Skip to main content
Log in

Soybean oil treatment impairs glucose-stimulated insulin secretion and changes fatty acid composition of normal and diabetic islets

  • Original
  • Published:
Acta Diabetologica Aims and scope Submit manuscript

Abstract

We investigated the effect of sub-chronic soybean oil (SO) treatment on the insulin secretion and fatty acid composition of islets of Langerhans obtained from Goto-Kakizaki (GK), a model of type 2 diabetes, and normal Wistar rats. We observed that soybean-treated Wistar rats present insulin resistance and defective islet insulin secretion when compared with untreated Wistar rats. The decrease in insulin secretion occurred at all concentrations of glucose and arginine tested. Furthermore we observed that soybean-treated normal islets present a significant decrease in two saturated fatty acids, myristic and heneicosanoic acids, and one monounsaturated eicosenoic acid, and the appearance of the monounsaturated erucic acid. Concerning diabetic animals, we observed that soybean-treated diabetic rats, when compared with untreated GK rats, present an increase in plasma non-fasting free fatty acids, an exacerbation of islet insulin secretion impairment in all conditions tested and a significant decrease in the monounsaturated palmitoleic acid. Altogether our results show that SO treatment results in a decrease of insulin secretion and alterations on fatty acid composition in normal and diabetic islets. Furthermore, the impairment of insulin secretion, islet erucic acid and fasting plasma insulin levels are similar in treated normal and untreated diabetic rats, suggesting that SO could have a deleterious effect on β-cell function and insulin sensitivity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Zimmet P, Cowie C, Ekoe J, Shan JE (2004) Classification of diabetes mellitus and other categories of glucose intolerance. In: DeFronzo RA, Ferrannini E, Keen H, Zimmet P (eds) International textbook of diabetes mellitus, 3rd Edn. John Wiley & Sons Ltd, England, pp 3–14

    Google Scholar 

  2. Golay A, Ybarra J (2005) Link between obesity and type 2 diabetes. Best Pract Res Clin Endocrinol Metab 19:649–663

    Article  PubMed  CAS  Google Scholar 

  3. Capito K, Hansen SE, Hedeskov CJ, Islin H, Thams P (1992) Fat-induced changes in mouse pancreatic islet insulin secretion, insulin biosynthesis and glucose metabolism. Acta Diabetol 8:193–198

    Article  Google Scholar 

  4. Mason TM, Goh T, Tchipashvili V, Sandhu H, Gupta N, Lewis GF, Giacca A (1999) Prolonged elevation of plasma free fatty acids desensitizes the insulin secretory response to glucose in vivo in rats. Diabetes 48:524–530

    Article  PubMed  CAS  Google Scholar 

  5. Zhou YP, Grill VE (1994) Long-term exposure of rat pancreatic islets to fatty acids inhibits glucose-induced insulin secretion and biosynthesis through a glucose fatty acid cycle. J Clin Invest 93:870–876

    PubMed  CAS  Google Scholar 

  6. Randle PJ (1998) Regulatory interaction between lipids and carbohydrates: the glucose fatty acid cycle after 35 years. Diabetes Metab Rev 14:263–283

    Article  PubMed  CAS  Google Scholar 

  7. Carlsson C, Borg LAH, Welsh N (1999) Sodium palmitate induces partial mitochondrial uncoupling and reactive oxygen species in rat pancreatic islets in vitro. Endocrinology 140:3422–3428

    Article  PubMed  CAS  Google Scholar 

  8. Garvey WT (2004) Mechanisms of insulin signal transduction. In DeFronzo RA, Ferrannini E, Keen H, Zimmet P (eds) International textbook of diabetes mellitus, 3rd Edn. John Wiley & Sons Ltd, England, pp 227–252

    Google Scholar 

  9. Kishore P, Tonelli J, Koppaka S (2006) Time-dependent effects of free Fatty acids on glucose effectiveness in type 2 diabetes. Diabetes 55:1761–1768

    Article  PubMed  CAS  Google Scholar 

  10. Winzell MS, Strom K, Holm C, Ahren B (2006) Glucose-stimulated insulin secretion correlates with beta-cell lipolysis. Nutr Metab Cardiovasc Dis 16[Suppl 1]:S11–S16

    Article  PubMed  CAS  Google Scholar 

  11. Briaud I, Kelpe CL, Johnson LM, Tran POT, Poitout V (2002) Differential effects of hyperlipidemia on insulin secretion in islets of Langerhans from hyperglycaemic versus normoglycemic rats. Diabetes 51:662–668

    Article  PubMed  CAS  Google Scholar 

  12. Tinahones FJ, Pareja A, Soringuer FJ, Gómez-Zumaquero JM, Cardona F, Rojo-Martínez G (2002) Dietary fatty acids modify insulin secretion of rat pancreatic islet cells in vitro. J. Endocrinol Invest 25:436–441

    PubMed  CAS  Google Scholar 

  13. Haber EP, Proscopio J, Carvalho CR, Carpinelli AR, Newsholme P, Curi R (2006) New insights into fatty acids modulation of pancreatic beta-cell function. Int Rev Cytol 248:1–41

    PubMed  CAS  Google Scholar 

  14. Hulbert AJ, Turner N, Storlien LH, Else PL (2005) Dietary fatty acids and membrane function: implications for metabolism and disease. Biol Rev Camb Philos Soc 80:155–169

    Article  PubMed  CAS  Google Scholar 

  15. Mishra R, Simonson MS (2005) Sturated free fatty acids and apoptosis in microvascular measangial cells: palmitate activates pro-apoptotic signalling involving caspase 9 and mitochondrial release of endonuclease G. Cardiovasc Diabetol 4:2

    Article  PubMed  CAS  Google Scholar 

  16. Riedel MJ, Light PE (2005) Saturated and cis/trans unsaturated acyl CoA esters differentially regulate wild-type and polymorphic β-cell ATP-sensitive K+ channels. Diabetes 54:2070–2079

    Article  PubMed  CAS  Google Scholar 

  17. Stubhaug I, Tocher DR, Bell JG, Dick JR, Torstensen BE (2005) Fatty acids metabolism in Atlantic salmon (Salmo salar L.) hepatocytes and influence of dietary vegetable oil. Biochim Biophys Acta 1734:277–288

    PubMed  CAS  Google Scholar 

  18. Dobbins RL, Szczepaniak LS, Myhill J (2002) The composition of dietary fat directly influences glucose-stimulated insulin secretion in rats. Diabetes 51:1825–1833

    Article  PubMed  CAS  Google Scholar 

  19. Azevedo-Martins AK, Monteiro AP, Lima CL, Lenzen S, Curi R (2006) Fatty acids-induced toxicity and neutral lipid accumulation in insulin-producing RINm5F cells. Toxicol In Vitro 20:1106–1113

    Article  PubMed  CAS  Google Scholar 

  20. Xiao C, Giacca A, Carpentier A, Lewis GF (2006) Differential effects of monounsaturated, polyunsaturated and saturated fat ingestion on glucose-stimulated insulin secretion, sensitivity and clearance in overweight and obese, nondiabetic humans. Diabetologia 49:1371–1379

    Article  PubMed  CAS  Google Scholar 

  21. Alstrup KK, Brock B, Hermansen K (2004) Long-term exposure of INS-1 cells to cis and trans fatty acids influences insulin release and fatty acids oxidation differentially. Metabolism 53:1158–1165

    Article  PubMed  CAS  Google Scholar 

  22. Sudha V, Radhika G, Mohan V (2004) Current dietary trends in the management of diabetes. Indian J Med Res 120:4–8

    PubMed  CAS  Google Scholar 

  23. Rocca AS, LaGreca J, Kalitsky J, Brubaker PL (2005) Monousaturated fatty acid diets improve glycaemia tolerance through increased secretion of glucagons-like peptide-1. Endocrinology 142:1148–1155

    Article  Google Scholar 

  24. van Dam RM, Willett WC, Rimm EB, Stampfer MJ, Hu FB (2002) Dietary fat and meat intake in relation to risk of type 2 diabetes in men. Diabetes Care 25:417–424

    Article  PubMed  Google Scholar 

  25. Biden TJ, Robinson D, Cordery D, Hughes WE, Busch AK (2004) Chronic effects of fatty acids on pancreatic β-cell function. New insights from functional genomics. Diabetes 53:S159–S165

    Article  PubMed  CAS  Google Scholar 

  26. Briaud I, Harmon JS, Kelpe CL, Segu VB, Poitout V (2001) Lipotoxicity of the pancreatic beta-cell is associated with glucose-dependent esterification of fatty acids into neutral lipids. Diabetes 50:315–321

    Article  PubMed  CAS  Google Scholar 

  27. Maedler K, Spinas GA, Dyntar D, Moritz W, Kaiser N, Donath MY (2001) Distinct effects of saturated and monounsaturated fatty acids on β-cell turnover and function. Diabetes 50:69–76

    Article  PubMed  CAS  Google Scholar 

  28. Maedler K, Oberholzer J, Bucher P, Spinas GA, Donath MY (2003) Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic β-cell turnover and function. Diabetes 52:726–733

    Article  PubMed  CAS  Google Scholar 

  29. Nettleton JA, Katz R (2005) n-3 Long-chain polyunsaturated fatty acids in type 2 diabetes: a review. J Am Diet Assoc 105:428–440

    Article  PubMed  CAS  Google Scholar 

  30. Wang X, Li H, De Leo D (2004) Gene and protein kinase expression profiling of reactive oxygen species-associated lipotoxicity in the pancreatic β-cell line MIN6. Diabetes 53:129–140

    Article  PubMed  CAS  Google Scholar 

  31. Calder PC (2003) Long-chain n-3 fatty acids and inflammation: potential application in surgical and trauma patients. Braz J Med Biol Res 36:433–446

    Article  PubMed  CAS  Google Scholar 

  32. Nishimura M, Yamauchi A, Yamaguchi M, Ueda N, Naito S (2005) Soybean oil in total parenteral nutrition maintains albumin and antioxidant enzyme mRNA levels. Biol Pharm Bull 28:1265–1269

    Article  PubMed  CAS  Google Scholar 

  33. Stark AH, Timar B, Madar Z (2000) Adaptation of Sprague Dawley rats to long-term feeding of high fat or high fructose diets. Eur J Nutr 39:229–234

    Article  PubMed  CAS  Google Scholar 

  34. Pellizzon M, Buison A, Ordiz F Jr, Santana Ana L, Jen KL (2002) Effects of dietary fatty acids and exercise on bodyweight regulation and metabolism in rats. Obes Res 10:947–955

    PubMed  CAS  Google Scholar 

  35. Jen KLC, Buison A, Pellizzon M, Ordiz F Jr, Santa Ana L, Brown J (2003) Differential effects of fatty acids and exercise on body weight regulation and metabolism in female Wistar rats. Exp Biol Med 228:843–849

    CAS  Google Scholar 

  36. Picinato MC, Curi R, Machado UF, Carpinelli AR (1998) Soybean-and olive-oils-enriched diets increase insulin secretion to glucose stimulus in isolated pancreatic rat islets. Physiol Behav 65:289–294

    Article  PubMed  CAS  Google Scholar 

  37. Hermansen K, Sondergaard M, Hoie L, Carstensen M, Brock B (2001) Beneficial effects of soy-based dietary supplement on lipid levels and cardiovascular risk markers in type 2 diabetic subjects. Diabetes Care 24:228–233

    Article  PubMed  CAS  Google Scholar 

  38. Shang W, Yasuda K, Takahashi A (2002) Effect of high dietary fat on insulin secretion in genetically diabetic Goto-Kakizaki rats. Pancreas 25:393–399

    Article  PubMed  Google Scholar 

  39. Chen H, Sullivan G, Quon MJ (2005) Assessing the predictive accuracy of QUICKI as a surrogate index for insulin sensitivity using a calibration model. Diabetes 54:1914–1925

    Article  PubMed  CAS  Google Scholar 

  40. Seiça RM, Suzuki KI, Santos RM, Rosário LM (2004) Impaired insulin secretion in isolated islets of Goto-Kakizaki rats, an animal model of non obese type 2 diabetes, is a primary event. Acta Med Port 17:42–48 (In Portuguese)

    PubMed  Google Scholar 

  41. Bergsten P, Hellman B (1993) Glucose-induced amplitude regulation of pulsatile insulin secretion from individual pancreatic islets. Diabetes 42:670–674

    Article  PubMed  CAS  Google Scholar 

  42. Rosa D, Catalá A (1998) Fatty acids profiles and non enzymatic lipid peroxidation of microsomes and mitochondria from bovine liver, kidney, lung and heart. Arch Physiol Biochem 106:33–37

    Article  PubMed  CAS  Google Scholar 

  43. Peixoto F, Vicente J, Madeira VMC (2004) A comparative study of plant and animal mitochondria exposed to paraquat reveals that hydrogen peroxide is not related to the observed toxicity. Toxicol in Vitro 18:733–739

    Article  PubMed  CAS  Google Scholar 

  44. Goto Y, Kakizaki M (1981) The spontaneous diabetic rat a model of noninsulin dependent diabetes mellitus. Proc Jpn Acad 57:381–384

    Article  Google Scholar 

  45. Seiça RM, Martins MJ, Pessa PB (2003) Morphological changes of islet of Langerhans in an animal model of type 2 diabetes. Acta Med Port 16:381–388 (In Portuguese)

    PubMed  Google Scholar 

  46. Portha B (2005) Programmed disorders of β-cell development and function as one cause for type 2 diabetes? The GK rat paradigm. Diabetes Metab Res Rev 21:495–504

    Article  PubMed  CAS  Google Scholar 

  47. Ihara Y, Toyokuni S, Uchida K (1999) Hyperglycemia causes oxidative stress in pancreatic β-cells of GK rats, a model of type 2 diabetes. Diabetes 48:927–932

    Article  PubMed  CAS  Google Scholar 

  48. Dolz M, Bailbe D, Giroix MH (2005) Restitution of defective glucose-stimulated insulin secretion in diabetic GK rat by acetylcholine uncovers paradoxical stimulatory effect of beta-cell muscarinic receptor activation on cAMP production. Diabetes 54:3229–3237

    Article  PubMed  CAS  Google Scholar 

  49. Warwar N, Efendic S, Ostenson C, Haber EP, Cerasi E, Nesher R (2006) Dynamics of glucose-induced localization of PKC isoenzymes in pancreatic β-cell. Diabetes-related changes in the GK rats. Diabetes 55:590–599

    Article  PubMed  CAS  Google Scholar 

  50. Bjorntorp P (2004) The relationship between obesity and diabetes — The role of neuroendocrine and autonomic factors. In DeFronzo RA, Ferrannini E, Keen H, Zimmet P (eds) International textbook of diabetes mellitus, 3rd Edn. John Wiley & Sons Ltd, England, pp 565–582

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Seiça.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nunes, E., Peixoto, F., Louro, T. et al. Soybean oil treatment impairs glucose-stimulated insulin secretion and changes fatty acid composition of normal and diabetic islets. Acta Diabetol 44, 121–130 (2007). https://doi.org/10.1007/s00592-007-0252-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00592-007-0252-8

Key words

Navigation