Ukr.Biochem.J. 2014; Volume 86, Issue 1, Jan-Feb, pp. 101-110

doi: http://dx.doi.org/10.15407/ubj86.01.101

The effect of N-stearoylethanolamine on liver phospholipid composition of rats with insulin resistance caused by alimentary obesity

O. V. Onopchenko, G. V. Kosiakova, T. M. Goridko, V. M. Klimashevsky, N. M. Hula

Palladin Institute of Biochemistry, National Academy of Sciences of Ukraine, Kyiv;
e-mail: onop.89.av@mail.ru

We used alimentary obesity-induced insulin resistance (IR) model in rats to investigate the influence of N-stearoylethanolamine on the content of phospholipids and their fatty acid composition.  Our results show that prolonged high-fat diet triggers considerable aberrations in the composition of main phospholipids in the liver and can be one of the causes of IR in rats. In particular, the increase of phosphatidylcholine, phosphatidylethanolamine and significant decrease of other phospholipids: lysophosphatidylcholine, lysophosphatidylethanolamine, sphingomyelin, phosphatidylinositol, phosphatidylserine and diphosphaglicerol were observed. The levels of monounsaturated (erucic, nervonic, oleic) and polyunsaturated (eicosatrienoic, docosatrienoic, arachidonic) fatty acids were increased; meanwhile the content of diunsaturated acids was decreased.  The NSE administration (50 mg/kg of body weight) caused restoration of the phospholipids content in the liver of rats with diet-induced IR that highly correlated with the decrease in plasma insulin level and the improvement of insulin sensitivity. Moreover, the effect of NSE was accompanied by the normalization of fatty acids composition of phospholipids that could be related to modulating influen­ce of NSE on the activity of the main fatty acid desaturases.  It is known that the imbalance in phospholipid composition of the rat liver causes substantial metabolic alterations that are associated with the development of IR. Accordingly, the compensations of the imbalance by NSE can help to restore insulin sensitivity, inhibit the development of obesity, IR and type 2 diabetes.

Keywords: , , , ,


References:

  1. Pereira-Lancha LO, Campos-Ferraz PL, Lancha AH Jr. Obesity: considerations about etiology, metabolism, and the use of experimental models. Diabetes Metab Syndr Obes. 2012;5:75-87. Epub 2012 Apr 10. PubMed, PubMedCentral, CrossRef
  2. Zeghari N, Younsi M, Meyer L, Donner M, Drouin P, Ziegler O. Adipocyte and erythrocyte plasma membrane phospholipid composition and hyperinsulinemia: a study in nondiabetic and diabetic obese women. Int J Obes Relat Metab Disord. 2000 Dec;24(12):1600-7. PubMed, CrossRef
  3. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001 Dec 13;414(6865):799-806. PubMed, CrossRef
  4. Kosiakova HV, Hula NM. The N-stearoylethanolamine effect on the NO-synthase way of nitrogen oxide formation and phospholipid composition of erythrocyte membranes in rats with streptozotocine diabetes. Ukr Biokhim Zhurn. 2007 Nov-Dec;79(6):53-9. PubMed
  5. Gula NM, Goridko TM, Stogniy NA, Klymashevsky VM, Meged OF, Kosyakova GV, Shovkun SA, Kindruk NL, Berdyshev AG. Protective effect of N‑stearoylethanolamine under acute alcohol intoxication in rats. Ukr Biokhim Zhurn. 2010 Mar-Apr;82(2):42-52. PubMed
  6. Onopchenko OV, Kosiakova GV, Goridko TM, Berdyschev AG, Meged OF, Hula NM. The effect of N-stearoylethanolamine on the activity of ant ioxidant enzymes, content of lipid peroxidation products and nitric oxide in the blood plasma and liver of rats with induced insulin-resistance. Ukr. Biokhim. Zhurn. 2013 Sep-Oct;85(5):88–96. PubMed
  7. Hosker JP, Matthews DR, Rudenski AS, Burnett MA, Darling P, Bown EG, Turner RC. Continuous infusion of glucose with model assessment: measurement of insulin resistance and beta-cell function in man. Diabetologia. 1985 Jul;28(7):401-11. PubMed, CrossRef
  8. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911-7. PubMed, CrossRef
  9. Vaskovsky VE, Terekhova TA. HPTLC of phospholipids mixtures containing phosphatidylglycerol. J High Resolut Chromatogr Chromatogr Commun. 1979;2(11):671–672.  CrossRef
  10. Svetashev VI, Vaskovsky VE. A simplified technique for thin-layer microchromatography of lipids. J Chromatogr. 1972 May 3;67(2):376-8. PubMed, CrossRef
  11. Vaskovsky VE, Kostetsky EY, Vasendin IM. A universal reagent for phospholipid analysis. J Chromatogr. 1975 Nov 12;114(1):129-41. PubMed, CrossRef
  12. Carreau. JP, Dubacq JP. Adaptation of a macro-scale methods to the micro-scale for fatty acid methyl transcsterification of biological lipid extracts. J Chromatogr. 1978;151(3):384-390.  CrossRef
  13. Chow LS, Li S, Eberly LE, Seaquist ER, Eckfeldt JH, Hoogeveen RC, Couper DJ, Steffen LM, Pankow JS. Estimated plasma stearoyl co-A desaturase-1 activity and risk of incident diabetes: the atherosclerosis risk in communities (ARIC) study. Metabolism. 2013 Jan;62(1):100-8. Epub 2012 Jul 21. PubMed, PubMedCentral, CrossRef
  14. Uchida T. Stimulation of phospholipid synthesis in HeLa cells by epidermal growth factor and insulin: activation of choline kinase and glycerophosphate acyltransferase. Biochim Biophys Acta. 1996 Nov 22;1304(2):89-104. PubMed, CrossRef
  15. Kiechle FL, Sykes E, Artiss JD. Insulin and adenosine regulate the phosphatidylcholine concentration in isolated rat adipocyte plasma membranes. Ann Clin Lab Sci. 1995 Jul-Aug;25(4):310-8. PubMed
  16. Cui Z, Houweling M. Phosphatidylcholine and cell death. Biochim Biophys Acta. 2002 Dec 30;1585(2-3):87-96. Review. PubMed, CrossRef
  17. Vance DE. Physiological roles of phosphatidylethanolamine N-methyltransferase. Biochim Biophys Acta. 2013 Mar;1831(3):626-32. Epub 2012 Jul 31. Review. PubMed, CrossRef
  18. Schuiki I, Daum G. Phosphatidylserine decarboxylases, key enzymes of lipid metabolism. IUBMB Life. 2009 Feb;61(2):151-62. Review. PubMed, CrossRef
  19. Slater SJ, Kelly MB, Taddeo FJ, Ho C, Rubin E, Stubbs CD. The modulation of protein kinase C activity by membrane lipid bilayer structure. J Biol Chem. 1994 Feb 18;269(7):4866-71. PubMed
  20. Zolese G, Wozniak M, Mariani P, Saturni L, Bertoli E, Ambrosini A. Different modulation of phospholipase A2 activity by saturated and monounsaturated N-acylethanolamines. J Lipid Res. 2003 Apr;44(4):742-53. PubMed, CrossRef
  21. Barber MN, Risis S, Yang C, Meikle PJ, Staples M, Febbraio MA, Bruce CR. Plasma lysophosphatidylcholine levels are reduced in obesity and type 2 diabetes. PLoS One. 2012;7(7):e41456. Epub 2012 Jul 25. PubMed, PubMedCentral, CrossRef
  22. Fuller N, Rand RP. The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranes. Biophys J. 2001 Jul;81(1):243-54. PubMed, PubMedCentral, CrossRef
  23. Mosior M, Newton AC. Mechanism of the apparent cooperativity in the interaction of protein kinase C with phosphatidylserine. Biochemistry. 1998 Dec 8;37(49):17271-9. PubMed, CrossRef
  24. Sweet LJ, Dudley DT, Pessin JE, Spector AA. Phospholipid activation of the insulin receptor kinase: regulation by phosphatidylinositol. FASEB J. 1987 Jul;1(1):55-9. PubMed
  25. Goridko T. M., Gula N. M., Stogniy N. A., Meged O. F., Klimashevsky V. M., Shovkun S. A., Kindruk N. L., Berdyshev A. G. Influence of N‑stearoylethanolamine on the lipid peroxidation process and lipid composition of the rat liver under acute morphine intoxication. Ukr Biokhim Zhurn. 2007 Sep-Oct;79(5):175-85. PubMed
  26. Lingwood D, Kaiser HJ, Levental I, Simons K. Lipid rafts as functional heterogeneity in cell membranes. Biochem Soc Trans. 2009 Oct;37(Pt 5):955-60. Review. PubMed, CrossRef
  27. Stratford S, Hoehn KL, Liu F, Summers SA. Regulation of insulin action by ceramide: dual mechanisms linking ceramide accumulation to the inhibition of Akt/protein kinase B. J Biol Chem. 2004 Aug 27;279(35):36608-15. PubMed, CrossRef
  28. Widlansky ME, Wang J, Shenouda SM, Hagen TM, Smith AR, Kizhakekuttu TJ, Kluge MA, Weihrauch D, Gutterman DD, Vita JA. Altered mitochondrial membrane potential, mass, and morphology in the mononuclear cells of humans with type 2 diabetes. Transl Res. 2010 Jul;156(1):15-25. Epub 2010 May 11. PubMed, PubMedCentral, CrossRef
  29. Ruddock MW, Stein A, Landaker E, Park J, Cooksey RC, McClain D, Patti ME. Saturated fatty acids inhibit hepatic insulin action by modulating insulin receptor expression and post-receptor signalling. J Biochem. 2008 Nov;144(5):599-607. Epub 2008 Aug 19. PubMed, CrossRef
  30. Wang Y, Botolin D, Xu J, Christian B, Mitchell E, Jayaprakasam B, Nair MG, Peters JM, Busik JV, Olson LK, Jump DB. Regulation of hepatic fatty acid elongase and desaturase expression in diabetes and obesity. J Lipid Res. 2006 Sep;47(9):2028-41. PubMed, PubMedCentral, CrossRef
  31. Gutiérrez-Juárez R, Pocai A, Mulas C, Ono H, Bhanot S, Monia BP, Rossetti L. Critical role of stearoyl-CoA desaturase-1 (SCD1) in the onset of diet-induced hepatic insulin resistance. J Clin Invest. 2006 Jun;116(6):1686-95. PubMed, PubMedCentral, CrossRef
  32. Flowers MT, Ntambi JM. Role of stearoyl-coenzyme A desaturase in regulating lipid metabolism. Curr Opin Lipidol. 2008 Jun;19(3):248-56. Review. PubMed, PubMedCentral, CrossRef
  33. Terrazzino S, Berto F, Dalle Carbonare M, Fabris M, Guiotto A, Bernardini D, Leon A. Stearoylethanolamide exerts anorexic effects in mice via down-regulation of liver stearoyl-coenzyme A desaturase-1 mRNA expression. FASEB J. 2004 Oct;18(13):1580-2. Epub 2004 Aug 2. PubMed
  34. Guillou H, Zadravec D, Martin PG, Jacobsson A. The key roles of elongases and desaturases in mammalian fatty acid metabolism: Insights from transgenic mice. Prog Lipid Res. 2010 Apr;49(2):186-99. Epub 2009 Dec 16. Review. PubMed, CrossRef
  35. Demcakova E, Sebokova, Ukropec J, Gasperikova D, Klimes I. Delta-6 desaturase activity and gene expression, tissue fatty acid profile and glucose turnover rate in hereditary hypertriglyceridemic rats. Endocr Regul. 2001 Dec;35(4):179-86. PubMed
  36. Porter NA, Caldwell SE, Mills KA. Mechanisms of free radical oxidation of unsaturated lipids. Lipids. 1995 Apr;30(4):277-90. Review. PubMed, CrossRef
  37. Hunt JV, Smith CC, Wolff SP. Autoxidative glycosylation and possible involvement of peroxides and free radicals in LDL modification by glucose. Diabetes. 1990 Nov;39(11):1420-4. PubMed, CrossRef
  38. Raina N, Matsui J, Cunnane SC, Jeejeebhoy KN. Effect of tumor necrosis factor-alpha on triglyceride and phospholipid content and fatty acid composition of liver and carcass in rats. Lipids. 1995 Aug;30(8):713-8. PubMed, CrossRef
  39. Ollila S, Hyvönen MT, Vattulainen I. Polyunsaturation in lipid membranes: dynamic properties and lateral pressure profiles. J Phys Chem B. 2007 Mar 29;111(12):3139-50. Epub 2007 Mar 3. PubMed, CrossRef

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.