Oleic acid and peanut oil high in oleic acid reverse the inhibitory effect of insulin production of the inflammatory cytokine TNF-alpha both in vitro and in vivo systems
Evros K Vassiliou, Andres Gonzalez, Carlos Garcia, James H Tadros, Goutam Chakraborty, Jeffrey H Toney, Evros K Vassiliou, Andres Gonzalez, Carlos Garcia, James H Tadros, Goutam Chakraborty, Jeffrey H Toney
Abstract
Background: Chronic inflammation is a key player in pathogenesis. The inflammatory cytokine, tumor necrosis factor-alpha is a well known inflammatory protein, and has been a therapeutic target for the treatment of diseases such as Rheumatoid Arthritis and Crohn's Disease. Obesity is a well known risk factor for developing non-insulin dependent diabetes melitus. Adipose tissue has been shown to produce tumor necrosis factor-alpha, which has the ability to reduce insulin secretion and induce insulin resistance. Based on these observations, we sought to investigate the impact of unsaturated fatty acids such as oleic acid in the presence of TNF-alpha in terms of insulin production, the molecular mechanisms involved and the in vivo effect of a diet high in oleic acid on a mouse model of type II diabetes, KKAy.
Methods: The rat pancreatic beta cell line INS-1 was used as a cell biological model since it exhibits glucose dependent insulin secretion. Insulin production assessment was carried out using enzyme linked immunosorbent assay and cAMP quantification with competitive ELISA. Viability of TNF-alpha and oleic acid treated cells was evaluated using flow cytometry. PPAR-gamma translocation was assessed using a PPRE based ELISA system. In vivo studies were carried out on adult male KKAy mice and glucose levels were measured with a glucometer.
Results: Oleic acid and peanut oil high in oleic acid were able to enhance insulin production in INS-1. TNF-alpha inhibited insulin production but pre-treatment with oleic acid reversed this inhibitory effect. The viability status of INS-1 cells treated with TNF-alpha and oleic acid was not affected. Translocation of the peroxisome proliferator- activated receptor transcription factor to the nucleus was elevated in oleic acid treated cells. Finally, type II diabetic mice that were administered a high oleic acid diet derived from peanut oil, had decreased glucose levels compared to animals administered a high fat diet with no oleic acid.
Conclusion: Oleic acid was found to be effective in reversing the inhibitory effect in insulin production of the inflammatory cytokine TNF-alpha. This finding is consistent with the reported therapeutic characteristics of other monounsaturated and polyunsaturated fatty acids. Furthermore, a diet high in oleic acid, which can be easily achieved through consumption of peanuts and olive oil, can have a beneficial effect in type II diabetes and ultimately reverse the negative effects of inflammatory cytokines observed in obesity and non insulin dependent diabetes mellitus.
Figures
References
- Cavaillon JM. Cytokines in inflammation. C R Seances Soc Biol Fil. 1995;189:531–544.
- Vassiliou E, Jing H, Ganea D. Prostaglandin E2 inhibits TNF production in murine bone marrow-derived dendritic cells. Cell Immunol. 2003;223:120–132. doi: 10.1016/S0008-8749(03)00158-8.
- Yudkin JS. Inflammation, obesity, and the metabolic syndrome. Horm Metab Res. 2007;39:707–709. doi: 10.1055/s-2007-985898.
- Kim HE, Choi SE, Lee SJ, Lee JH, Lee YJ, Kang SS, Chun J, Kang Y. Tumour necrosis factor-alpha-induced glucose-stimulated insulin secretion inhibition in INS-1 cells is ascribed to a reduction of the glucose-stimulated Ca2+ influx. J Endocrinol. 2008;198:549–560. doi: 10.1677/JOE-08-0131.
- Zhang S, Kim KH. TNF-alpha inhibits glucose-induced insulin secretion in a pancreatic beta-cell line (INS-1) FEBS Lett. 1995;377:237–239. doi: 10.1016/0014-5793(95)01272-9.
- del Aguila LF, Claffey KP, Kirwan JP. TNF-alpha impairs insulin signaling and insulin stimulation of glucose uptake in C2C12 muscle cells. Am J Physiol. 1999;276:E849–E855.
- Ridker PM, Danielson E, Fonseca FA, Genest J, Gotto AM, Jr, Kastelein JJ, Koenig W, Libby P, Lorenzatti HA, MacFadyen JG, Nordestgaard BG, Shepherd J, Willerson JT, Glynn RJ. Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med. 2008;359:2195–2207. doi: 10.1056/NEJMoa0807646.
- Jimenez-Gomez Y, Lopez-Miranda J, Blanco-Colio LM, Marin C, Perez-Martinez P, Ruano J, Paniagua JA, Rodriguez F, Egido J, Perez-Jimerez F. Olive oil and walnut breakfasts reduce the postprandial inflammatory response in mononuclear cells compared with a butter breakfast in healthy men. Atherosclerosis. 2008;204:e70–76. doi: 10.1016/j.atherosclerosis.2008.09.011.
- Micallef MA, Garg ML. Anti-inflammatory and cardioprotective effects of n-3 polyunsaturated fatty acids and plant sterols in hyperlipidemic individuals. Atherosclerosis. 2009;204:476–482. doi: 10.1016/j.atherosclerosis.2008.09.020.
- Ouellet V, Weisnagel SJ, Marois J, Bergeron J, Julien P, Gougeon R, Tchernof A, Holub BJ, Jacques H. Dietary cod protein reduces plasma C-reactive protein in insulin-resistant men and women. J Nutr. 2008;138:2386–2391. doi: 10.3945/jn.108.092346.
- Lichtenstein AH, Ausman LM, Carrasco W, Jenner JL, Ordovas JM, Schaefer EJ. Hydrogenation impairs the hypolipidemic effect of corn oil in humans. Hydrogenation, trans fatty acids, and plasma lipids. Arterioscler Thromb. 1993;13:154–161.
- Vassiliou EK, Kesler OM, Tadros JH, Ganea D. Bone marrow-derived dendritic cells generated in the presence of resolvin E1 induce apoptosis of activated CD4+ T cells. J Immunol. 2008;181:4534–4544.
- Arita M, Yoshida M, Hong S, Tjonahen E, Glickman JN, Petasis NA, Blumberg RS, Serhan CN. Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc Natl Acad Sci USA. 2005;102:7671–7676. doi: 10.1073/pnas.0409271102.
- Li H, Ruan XZ, Powis SH, Fernando R, Mon WY, Wheeler DC, Moorhead JF, Varghese Z. EPA and DHA reduce LPS-induced inflammation responses in HK-2 cells: evidence for a PPAR-gamma-dependent mechanism. Kidney Int. 2005;67:867–874. doi: 10.1111/j.1523-1755.2005.00151.x.
- Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr. 2004;92:347–355. doi: 10.1079/BJN20041213.
- Tsimikas S, Philis-Tsimikas A, Alexopoulos S, Sigari F, Lee C, Reaven PD. LDL isolated from Greek subjects on a typical diet or from American subjects on an oleate-supplemented diet induces less monocyte chemotaxis and adhesion when exposed to oxidative stress. Arterioscler Thromb Vasc Biol. 1999;19:122–130.
- Jossa F, Mancini M. The Mediterranean diet in the prevention of arteriosclerosis. Recenti Prog Med. 1996;87:175–181.
- Panagiotakos DB, Dimakopoulou K, Katsouyanni K, Bellander T, Grau M, Koenig W, Lanki T, Pistelli R, Schneider A, Peters A. Mediterranean diet and inflammatory response in myocardial infarction survivors. Int J Epidemiol. 2009;38:856–866. doi: 10.1093/ije/dyp142.
- Winzell MS, Ahren B. The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes. 2004;53:S215–S219. doi: 10.2337/diabetes.53.suppl_3.S215.
- Chakraborty G, Zhao YM, Sheng SL, Zhao W, Li LH, Ruskin MS, Toney JH. Peanut oil lowers blood glucose in models of type II but not type I diabetic mice. ADA. 2005;54:A645.
- Catalan V, Gomez-Ambrosi J, Ramirez B, Rotellar F, Pastor C, Silva C, Rotellar F, Gil MJ, Cienfuegos JA, Salvador J, Vendrell J, Fruhbeck G. Proinflammatory cytokines in obesity: impact of type 2 diabetes mellitus and gastric bypass. Obes Surg. 2007;17:1464–1474. doi: 10.1007/s11695-008-9424-z.
- Pitsavos C, Chrysohoou C, Panagiotakos DB, Lentzas Y, Stefanadis C. Abdominal obesity and inflammation predicts hypertension among prehypertensive men and women: the ATTICA Study. Heart Vessels. 2008;23:96–103. doi: 10.1007/s00380-007-1018-5.
- Kalofoutis C, Piperi C, Zisaki A, Singh J, Harris F, Phoenix D, Alaveras A, Kalofoutis A. Differences in expression of cardiovascular risk factors among type 2 diabetes mellitus patients of different age. Ann N Y Acad Sci. 2006;1084:166–177. doi: 10.1196/annals.1372.001.
- Kebede M, Alquier T, Latour MG, Semache M, Tremblay C, Poitout V. The fatty acid receptor GPR40 plays a role in insulin secretion in vivo after high-fat feeding. Diabetes. 2008;57:2432–2437. doi: 10.2337/db08-0553.
- Nagasumi K, Esaki R, Iwachidow K, Yasuhara Y, Ogi K, Tanaka H, Nakata M, Yano T, Shimakawa K, Taketomi S, Takeuchi K, Odaka H, Kaisho Y. Overexpression of GPR40 in Pancreatic {beta}-Cells Augments Glucose Stimulated Insulin Secretion and Improves Glucose Tolerance in Normal and Diabetic Mice. Diabetes. 2009;58:1067–1076. doi: 10.2337/db08-1233.
- Calabro P, Samudio I, Safe SH, Willerson JT, Yeh ET. Inhibition of tumor-necrosis-factor-alpha induced endothelial cell activation by a new class of PPAR-gamma agonists. An in vitro study showing receptor-independent effects. J Vasc Res. 2005;42:509–516. doi: 10.1159/000088260.
- Sood V, Colleran K, Burge MR. Thiazolidinediones: a comparative review of approved uses. Diabetes Technol Ther. 2000;2:429–440. doi: 10.1089/15209150050194297.
- Navarro MA, Acin S, Carnicer R, Guzman-Garcia MA, Arbones-Mainar JM, Surra JC, Cebrian JA, Arnal C, Isabel B, Lopez-Bote CJ, Osada J. Response of ApoA-IV in pigs to long-term increased dietary oil intake and to the degree of unsaturation of the fatty acids. Br J Nutr. 2004;92:763–769. doi: 10.1079/BJN20041266.
- Plomgaard P, Nielsen AR, Fischer CP, Mortensen OH, Broholm C, Penkowa M, Krogh-Madsen R, Erikstrup C, Petersen AM, Lindegaard B, Taudorf S, Pedersen BK. Associations between insulin resistance and TNF-alpha in plasma, skeletal muscle and adipose tissue in humans with and without type 2 diabetes. Diabetologia. 2007;50:2562–2571. doi: 10.1007/s00125-007-0834-6.
- Vock C, Gleissner M, Klapper M, Doring F. Oleate regulates genes controlled by signaling pathways of mitogen-activated protein kinase, insulin, and hypoxia. Nutr Res. 2008;28:681–689. doi: 10.1016/j.nutres.2008.06.010.
- Koshkin V, Dai FF, Robson-Doucette CA, Chan CB, Wheeler MB. Limited mitochondrial permeabilization is an early manifestation of palmitate-induced lipotoxicity in pancreatic beta-cells. J Biol Chem. 2008;283:7936–7948. doi: 10.1074/jbc.M705652200.
- Guo W, Wong S, Xie W, Lei T, Luo Z. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab. 2007;293:E576–E586. doi: 10.1152/ajpendo.00523.2006.
- Fu L, Isobe K, Zeng Q, Suzukawa K, Takekoshi K, Kawakami Y. beta-adrenoceptor agonists downregulate adiponectin, but upregulate adiponectin receptor 2 and tumor necrosis factor-alpha expression in adipocytes. Eur J Pharmacol. 2007;569:155–162. doi: 10.1016/j.ejphar.2007.05.005.
- Jiang R, Manson JE, Stampfer MJ, Liu S, Willett WC, Hu FB. Nut and peanut butter consumption and risk of type 2 diabetes in women. JAMA. 2002;288:2554–2560. doi: 10.1001/jama.288.20.2554.
- Sanders TH, McMichael RW, Jr, Hendrix KW. Occurrence of resveratrol in edible peanuts. J Agric Food Chem. 2000;48:1243–1246. doi: 10.1021/jf990737b.
- Alam M, Basha SM, Boyd LC. Characterization of methanol-soluble and methanol-insoluble proteins from developing peanut seed. J Agric Food Chem. 2000;48:5517–5521. doi: 10.1021/jf991337r.
- Sathe SK, Hamaker BR, Sze-Tao KW, Venkatachalam M. Isolation, purification, and biochemical characterization of a novel water soluble protein from Inca peanut (Plukenetia volubilis L.) J Agric Food Chem. 2002;50:4906–4908. doi: 10.1021/jf020126a.
- Bland JM, Lax AR. Isolation and characterization of a peanut maturity-associated protein. J Agric Food Chem. 2000;48:3275–3279. doi: 10.1021/jf000307h.
- Bersamin A, Luick BR, King IB, Stern JS, Zidenberg-Cherr S. Westernizing diets influence fat intake, red blood cell fatty acid composition, and health in remote Alaskan Native communities in the center for Alaska Native health study. J Am Diet Assoc. 2008;108:266–273. doi: 10.1016/j.jada.2007.10.046.
- Lardinois CK. The role of omega 3 fatty acids on insulin secretion and insulin sensitivity. Med Hypotheses. 1987;24:243–248. doi: 10.1016/0306-9877(87)90071-5.
- Mulvad G, Pedersen HS, Hansen JC, Dewailly E, Jul E, Pedersen M, Deguchi Y, Newman WP, Malcom GT, Tracy RE, Middaugh JP, Bjerreggard P. The Inuit diet. Fatty acids and antioxidants, their role in ischemic heart disease, and exposure to organochlorines and heavy metals. An international study. Arctic Med Res. 1996;55:20–24.
- Segall L, Lameloise N, Assimacopoulos-Jeannet F, Roche E, Corkey P, Thumelin S, Corkey BE, Prentki M. Lipid rather than glucose metabolism is implicated in altered insulin secretion caused by oleate in INS-1 cells. Am J Physiol. 1999;277:E521–E528.
- Grimble RF, Tappia PS. Modulation of pro-inflammatory cytokine biology by unsaturated fatty acids. Z Ernahrungswiss. 1998;37:57–65.
- Zhang M, Fritsche KL. Fatty acid-mediated inhibition of IL-12 production by murine macrophages is independent of PPARgamma. Br J Nutr. 2004;91:733–739. doi: 10.1079/BJN20041096.
Source: PubMed