Trans fatty acids and atopic eczema/dermatitis syndrome: The relationship with a free radical cis-trans isomerization of membrane lipids

Abstract

The formation of trans FA residues in membrane phospholipids may be due to a free radical-catalyzed isomerization process occurring to the cis unsaturated FA moieties. Radical stress is well documented in inflammatory processes of atopic diseases, but no data are yet available about a possible association with trans FA detected in these patients. We investigated the presence of trans lipid isomers in the erythrocyte and T-lymphocyte membranes of 26 children affected by atopic eczema/dermatitis syndrome (AEDS). Trans lipid isomers were found in both cell membranes, up to a total content of 2.7 and 4.9% of the FA composition, respectively. By using the geometrical trans lipid library derived from in vitro models of thiyl radical-catalyzed isomerization, oleic and arachidonic acid isomers were detected. The statistical significance was evaluated by comparison with an age-matched control group. These results suggest the role of an endogenous free radical isomerization path occurring to membrane unsaturated lipids, complementary to the dietary contribution, which can be involved in the lipid impairment in AEDS. This study contributes to lipidomic research regarding the double bond structure and the influence of a geometrical change of membrane lipids in physiology and diseases.

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

Abbreviations

AEDS:

atopic eczema/dermatitis syndrome

CD:

cluster of differentiation

DGLA:

dinomo-g-linolenic acid

MUFA:

monounsaturated FA

PBMC:

peripheral blood mononuclear cell

RAST:

RadioAllergoSorbent Test

SCORAD:

skin clinical score

SFA:

saturated FA

TCR:

T-cell receptor

TFA:

trans FA

Th:

T-helper

THP-1:

a human leukemia cell line

References

  1. 1.

    Horrobin, D.F. (2000) Essential Fatty Acid Metabolism and Its Modification in Atopic Eczema, Am. J. Clin. Nutr. 71, 367S-372S.

    PubMed  CAS  Google Scholar 

  2. 2.

    Zeyda, M., Szekeres, A.B., Saemann, M.D., Geyeregger, R., Stockinger, H., Zlabinger, G.J., Waldhausl, W., and Stulnig, T.M. (2003) Suppression of T Cell Signaling by Polyunsaturated Fatty Acids: Selectivity in Inhibition of Mitogen-Activated Protein Kinase and Nuclear Factor Activation, J. Immunol. 170, 6033–6039.

    PubMed  CAS  Google Scholar 

  3. 3.

    Galli, E., Picardo, M., Chini, L., Passi, S., Moschesse, V., Terminali, O., Paone, F., Fraioli, G., and Rossi, P. (1994) Analysis of Polyunsaturated Fatty Acids in Newborn Sera: A Screening Tool for Atopic Disease? Br. J. Dermatol. 130, 752–756.

    PubMed  CAS  Article  Google Scholar 

  4. 4.

    Yu, G., and Bjorksten, B. (1998) Serum Levels of Phospholipid Fatty Acids in Mothers and Their Babies in Relation to Allergic Disease, Eur. J. Pediatr. 157, 298–303.

    PubMed  CAS  Article  Google Scholar 

  5. 5.

    Calder, P.C., and Miles, E.A. (2000) Fatty Acids and Atopic Disease, Pediatr. Allergy Immunol. 11 (Suppl. 13), 29–36.

    PubMed  Article  Google Scholar 

  6. 6.

    Roach, C., Feller, S.E., Ward, J.A., Raza Shaikh, S., Zerouga, M., and Stillwell, W. (2004) Comparison of cis and trans Fatty Acid Containing Phosphatidylcholines on Membrane Properties, Biochemistry 43, 6344–6351.

    PubMed  CAS  Article  Google Scholar 

  7. 7.

    Niu, S.-L., Mitchell, D.C., and Litman, B.J. (2005) Trans Fatty Acid Derived Phospholipids Show Increased Membrane Cholesterol Reduced Receptor Activation as Compared to Their cis Analogs, Biochemistry 44, 4458–4465.

    PubMed  CAS  Article  Google Scholar 

  8. 8.

    Helmkamp, G.M., Jr. (1980) Effects of Phospholipid Fatty Acid Composition and Membrane Fluidity on the Activity of Bovine Brain Phospholipid Exchange Protein, Biochemistry 19, 2050–2056.

    PubMed  CAS  Article  Google Scholar 

  9. 9.

    Kummerow, F.A., Zhou, Q., and Mahfouz, M. (1999) Effect of trans Fatty Acids on Calcium Influx into Human Arterial Endothelial Cells, Am. J. Clin. Nutr. 70, 832–838.

    PubMed  CAS  Google Scholar 

  10. 10.

    Sébédio, J.L., and Christie, W.W., (eds.) (1998) Trans Fatty Acids in Human Nutrition, The Oily Press, Dundee.

    Google Scholar 

  11. 11.

    Larque, E., Zamora, S., and Gil, A. (2001) Dietary trans Fatty Acids in Early Life: A Review, Early Hum. Dev. 65, S31–S41.

    PubMed  CAS  Article  Google Scholar 

  12. 12.

    Wolff, R.I., and Entressangles, B. (1994) Steady-state Fluorescence Polarization Study of Structurally Defined Phospholipids from Livier Mitochondria of Rats Fed Elaidic Acid, Biochim. Biophys. Acta 1211, 198–206.

    PubMed  CAS  Google Scholar 

  13. 13.

    Acar, N., Chardigny, J.M., Darbois, M., Pasquis, B., and Sébédio, J.L. (2003) Modification of the Dopaminergic Neurotransmitters in Striatum, Frontal Cortex and Hippocampus of Rats Fed for 21 Months with trans Isomers of α-Linolenic Acid, Neurosci. Res. 45, 375–382.

    PubMed  CAS  Article  Google Scholar 

  14. 14.

    Sébédio, J.L., Vermunt, S.H.F., Chardigny, J.M., Beaufrere, B., Mensink, R.P., Armstrong, R.A., Christie, W.W., Niemela, J., Henon, G., and Riemersma, R.A. (2000) The Effects of Dietary trans α-Linolenic Acid on Plasma Lipids and Platelet Fatty Acid Composition: The TransLinE Study, Eur. J. Clin. Nutr. 54, 104–113.

    PubMed  Article  Google Scholar 

  15. 15.

    Lemaitre, R.N., King, I.B., Raghunathan, T.E., Pearce, R.M., Weinmann, S., Knopp, R.H., Copass, M.K., Cobb, L.A., and Siscovick, D.S. (2002) Cell Membrane trans-Fatty Acids and the Risk of Primary Cardiac Arrest, Circulation 105, 697–701.

    PubMed  CAS  Article  Google Scholar 

  16. 16.

    Weiland, S.K., von Mutius, E., Husing, A., and Asher, M.I. (1999) Intake of trans Fatty Acids and Prevalence of Childhood Asthma and Allergies in Europe, ISAAC Steering Committee, Lancet 353, 2040–2041.

    PubMed  CAS  Article  Google Scholar 

  17. 17.

    Nagel, G., and Linseisen, J. (2005) Dietary Intake of Fatty Acids, Antioxidants and Selected Food Groups and Asthma in Adults, Eur. J. Clin. Nutr. 59, 8–15.

    PubMed  CAS  Article  Google Scholar 

  18. 18.

    Chatgilialoglu, C., and Ferreri, C. (2005) Trans Lipids: The Free Radical Path, Acc. Chem. Res. 38, 441–448.

    PubMed  CAS  Article  Google Scholar 

  19. 19.

    Ferreri, C., Costantino, C., Perrotta, L., Landi, L., Mulazzani, Q.G., and Chatgilialoglu, C. (2001) Cis-trans Isomerization of Polyunsaturated Fatty Acid Residues in Phospholipids Catalyzed by Thiyl Radicals, J. Am. Chem. Soc. 123, 4459–4468.

    PubMed  CAS  Article  Google Scholar 

  20. 20.

    Ferreri, C., Faraone-Mennella, M.R., Formisano, C., Landi, L., and Chatgilialoglu, C. (2002) Arachidonate Geometrical Isomers Generated by Thiyl Radicals: The Relationship with trans Lipids Detected in Biological Samples, Free Radic. Biol. Med. 33, 1516–1526.

    PubMed  CAS  Article  Google Scholar 

  21. 21.

    Ferreri, C., Samadi, A., Sassatelli, F., Landi, L., and Chatgilialoglu, C. (2004) Regioselective cis-trans Isomerization of Arachidonic Double Bonds by Thiyl Radicals: The Influence of Phospholipid Supramolecular Organization, J. Am. Chem. Soc. 126, 1063–1072.

    PubMed  CAS  Article  Google Scholar 

  22. 22.

    Zghibeh, C.M., Gopal, V.R., Poff, C.D., Falck, J.R., and Balazy, M. (2004) Determination of trans-Arachidonic Acid Isomers in Human Blood Plasma, Anal. Biochem. 332, 137–144.

    PubMed  CAS  Article  Google Scholar 

  23. 23.

    Ferreri, C., Kratzsch, S., Brede, O., Marciniak, B., and Chatgilialoglu, C. (2005) Trans Lipids Formation Induced by Thiols in Human Monocytic Cells, Free Radic. Biol. Med. 38, 1180–1187.

    PubMed  CAS  Article  Google Scholar 

  24. 24.

    Tsukahara, H., Shibata, R., Ohshima, Y., Todoroki, Y., Sato, S., Ohta, N., Hiraoka, M., Yoshida, A., Nishima, S., and Mayumi, M. (2003) Oxidative Stress and Altered Antioxidant Defenses in Children with Acute Exacerbation of Atopic Dermatitis, Life Sci. 72, 2509–2516.

    PubMed  CAS  Article  Google Scholar 

  25. 25.

    Berdeaux, O., Blond, J.P., Bretillon, L., Chardigny, J.M., Mairot, T., Vatele, J.M., Poullain, D., and Sébédio, J.L. (1998) In vitro Desaturation or Elongation of Monotrans Isomers of Linoleic Acid by Rat Liver Microsomes, Mol. Cell. Biochem. 185, 17–25.

    PubMed  CAS  Article  Google Scholar 

  26. 26.

    Rosenthal, M.D., and Doloresco, M.A. (1984) The Effects of trans Fatty Acids on Fatty Acyl Δ5 Desaturation by Human Skin Fibroblast, Lipids 19, 869–874.

    PubMed  CAS  Google Scholar 

  27. 27.

    O’Keefe, S.F., Lagarde, M., Grandgirard, A., and Sébédio, J.L. (1990) Trans n-3 Eicosapentaenoic and Docosahexaenoic Acid Isomers Exhibit Different Inhibitory Effects on Arachidonic Acid Metabolism in Human Platelets Compared to the Respective cis Fatty Acids, J. Lipid Res. 31, 1241–1246.

    PubMed  CAS  Google Scholar 

  28. 28.

    Samadi, A., Andreu, I., Ferreri, C., Dellonte, S., and Chatgilialoglu, C. (2004) Thiyl Radical Catalyzed Isomerization of Oils: An Entry to the trans Lipid Library, J. Am. Oil Chem. Soc. 81, 753–758.

    CAS  Google Scholar 

  29. 29.

    (1993) Severity Scoring of Atopic Dermatitis: The SCORAD Index. Consensus Report of the European Task Force on Atopic Dermatitis, Dermatology 186, 23–31.

  30. 30.

    Baldwin, S.A., and Lienhard, G.E. (1989) Purification and Reconsititution of Glucose Transporter from Human Erythrocytes, Methods Enzymol. 174, 39–45.

    PubMed  CAS  Article  Google Scholar 

  31. 31.

    Bligh, E.G., and Dyer, W.J. (1959) A Rapid Method of Total Lipid Extraction and Purification, Can. J. Biochem. Physiol. 37, 911–917.

    PubMed  CAS  Google Scholar 

  32. 32.

    Krmaer, J.K.G., Fellner, V., Dugan, M.E.R., Sauer, F.D., Mossoba, M.M., and Yurawecz, M.P. (1997) Evaluating Acid and Base Catalysts in the Methylation of Milk and Rumen Fatty Acids with Special Emphasis on Conjugated Dienes and Total trans Fatty Acids, Lipids 32, 1219–1228.

    Article  Google Scholar 

  33. 33.

    Wright, S. (1985) Atopic Dermatitis and Essential Fatty Acids. A Biochemical Basis for Atopy, Acta Derm. Venereol. 114 (suppl.), 143–145.

    CAS  Google Scholar 

  34. 34.

    Oliwiecki, S., Burton, J.L., Elles, K., and Horrobin, D.F. (1991) Levels of Essential and Other Fatty Acids in Plasma and Red Cell Phospholipids from Normal Controls and Patients with Atopic Eczema, Acta Derm. Venereol. 71, 224–228.

    PubMed  CAS  Google Scholar 

  35. 35.

    Duchén, K., and Björktén, B. (2001) Polyunsaturated n-3 Fatty Acids and the Development of Atopic Disease, Lipids 36, 1033–1042.

    PubMed  Article  Google Scholar 

  36. 36.

    Biagi, P.L., Hrelia, S., Celadon, M., Turchetto, E., Masi, M., Ricci, G., Specchia, F., Cannella, M.V., Horrobin, D.F., and Bordoni, A. (1993) Erythrocyte Membrane Fatty Acid Composition in Children with Atopic Dermatitis Compared to Age-Matched Controls, Acta Paediatr. 82, 789–790.

    PubMed  CAS  Google Scholar 

  37. 37.

    Agatha, G., Hafer, R., and Zintl, F. (2001) Fatty Acid Composition of Lymphocyte Membrane Phospholipids in Children with Acute Leukemia, Cancer Lett. 173, 139–144.

    PubMed  CAS  Article  Google Scholar 

  38. 38.

    Paganelli, F., Maixent, J.M., Duran, M.J., Parhizgar, R., Pieroni, G., and Sennoune, S. (2001) Altered Erythrocyte n-3 Fatty Acids in Mediterranean Patients with Coronary Artery Disease, Int. J. Cardiol. 78, 27–32.

    PubMed  CAS  Article  Google Scholar 

  39. 39.

    Barò, L., Hermoso, J.C., Nuñez, M.C., Jimenez-Rios, J.A., and Gil, A. (1998) Abnormalities in Plasma and Red Blood Cell Fatty Acid Profiles of Patients with Colorectal Cancer, Br. J. Cancer 77, 1978–1983.

    PubMed  Google Scholar 

  40. 40.

    Ponnappan, V., Holley, D.H., and Lipschitz, D.A. (1996) Effect of Age on the Fatty Acid Composition of Phospholipids in Human Lymphocytes, Exp. Gerontol. 31, 125–133.

    PubMed  CAS  Article  Google Scholar 

  41. 41.

    Caprari, P., Scuteri, A., Salvati, A.M., Banco, C., Cantafora, A., Masella, R., Modesti, D., Tarzia, A., and Marigliano, V. (1999) Aging and Red Blood Cell Membranes: A Study of Centenarians, Exp. Gerontol. 34, 47–57.

    PubMed  CAS  Article  Google Scholar 

  42. 42.

    Decsi, T., and Koletzko, B. (1994) Fatty Acid Composition of Plasma Lipid Classes in Healthy Subjects from Birth to Young Adulthood, Eur. J. Pediatr. 153, 520–525.

    PubMed  CAS  Article  Google Scholar 

  43. 43.

    Fuchs, J., Zollner, T.M., Kaufmann, R., and Podda, M. (2001) Redox-Modulated Pathways in Inflammatory Skin Diseases, Free Radic. Biol. Med. 30, 337–353.

    PubMed  CAS  Article  Google Scholar 

  44. 44.

    Chatgilialoglu, C., Zambonin, L., Altieri, A., Ferreri, C., Mulazzani, Q.G., and Landi, L. (2002) Geometrical Isomerism of Monounsaturated Fatty Acids. Thiyl Radical Catalysis and Influence of Antioxidant Vitamins, Free Radic. Biol. Med. 33, 1681–1692.

    PubMed  CAS  Article  Google Scholar 

  45. 45.

    Egmond, G.J.N., Pabon, H.J.J., and van Dorp, D.A. (1977) Total Synthesis of Methyl t-5,c-8,c-11,c-14-Eicosatetraenoate and of t-2,c-5,c-8,c-11,c-14-Eicosapentaneoic Acid, Rec. Trav. Chim, Pays-Bas 96, 172–175.

    CAS  Google Scholar 

  46. 46.

    Berdeaux, O., Vatèle, J.-M., Eynard, T., Nour, M., Poullain, D., Noël, J.P., and Sébédio, J.L. (1995) Synthesis of (9Z,12E)-and (9E,12Z)-[1-14C]Linoleic Acid and (5Z,8Z,11Z,14E)-[1-14C]Arachidonic Acid, Chem. Phys. Lipids 78, 71–80.

    CAS  Article  Google Scholar 

  47. 47.

    Berdeaux, O., Chardigny, J.M., Sébédio, J.L., Mairot, T., Poullain, D., Vatèle, J.M., and Noël, J.P. (1996) Effects of a trans Isomer of Arachidonic Acid on Rat Platelet Aggregation and Eicosanoid Production, J. Lipid Res. 37, 2244–2250.

    PubMed  CAS  Google Scholar 

  48. 48.

    Roy, U., Loreau, O., and Balazy, M. (2004) Cytochrome P450/NADPH-Dependent Formation of trans Epoxides from trans-Arachidonic Acids, Bioorg. Med. Chem. Lett. 14, 1019–1022.

    PubMed  CAS  Article  Google Scholar 

  49. 49.

    Marzo, I., Martinez-Lorenzo, M.J., Anel, A., Desportes, P., Alava, M.A., Naval, J., and Piñeiro, A. (1995) Biosynthesis of Unsaturated Fatty Acids in the Main Cell Lineages of Human Leukemia and Lymphoma, Biochim. Biophys. Acta 1257, 140–148.

    PubMed  Google Scholar 

  50. 50.

    Williard, D.E., Nwankwo, J.O., Kaduce, T.L., Harmon, S.D., Irons, M., Moser, H.W., Raymond, G.V., and Spector, A.A. (2001) Identification of a Fatty Acid Δ6-Desaturase Deficiency in Human Skin Fibroblasts, J. Lipid Res. 42, 501–508.

    PubMed  CAS  Google Scholar 

  51. 51.

    Decsi, T., Boehm, G., Ria Tjoonk, H.M., Molnár, S., Dijck-Brouwer, D.A.J., Hadders-Algra, M., Martini, I.A., Muskiet, F.A., and Boersma, E.R. (2002) Trans Isomeric Octadecenoic Acids Are Related Inversely to Arachidonic Acid and DHA and Positively Related to Mead Acid in Umbilical Vessel Wall Lipids, Lipids 37, 954–965.

    Google Scholar 

  52. 52.

    Graham-Brown, R. (2000) Atopic Dermatitis: Unapproved Treatments or Indications, Clin. Dermatol. 18, 153–158.

    PubMed  CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Carla Ferreri.

About this article

Cite this article

Ferreri, C., Angelini, F., Chatgilialoglu, C. et al. Trans fatty acids and atopic eczema/dermatitis syndrome: The relationship with a free radical cis-trans isomerization of membrane lipids. Lipids 40, 661–667 (2005). https://doi.org/10.1007/s11745-005-1428-7

Download citation

Keywords

  • Atopic Dermatitis
  • Erythrocyte Membrane
  • Trans Fatty Acid
  • Atopic Disease
  • Radical Stress