S38.
    1. Mensink RP, Zock PL, Kester ADM, Katan MB. Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. The American Journal of Clinical Nutrition. 2003;77(5):1146–1155.
    1. Nicklas TA, Hampl JS, Taylor CA, Thompson VJ, Heird WC. Monounsaturated fatty acid intake by children and adults: temporal trends and demographic differences. Nutrition Reviews. 2004;62(4):132–141.
    1. Gillingham LG, Harris-Janz S, Jones PJH. Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids. 2011;46(3):209–228.
    1. Haghighatdoost F, Hosseinzadeh-Attar MJ, Kabiri A, Eshraghian M, Esmaillzadeh A. Effect of substituting saturated with monounsaturated fatty acids on serum visfatin levels and insulin resistance in overweight women: a randomized cross-over clinical trial. International Journal of Food Sciences and Nutrition. 2012;63(7):772–781.
    1. Maguire LS, O'Sullivan SM, Galvin K, O'Connor TP, O'Brien NM. Fatty acid profile, tocopherol, squalene and phytosterol content of walnuts, almonds, peanuts, hazelnuts and the macadamia nut. International Journal of Food Sciences and Nutrition. 2004;55(3):171–178.
    1. Griel AE, Cao Y, Bagshaw DD, Cifelli AM, Holub B, Kris-Etherton PM. A Macadamia nut-rich diet reduces total and LDL-cholesterol in mildly hypercholesterolemic men and women. Journal of Nutrition. 2008;138(4):761–767.
    1. Curb JD, Wergowske G, Dobbs JC, Abbott RD, Huang B. Serum lipid effects of a high-monounsaturated fat diet based on macadamia nuts. Archives of Internal Medicine. 2000;160(8):1154–1158.
    1. Matthan NR, Dillard A, Lecker JL, Ip B, Lichtenstein AH. Effects of dietary palmitoleic acid on plasma lipoprotein profile and aortic cholesterol accumulation are similar to those of other unsaturated fatty acids in the f1b golden syrian hamster. The Journal of Nutrition. 2009;139(2):215–221.
    1. Cao H, Gerhold K, Mayers JR, Wiest MM, Watkins SM, Hotamisligil GS. Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism. Cell. 2008;134(6):933–944.
    1. Jensen MD. Role of body fat distribution and the metabolic complications of obesity. Journal of Clinical Endocrinology and Metabolism. 2008;93(11):S57–S63.
    1. Kien CL. Dietary interventions for metabolic syndrome: role of modifying dietary fats. Current Diabetes Reports. 2009;9(1):43–50.
    1. Samuel VT, Petersen KF, Shulman GI. Lipid-induced insulin resistance: unravelling the mechanism. The Lancet. 2010;375(9733):2267–2277.
    1. Han D-H, Hansen PA, Host HH, Holloszy JO. Insulin resistance of muscle glucose transport in rats fed a high-fat diet: a reevaluation. Diabetes. 1997;46(11):1761–1767.
    1. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annual Review of Immunology. 2011;29:415–445.
    1. Lim HH, Lee SO, Kim SY, Yang SJ, Lim Y. Anti-inflammatory and antiobesity effects of mulberry leaf and fruit extract on high fat diet-induced obesity. Experimental Biology and Medicine. 2013;238(10):1160–1169.
    1. Reyna SM, Ghosh S, Tantiwong P, et al. Elevated toll-like receptor 4 expression and signaling in muscle from insulin-resistant subjects. Diabetes. 2008;57(10):2595–2602.
    1. Jin J, Zhang X, Lu Z, et al. Acid sphingomyelinase plays a key role in palmitic acid-amplified inflammatory signaling triggered by lipopolysaccharide at low concentrations in macrophages. American Journal of Physiology: Endocrinology and Metabolism. 2013;305(7):E853–E867.
    1. Waki H, Tontonoz P. Endocrine functions of adipose tissue. Annual Review of Pathology. 2007;2:31–56.
    1. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nature Reviews Immunology. 2011;11(2):85–97.
    1. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW., Jr. Obesity is associated with macrophage accumulation in adipose tissue. Journal of Clinical Investigation. 2003;112(12):1796–1808.
    1. Patsouris D, Li P-P, Thapar D, Chapman J, Olefsky JM, Neels JG. Ablation of CD11c-positive cells normalizes insulin sensitivity in obese insulin resistant animals. Cell Metabolism. 2008;8(4):301–309.
    1. Masi LN, Martins AR, Neto JCR, et al. Sunflower oil supplementation has proinflammatory effects and does not reverse insulin resistance in obesity induced by high-fat diet in C57BL/6 mice. Journal of Biomedicine and Biotechnology. 2012;2012:9 pages.945131
    1. Vinolo MAR, Rodrigues HG, Festuccia WT, et al. Tributyrin attenuates obesity-associated inflammation and insulin resistance in high-fat-fed mice. The American Journal of Physiology—Endocrinology and Metabolism. 2012;303(2):E272–E282.
    1. Papadimitriou JM, Van Bruggen I. The effects of malnutrition on murine peritoneal macrophages. Experimental and Molecular Pathology. 1988;49(2):161–170.
    1. Sen NP, Donaldson B. Improved colorimetric method for determining nitrate and nitrate in foods. Journal of the Association of Official Analytical Chemists. 1978;61(6):1389–1394.
    1. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry. 1987;162(1):156–159.
    1. Higuchi R, Dollinger G, Walsh PS, Griffith R. Simultaneous amplification and detection of specific DNA sequences. Bio/Technology. 1992;10(4):413–417.
    1. Liu W, Saint DA. Validation of a quantitative method for real time PCR kinetics. Biochemical and Biophysical Research Communications. 2002;294(2):347–353.
    1. Matsuda M, Shimomura I. Increased oxidative stress in obesity: Implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obesity Research and Clinical Practice. 2013;7(5):e330–e341.
    1. Fernandes-Santos C, Carneiro RE, de Souza Mendonca L, Aguila MB, Mandarim-de-Lacerda CA. Pan-PPAR agonist beneficial effects in overweight mice fed a high-fat high-sucrose diet. Nutrition. 2009;25(7-8):818–827.
    1. Fraulob JC, Ogg-Diamantino R, Fernandes-Santos C, Aguila MB, Mandarim-de-Lacerda CA. A mouse model of metabolic syndrome: insulin resistance, fatty liver and Non-Alcoholic Fatty Pancreas Disease (NAFPD) in C57BL/6 mice fed a high fat diet. Journal of Clinical Biochemistry and Nutrition. 2010;46(3):212–223.
    1. Pimentel GD, Dornellas APS, Rosa JC, et al. High-fat diets rich in soy or fish oil distinctly alter hypothalamic insulin signaling in rats. Journal of Nutritional Biochemistry. 2012;23(7):822–828.
    1. Chen L, Magliano DJ, Zimmet PZ. The worldwide epidemiology of type 2 diabetes mellitus—present and future perspectives. Nature Reviews Endocrinology. 2012;8(4):228–236.
    1. Rebello CJ, Greenway FL, Finley JW. A review of the nutritional value of legumes and their effects on obesity and its related co-morbidities. Obesity Reviews. 2014;15(5):392–407.
    1. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. Journal of Clinical Investigation. 2005;115(5):1111–1119.
    1. Gray SL, Vidal-Puig AJ. Adipose tissue expandability in the maintenance of metabolic homeostasis. Nutrition Reviews. 2007;65(supplement 1):S7–S12.
    1. Higa TS, Spinola AV, Fonseca-Alaniz MH, Anna Evangelista FS. Comparison between cafeteria and high-fat diets in the induction of metabolic dysfunction in mice. International Journal of Physiology, Pathophysiology and Pharmacology. 2014;6(1):47–54.
    1. Kwon H, Pessin JE. Adipokines mediate inflammation and insulin resistance. Frontiers in Endocrinology. 2013;4, article 71
    1. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation- induced immunosuppression. Nature. 1998;394(6696):897–901.
    1. Marzullo P, Minocci A, Giarda P, et al. Lymphocytes and immunoglobulin patterns across the threshold of severe obesity. Endocrine. 2014;45(3):392–400.
    1. Santos-Alvarez J, Goberna R, Sánchez-Margalet V. Human leptin stimulates proliferation and activation of human circulating monocytes. Cellular Immunology. 1999;194(1):6–11.
    1. Acedo SC, Gambero S, Cunha FGP, Lorand-Metze I, Gambero A. Participation of leptin in the determination of the macrophage phenotype: An additional role in adipocyte and macrophage crosstalk. In Vitro Cellular and Developmental Biology - Animal. 2013;49(6):473–478.
    1. Okuno A, Tamemoto H, Tobe K, et al. Troglitazone increases the number of small adipocytes without the change of white adipose tissue mass in obese Zucker rats. Journal of Clinical Investigation. 1998;101(6):1354–1361.
    1. Rigamonti E, Chinetti-Gbaguidi G, Staels B. Regulation of macrophage functions by PPAR- α, PPAR- γ, and LXRs in mice and men. Arteriosclerosis, Thrombosis, and Vascular Biology. 2008;28(6):1050–1059.
    1. Fujisaka S, Usui I, Bukhari A, et al. Regulatory mechanisms for adipose tissue M1 and M2 macrophages in diet-induced obese mice. Diabetes. 2009;58(11):2574–2582.
    1. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends in Immunology. 2004;25(12):677–686.
    1. Hong E-G, Hwi JK, Cho Y-R, et al. Interleukin-10 prevents diet-induced insulin resistance by attenuating macrophage and cytokine response in skeletal muscle. Diabetes. 2009;58(11):2525–2535.
    1. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. Journal of Clinical Investigation. 2007;117(1):175–184.
    1. Tilg H, Moschen AR. Inflammatory mechanisms in the regulation of insulin resistance. Molecular Medicine. 2008;14(3-4):222–231.
    1. McArdle MA, Finucane OM, Connaughton RM, McMorrow AM, Roche HM. Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies. Frontiers in Endocrinology. 2013;4, article 52Article 52
    1. Jager J, Grémeaux T, Cormont M, Le Marchand-Brustel Y, Tanti J-F. Interleukin-1β-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology. 2007;148(1):241–251.
    1. Spranger J, Kroke A, Möhlig M, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based european prospective investigation into cancer and nutrition (epic)-potsdam study. Diabetes. 2003;52(3):812–817.
    1. Zhong Y, Chiou Y-S, Pan M-H, Shahidi F. Anti-inflammatory activity of lipophilic epigallocatechin gallate (EGCG) derivatives in LPS-stimulated murine macrophages. Food Chemistry. 2012;134(2):742–748.
    1. Han S, Lee JH, Kim C, et al. Capillarisin inhibits iNOS, COX-2 expression, and proinflammatory cytokines in LPS-induced RAW 264.7 macrophages via the suppression of ERK, JNK, and NF-κB activation. Immunopharmacology and Immunotoxicology. 2013;35(1):34–42.

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