DOI QR코드

DOI QR Code

Evaluation of fish oil-rich in MUFAs for anti-diabetic and anti-inflammation potential in experimental type 2 diabetic rats

  • Keapai, Waranya (Department of Physiology, Faculty of Medicine, Chiang Mai University) ;
  • Apichai, Sopida (Department of Occupational Therapy, Faculty of Associated Medical Sciences, Chiang Mai University) ;
  • Amornlerdpison, Doungporn (Faculty of Fisheries Technology and Aquatic Resources, Maejo University) ;
  • Lailerd, Narissara (Department of Physiology, Faculty of Medicine, Chiang Mai University)
  • Received : 2016.03.11
  • Accepted : 2016.08.16
  • Published : 2016.11.01

Abstract

The advantages of monounsaturated fatty acids (MUFAs) on insulin resistance and type 2 diabetes mellitus (T2DM) have been well established. However, the molecular mechanisms of the anti-diabetic action of MUFAs remain unclear. This study examined the anti-hyperglycemic effect and explored the molecular mechanisms involved in the actions of fish oil- rich in MUFAs that had been acquired from hybrid catfish (Pangasius larnaudii${\times}$Pangasianodon hypophthalmus) among experimental type 2 diabetic rats. Diabetic rats that were fed with fish oil (500 and 1,000 mg/kg BW) for 12 weeks significantly reduced the fasting plasma glucose levels without increasing the plasma insulin levels. The diminishing levels of plasma lipids and the muscle triglyceride accumulation as well as the plasma leptin levels were identified in T2DM rats, which had been administrated with fish oil. Notably, the plasma adiponectin levels increased among these rats. The fish oil supplementation also improved glucose tolerance, insulin sensitivity and pancreatic histological changes. Moreover, the supplementation of fish oil improved insulin signaling ($p-Akt^{Ser473}$ and p-PKC-${\zeta}/{\lambda}^{Thr410/403}$), $p-AMPK^{Thr172}$ and membrane GLUT4 protein expressions, whereas the protein expressions of pro-inflammatory cytokines (TNF-${\alpha}$ and nuclear NF-${\kappa}B$) as well as p-PKC-${\theta}^{Thr538}$ were down regulated in the skeletal muscle. These data indicate that the effects of fish oil-rich in MUFAs in these T2DM rats were partly due to the attenuation of insulin resistance and an improvement in the adipokine imbalance. The mechanisms of the anti-hyperglycemic effect are involved in the improvement of insulin signaling, AMPK activation, GLUT4 translocation and suppression of pro-inflammatory cytokine protein expressions.

Keywords

References

  1. Muoio DM, Newgard CB. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol. 2008;9:193-205. https://doi.org/10.1038/nrm2327
  2. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2010;33(Suppl 1):S62-69. https://doi.org/10.2337/dc10-S062
  3. Karlsson HK, Zierath JR. Insulin signaling and glucose transport in insulin resistant human skeletal muscle. Cell Biochem Biophys. 2007;48:103-113. https://doi.org/10.1007/s12013-007-0030-9
  4. DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes Care. 2009;32 Suppl 2:S157-163.
  5. Savage DB, Petersen KF, Shulman GI. Mechanisms of insulin resistance in humans and possible links with inflammation. Hypertension. 2005;45:828-833. https://doi.org/10.1161/01.HYP.0000163475.04421.e4
  6. Ye J. Mechanisms of insulin resistance in obesity. Front Med. 2013;7:14-24. https://doi.org/10.1007/s11684-013-0262-6
  7. Vaag A, Henriksen JE, Beck-Nielsen H. Decreased insulin activation of glycogen synthase in skeletal muscles in young nonobese Caucasian first-degree relatives of patients with non-insulin-dependent diabetes mellitus. J Clin Invest. 1992;89:782-788. https://doi.org/10.1172/JCI115656
  8. Huang S, Czech MP. The GLUT4 glucose transporter. Cell Metab. 2007;5:237-252. https://doi.org/10.1016/j.cmet.2007.03.006
  9. Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S, Cline GW, Befroy D, Zemany L, Kahn BB, Papademetris X, Rothman DL, Shulman GI. The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci U S A. 2007;104:12587-12594. https://doi.org/10.1073/pnas.0705408104
  10. Dresner A, Laurent D, Marcucci M, Griffin ME, Dufour S, Cline GW, Slezak LA, Andersen DK, Hundal RS, Rothman DL, Petersen KF, Shulman GI. Effects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activity. J Clin Invest. 1999;103:253-259. https://doi.org/10.1172/JCI5001
  11. Hotamisligil GS. Inflammatory pathways and insulin action. Int J Obes Relat Metab Disord. 2003;27 Suppl 3:S53-55. https://doi.org/10.1038/sj.ijo.0802502
  12. Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, Kraegen EW. Influence of dietary fat composition on development of insulin resistance in rats. Relationship to muscle triglyceride and omega-3 fatty acids in muscle phospholipid. Diabetes. 1991;40:280-289. https://doi.org/10.2337/diab.40.2.280
  13. Riccardi G, Giacco R, Rivellese AA. Dietary fat, insulin sensitivity and the metabolic syndrome. Clin Nutr. 2004;23:447-456. https://doi.org/10.1016/j.clnu.2004.02.006
  14. Due A, Larsen TM, Hermansen K, Stender S, Holst JJ, Toubro S, Martinussen T, Astrup A. Comparison of the effects on insulin resistance and glucose tolerance of 6-mo high-monounsaturatedfat, low-fat, and control diets. Am J Clin Nutr. 2008;87:855-862. https://doi.org/10.1093/ajcn/87.4.855
  15. Gillingham LG, Harris-Janz S, Jones PJ. Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors. Lipids. 2011;46:209-228. https://doi.org/10.1007/s11745-010-3524-y
  16. Paniagua JA, de la Sacristana AG, Sánchez E, Romero I, Vidal- Puig A, Berral FJ, Escribano A, Moyano MJ, Peréz-Martinez P, López-Miranda J, Pérez-Jiménez F. A MUFA-rich diet improves posprandial glucose, lipid and GLP-1 responses in insulin-resistant subjects. J Am Coll Nutr. 2007;26:434-444. https://doi.org/10.1080/07315724.2007.10719633
  17. Shah M, Adams-Huet B, Brinkley L, Grundy SM, Garg A. Lipid, glycemic, and insulin responses to meals rich in saturated, cismonounsaturated, and polyunsaturated (n-3 and n-6) fatty acids in subjects with type 2 diabetes. Diabetes Care. 2007;30:2993-2998. https://doi.org/10.2337/dc07-1026
  18. Moon JH, Lee JY, Kang SB, Park JS, Lee BW, Kang ES, Ahn CW, Lee HC, Cha BS. Dietary monounsaturated fatty acids but not saturated fatty acids preserve the insulin signaling pathway via IRS-1/PI3K in rat skeletal muscle. Lipids. 2010;45:1109-1116. https://doi.org/10.1007/s11745-010-3475-3
  19. Yang ZH, Miyahara H, Takemura S, Hatanaka A. Dietary saury oil reduces hyperglycemia and hyperlipidemia in diabetic KKAy mice and in diet-induced obese C57BL/6J mice by altering gene expression. Lipids. 2011;46:425-434. https://doi.org/10.1007/s11745-011-3553-1
  20. Keapai W, Apichai S, Pongchaidecha A, Amonlerdpison D, Lailerd N. Enhancing of skeletal glucose uptake by fish oil-derived MUFAs through glucose transporter 4 translocation in rat diaphragm. Proceeding of the International Graduate Research Conference; 2014 Dec 12; Chiang Mai, Thailand. HS7-12.
  21. Cruz-Teno C, Perez-Martínez P, Delgado-Lista J, Yubero-Serrano EM, Garcia-Ríos A, Marin C, Gomez P, Jimenez-Gomez Y, Camargo A, Rodriguez-Cantalejo F, Malagon MM, Perez-Jimenez F, Roche HM, Lopez-Miranda J. Dietary fat modifies the postprandial inflammatory state in subjects with metabolic syndrome: the LIPGENE study. Mol Nutr Food Res. 2012;56:854-865. https://doi.org/10.1002/mnfr.201200096
  22. Martín-Pelaez S, Covas MI, Fito M, Kusar A, Pravst I. Health effects of olive oil polyphenols: recent advances and possibilities for the use of health claims. Mol Nutr Food Res. 2013;57:760-771. https://doi.org/10.1002/mnfr.201200421
  23. AOAC. Official method 996.06: fat (total, saturated, and unsaturated) in foods. AOAC International 18th ed, 2005; Ch4:p.20-25.
  24. Srinivasan K, Viswanad B, Asrat L, Kaul CL, Ramarao P. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res. 2005;52:313-320. https://doi.org/10.1016/j.phrs.2005.05.004
  25. Matthews JN, Altman DG, Campbell MJ, Royston P. Analysis of serial measurements in medical research. BMJ. 1990;300:230-235. https://doi.org/10.1136/bmj.300.6719.230
  26. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412-419. https://doi.org/10.1007/BF00280883
  27. Frayn KN, Maycock PF. Skeletal muscle triacylglycerol in the rat: methods for sampling and measurement, and studies of biological variability. J Lipid Res. 1980;21:139-144.
  28. Mohammad A, Sharma V, McNeill JH. Vanadium increases GLUT4 in diabetic rat skeletal muscle. Mol Cell Biochem. 2002;233:139-143. https://doi.org/10.1023/A:1015558328757
  29. Rhoads MG, Kandarian SC, Pacelli F, Doglietto GB, Bossola M. Expression of NF-kappaB and IkappaB proteins in skeletal muscle of gastric cancer patients. Eur J Cancer. 2010;46:191-197. https://doi.org/10.1016/j.ejca.2009.10.008
  30. Musi N, Goodyear LJ. AMP-activated protein kinase and muscle glucose uptake. Acta Physiol Scand. 2003;178:337-345. https://doi.org/10.1046/j.1365-201X.2003.01168.x
  31. Hilder TL, Baer LA, Fuller PM, Fuller CA, Grindeland RE, Wade CE, Graves LM. Insulin-independent pathways mediating glucose uptake in hindlimb-suspended skeletal muscle. J Appl Physiol (1985). 2005;99:2181-2188. https://doi.org/10.1152/japplphysiol.00743.2005
  32. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 2002;51:2005-2011. https://doi.org/10.2337/diabetes.51.7.2005
  33. Jove M, Planavila A, Sánchez RM, Merlos M, Laguna JC, Vazquez-Carrera M. Palmitate induces tumor necrosis factoralpha expression in C2C12 skeletal muscle cells by a mechanism involving protein kinase C and nuclear factor-kappaB activation. Endocrinology. 2006;147:552-561. https://doi.org/10.1210/en.2005-0440
  34. Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, Iwahashi H, Kuriyama H, Ouchi N, Maeda K, Nishida M, Kihara S, Sakai N, Nakajima T, Hasegawa K, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Hanafusa T, Matsuzawa Y. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol. 2000;20:1595-1599. https://doi.org/10.1161/01.ATV.20.6.1595
  35. Al-Shoumer KA, Al-Asousi AA, Doi SA, Vasanthy BA. Serum leptin and its relationship with metabolic variables in Arabs with type 2 diabetes mellitus. Ann Saudi Med. 2008;28:367-370. https://doi.org/10.4103/0256-4947.51692
  36. Rabe K, Lehrke M, Parhofer KG, Broedl UC. Adipokines and insulin resistance. Mol Med. 2008;14:741-751.
  37. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fattyacid oxidation by activating AMP-activated protein kinase. Nat Med. 2002;8:1288-1295. https://doi.org/10.1038/nm788
  38. Shehzad A, Iqbal W, Shehzad O, Lee YS. Adiponectin: regulation of its production and its role in human diseases. Hormones (Athens). 2012;11:8-20.
  39. Paz-Filho G, Mastronardi C, Wong ML, Licinio J. Leptin therapy, insulin sensitivity, and glucose homeostasis. Indian J Endocrinol Metab. 2012;16(Suppl 3):S549-555. https://doi.org/10.4103/2230-8210.105571
  40. Yadav A, Kataria MA, Saini V, Yadav A. Role of leptin and adiponectin in insulin resistance. Clin Chim Acta. 2013;417:80-84. https://doi.org/10.1016/j.cca.2012.12.007
  41. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE, Tataranni PA. Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001;86:1930-1935. https://doi.org/10.1210/jcem.86.5.7463
  42. Zhang S, Zhang Q, Zhang L, Li C, Jiang H. Expression of ghrelin and leptin during the development of type 2 diabetes mellitus in a rat model. Mol Med Rep. 2013;7:223-228. https://doi.org/10.3892/mmr.2012.1154
  43. Watson RT, Pessin JE. Intracellular organization of insulin signaling and GLUT4 translocation. Recent Prog Horm Res. 2001;56:175-193. https://doi.org/10.1210/rp.56.1.175
  44. Michelle Furtado L, Poon V, Klip A. GLUT4 activation: thoughts on possible mechanisms. Acta Physiol Scand. 2003;178:287-296. https://doi.org/10.1046/j.1365-201X.2003.01160.x
  45. Dimopoulos N, Watson M, Sakamoto K, Hundal HS. Differential effects of palmitate and palmitoleate on insulin action and glucose utilization in rat L6 skeletal muscle cells. Biochem J. 2006;399:473-481. https://doi.org/10.1042/BJ20060244
  46. Tavaré JM, Fletcher LM, Oatey PB, Tyas L, Wakefield JG, Welsh GI. Lighting up insulin action. Diabet Med. 2001;18:253-260. https://doi.org/10.1046/j.1464-5491.2001.00540.x
  47. Nardi F, Lipina C, Magill D, Hage Hassan R, Hajduch E, Gray A, Hundal HS. Enhanced insulin sensitivity associated with provision of mono and polyunsaturated fatty acids in skeletal muscle cells involves counter modulation of PP2A. PLoS One. 2014;9:e92255. https://doi.org/10.1371/journal.pone.0092255
  48. Coll T, Eyre E, Rodriguez-Calvo R, Palomer X, Sanchez RM, Merlos M, Laguna JC, Vazquez-Carrera M. Oleate reverses palmitateinduced insulin resistance and inflammation in skeletal muscle cells. J Biol Chem. 2008;283:11107-11116. https://doi.org/10.1074/jbc.M708700200
  49. Friedrichsen M, Mortensen B, Pehmoller C, Birk JB, Wojtaszewski JF. Exercise-induced AMPK activity in skeletal muscle: role in glucose uptake and insulin sensitivity. Mol Cell Endocrinol. 2013;366:204-214. https://doi.org/10.1016/j.mce.2012.06.013
  50. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001;414:799-806. https://doi.org/10.1038/414799a
  51. Hardie DG. Role of AMP-activated protein kinase in the metabolic syndrome and in heart disease. FEBS Lett. 2008;582:81-89. https://doi.org/10.1016/j.febslet.2007.11.018
  52. Bolsoni-Lopes A, Festuccia WT, Chimin P, Farias TS, Torres-Leal FL, Cruz MM, Andrade PB, Hirabara SM, Lima FB, Alonso-Vale MI1. Palmitoleic acid (n-7) increases white adipocytes GLUT4 content and glucose uptake in association with AMPK activation. Lipids Health Dis. 2014;13:199. https://doi.org/10.1186/1476-511X-13-199
  53. Chavez JA, Summers SA. Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3-L1 adipocytes and C2C12 myotubes. Arch Biochem Biophys. 2003;419:101-109. https://doi.org/10.1016/j.abb.2003.08.020
  54. Griffin ME, Marcucci MJ, Cline GW, Bell K, Barucci N, Lee D, Goodyear LJ, Kraegen EW, White MF, Shulman GI. Free fatty acidinduced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade. Diabetes. 1999;48:1270-1274. https://doi.org/10.2337/diabetes.48.6.1270
  55. Yu C, Chen Y, Cline GW, Zhang D, Zong H, Wang Y, Bergeron R, Kim JK, Cushman SW, Cooney GJ, Atcheson B, White MF, Kraegen EW, Shulman GI. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem. 2002;277:50230-50236. https://doi.org/10.1074/jbc.M200958200
  56. Kanety H, Feinstein R, Papa MZ, Hemi R, Karasik A. Tumor necrosis factor alpha-induced phosphorylation of insulin receptor substrate-1 (IRS-1). Possible mechanism for suppression of insulinstimulated tyrosine phosphorylation of IRS-1. J Biol Chem. 1995;270:23780-23784. https://doi.org/10.1074/jbc.270.40.23780
  57. Green CJ, Pedersen M, Pedersen BK, Scheele C. Elevated NF-${\kappa}B$ activation is conserved in human myocytes cultured from obese type 2 diabetic patients and attenuated by AMP-activated protein kinase. Diabetes. 2011;60:2810-2819. https://doi.org/10.2337/db11-0263

Cited by

  1. The Mediterranean diet and risk of type 2 diabetes in Iranian population vol.73, pp.1, 2016, https://doi.org/10.1038/s41430-018-0336-2
  2. Antihyperglycemic effect of rice husk derived xylooligosaccharides in high‐fat diet and low‐dose streptozotocin‐induced type 2 diabetic rat model vol.8, pp.1, 2016, https://doi.org/10.1002/fsn3.1327
  3. Detection of Early Disease Risk Factors Associated with Metabolic Syndrome: A New Era with the NMR Metabolomics Assessment vol.12, pp.3, 2016, https://doi.org/10.3390/nu12030806
  4. Effects of cashew nut consumption on body composition and glycemic indices: A meta-analysis and systematic review of randomized controlled trials vol.15, pp.2, 2016, https://doi.org/10.1016/j.dsx.2021.02.038