Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Relationship between red cell membrane fatty acids and adipokines in individuals with varying insulin sensitivity

European Journal of Clinical Nutrition volume 65, pages 690–695 (2011)Cite this article

Subjects

Abstract

Background/Objectives:

Plasma leptin and adiponectin, and membrane phospholipid fatty acid composition are implicated into the mechanism of insulin resistance but no clear pattern has emerged. Hence, this study examined these variables in subjects presenting to the diabetic clinic for a diagnostic glucose tolerance test.

Subjects/Methods:

Body composition, glucose, glycated hemoglobin, insulin, leptin, adiponectin, and red cell and plasma phospholipid fatty acids were assessed from 42 normal and 28 impaired glucose tolerant subjects. Insulin sensitivity was determined by homeostatic model assessment.

Results:

The plasma phosphatidylcholine fatty acid composition of the impaired glucose tolerant subjects was similar to that of normal subjects. However, the impaired glucose tolerant subjects had significantly lower linoleic (P<0.05), eicosapentaenoic (P<0.05) and docosahexaenoic (P<0.01) acids in the red cell phosphatidylcholine and phosphatidylethanolamine compared with the normal subjects. Moreover, red cell phosphatidylcholine docosahexaenoic acid correlated positively with adiponectin (r=0.290, P<0.05) but negatively with leptin (r=−0.252, P<0.05), insulin (r=−0.335, P<0.01) and insulin resistance (r=−0.322, P<0.01). Plasma triglycerides, leptin and glucose combined predicted about 60% of variation in insulin level whereas insulin was the only component that predicted the membrane fatty acids.

Conclusions:

We postulate that membrane phospholipids fatty acids have an indirect role in determining insulin concentration but insulin has a major role in determining membrane fatty acid composition.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  • Allen HG, Allen JC, Boyd LC, Alston-Mills BP, Fenner GP (2006). Determination of membrane lipid differences in insulin resistant diabetes mellitus type 2 in whites and blacks. Nutrition 22, 1096–1102.

    Article  CAS  PubMed  Google Scholar 

  • Almeida-Pititto BD, Gimeno SG, Sanudo A, Ribeiro-Filho FF, Ferreira SR, Japanese-Brazilian Diabetes Study Group (2005). Leptin is associated with insulin resistance in Japanese migrants. Metab Syndr Relat Disord 3, 140–146.

    Article  PubMed  Google Scholar 

  • Aurora R, Gothard P, Thomas B, Lowy C, Min Y, Ghebremeskel K (2005). High dose of MaxEPA treatment reduces fat mass of diet-treated type 2 diabetic patients. 23rd International Symposium on Diabetes and Nutrition. Ebeltoft: Denmark (abstract).

    Google Scholar 

  • Banga A, Unal R, Tripathi P, Pokrovskaya I, Owens RJ, Kern PA et al. (2009). Adiponectin translation is increased by the PPARgamma agonists pioglitazone and omega-3 fatty acids. Am J Physiol Endocrinol Metab 296, E480–E489.

    Article  CAS  PubMed  Google Scholar 

  • Clore JN, Harris PA, Li J, Azzam A, Gill R, Zuelzer W et al. (2000). Changes in phosphatidylcholine fatty acid composition are associated with altered skeletal muscle insulin responsiveness in normal man. Metabolism 49, 232–238.

    Article  CAS  PubMed  Google Scholar 

  • Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR et al. (1996). Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334, 292–295.

    Article  CAS  PubMed  Google Scholar 

  • Dang AQ, Faas FH, Jethmalani SM, Carter WJ (1991). Decreased incorporation of long-chain fatty acids into erythrocyte phospholipids of STZ-D rats. Diabetes 40, 1645–1651.

    Article  CAS  PubMed  Google Scholar 

  • Delarue J, LeFoll C, Corporeau C, Lucas D (2004). N-3 long chain polyunsaturated fatty acids: a nutritional tool to prevent insulin resistance associated to type 2 diabetes and obesity? Reprod Nutr Develop 44, 289–299.

    Article  CAS  Google Scholar 

  • Esteghamati A, Khalilzadeh O, Anvari M, Rashidi A, Mokhtari M, Nakhjavani M (2009). Association of serum leptin levels with homeostasis model assessment-estimated insulin resistance and metabolic syndrome: The key role of central obesity. Metab Synd Relat Disord 7, 447–452.

    Article  CAS  Google Scholar 

  • Fickova M, Hubert P, Crémel G, Leray C (1998). Dietary (n-3) and (n-6) polyunsaturated fatty acids rapidly modify fatty acid composition and insulin effects in rat adipocytes. J Nutr 128, 512–519.

    Article  CAS  PubMed  Google Scholar 

  • Field CJ, Ryan EA, Thomson AB, Clandinin MT (1990). Diet fat composition alters membrane phospholipid composition, insulin binding, and glucose metabolism in adipocytes from control and diabetic animals. J Biol Chem 265, 11143–11150.

    CAS  PubMed  Google Scholar 

  • Fisher FM, McTernan PG, Valsamakis G, Chetty R, Harte AL, Anwar AJ et al. (2002). Differences in adiponectin protein expression: effect of fat depots and type 2 diabetic status. Horm Metab Res 34, 650–654.

    Article  CAS  PubMed  Google Scholar 

  • Flachs P, Rossmeisl M, Bryhn M, Kopecky J (2009). Cellular and molecular effects of n-3 polyunsaturated fatty acids on adipose tissue biology and metabolism. Clin Sci (Lond) 116, 1–16.

    Article  CAS  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957). A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497–509.

    CAS  PubMed  Google Scholar 

  • Friedman JM, Halaas JL (1998). Leptin and the regulation of body weight in mammals. Nature 395, 763–770.

    Article  CAS  PubMed  Google Scholar 

  • Guebre-Egziabher F, Rabasa-Lhoret R, Bonnet F, Bastard JP, Desage M, Skilton MR et al. (2008). Nutritional intervention to reduce the n-6/n-3 fatty acid ratio increases adiponectin concentration and fatty acid oxidation in healthy subjects. Eur J Clin Nutr 62, 1287–1293.

    Article  CAS  PubMed  Google Scholar 

  • Itoh M, Suganami T, Satoh N, Tanimoto-Koyama K, Yuan X, Tanaka M et al. (2007). Increased adiponectin secretion by highly purified eicosapentaenoic acid in rodent models of obesity and human obese subjects. Arterioscler Thromb Vasc Biol 27, 1918–1925.

    Article  CAS  PubMed  Google Scholar 

  • Kamboj SS, Chopra K, Sandhir R (2009). Hyperglycemia-induced alterations in synaptosomal membrane fluidity and activity of membrane bound enzymes: beneficial effect of N-acetylcysteine supplementation. Neuroscience 162, 349–358.

    Article  CAS  PubMed  Google Scholar 

  • Kuypers FA (2007). Membrane lipid alterations in hemoglobinopathies. Hematology Am Soc Hematol Educ Program 68–73.

    Article  Google Scholar 

  • Le Petit-Thévenin J, Nobili O, Boyer J (1988). Decreased acylation of phosphatidylcholine in diabetic rat erythrocytes. Diabetes 37, 142–146.

    Article  PubMed  Google Scholar 

  • Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y et al. (1995). Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1, 1155–1161.

    Article  CAS  PubMed  Google Scholar 

  • Makar TK, Hungund BL, Cook GA, Kashfi K, Cooper AJ (1995). Lipid metabolism and membrane composition are altered in the brains of type II diabetic mice. J Neurochem 64, 2159–2168.

    Article  CAS  PubMed  Google Scholar 

  • Min Y, Ghebremeskel K, Lowy C, Thomas B, Crawford MA (2004). Adverse effect of obesity on red cell membrane arachidonic and docosahexaenoic acids in gestational diabetes. Diabetologia 47, 75–81.

    Article  CAS  PubMed  Google Scholar 

  • Min Y, Nam JH, Ghebremeskel K, Kim A, Crawford M (2006). A distinctive fatty acid profile in circulating lipids of Korean gestational diabetics: a pilot study. Diab Res Clin Pract 73, 178–183.

    Article  CAS  Google Scholar 

  • Nakamura Y, Ueshima H, Okuda N, Higashiyama A, Kita Y, Kadowaki T et al. (2008). Relation of dietary and other lifestyle traits to difference in serum adiponectin concentration of Japanese in Japan and Hawaii: the INTERLIPID Study. Am J Clin Nutr 88, 424–430.

    Article  CAS  PubMed  Google Scholar 

  • Neschen S, Morino K, Rossbacher JC, Pongratz RL, Cline GW, Sono S et al. (2006). Fish oil regulates adiponectin secretion by a peroxisome proliferator-activated receptor-gamma-dependent mechanism in mice. Diabetes 55, 924–928.

    Article  CAS  PubMed  Google Scholar 

  • Nishida M, Funahashi T, Shimomura I (2007). Pathophysiological significance of adiponectin. Med Mole Morphol 40, 55–67.

    Article  CAS  Google Scholar 

  • Pérez-Matute P, Marti A, Martínez JA, Fernández-Otero MP, Stanhope KL, Havel PJ et al. (2005). Eicosapentaenoic fatty acid increases leptin secretion from primary cultured rat adipocytes: role of glucose metabolism. Am J Physiol Regul Integr Comp Physiol 288, R1682–R1688.

    Article  PubMed  Google Scholar 

  • Ramel A, Parra D, Martinéz JA, Kiely M, Thorsdottir I (2009). Effects of seafood consumption and weight loss on fasting leptin and ghrelin concentrations in overweight and obese European young adults. Eur J Nutr 48, 107–114.

    Article  CAS  PubMed  Google Scholar 

  • Roelofsen B, Zwaal RFA (1976). The use of phospholipases in the determination of asymmetric phospholipid distribution in membranes. Meth Membr Biol 7, 147–177.

    Article  CAS  Google Scholar 

  • Rossi AS, Lombardo YB, Lacorte JM, Chicco AG, Rouault C, Slama G et al. (2005). Dietary fish oil positively regulates plasma leptin and adiponectin levels in sucrose-fed, insulin-resistant rats. Am J Physiol Regul Integr Comp Physiol 289, R486–R494.

    Article  CAS  PubMed  Google Scholar 

  • Selenscig D, Rossi A, Chicco A, Lombardo YB (2010). Increased leptin storage with altered leptin secretion from adipocytes of rats with sucrose-induced dyslipidemia and insulin resistance: effect of dietary fish oil. Metabolism 59, 787–795.

    Article  CAS  PubMed  Google Scholar 

  • Spranger J, Kroke A, Möhlig M, Bergmann MM, Ristow M, Boeing H et al. (2003). Adiponectin and protection against type 2 diabetes mellitus. Lancet 361, 226–228.

    Article  CAS  PubMed  Google Scholar 

  • Verkleij AJ, Zwaal RF, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LL (1973). The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy. Biochim Biophys Acta 323, 178–193.

    Article  CAS  PubMed  Google Scholar 

  • WHO (2006). Definition and diagnosis of diabetes mellitus and intermediate hyperglycaemia: Report of a WHO/IDF consultation. WHO Document Production Services: Geneva, Switzerland.

Download references

Acknowledgements

The financial support of the Guy's and St Thomas’ Charity (Endocrine and Diabetic Fund), The Letten Foundation, The Foyle Foundation, The Mother and Child Foundation, and FP6 Marie Curie Actions - Transfer of Knowledge (MTKD-CT-2005-029914) is gratefully acknowledged. We thank all participants and Miss Sonja Tait, Miss Virginie Alexandre and Dr Julia Geppert for their technical assistance.

Author information

Authors and Affiliations

  1. Institute of Brain Chemistry and Human Nutrition, Faculty of Life Science, London Metropolitan University, London, UK

    Y Min & C Lowy

  2. Guy’s, King’s and St Thomas’ Medical and Dental School, St Thomas’ Hospital, London, UK

    C Lowy, S Islam, F S Khan & R Swaminathan

Authors
  1. Y Min
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C Lowy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S Islam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F S Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R Swaminathan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y Min.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Min, Y., Lowy, C., Islam, S. et al. Relationship between red cell membrane fatty acids and adipokines in individuals with varying insulin sensitivity. Eur J Clin Nutr 65, 690–695 (2011). https://doi.org/10.1038/ejcn.2011.19

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2011.19

Keywords

This article is cited by

Search

Advanced search

Quick links