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Lipids

, Volume 40, Issue 7, pp 661–667 | Cite as

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

  • Carla FerreriEmail author
  • Federica Angelini
  • Chryssostomos Chatgilialoglu
  • Sergio Dellonte
  • Viviana Moschese
  • Paolo Rossi
  • Loredana Chini
Articles

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.

Keywords

Atopic Dermatitis Erythrocyte Membrane Trans Fatty Acid Atopic Disease Radical Stress 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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

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References

  1. 1.
    Horrobin, D.F. (2000) Essential Fatty Acid Metabolism and Its Modification in Atopic Eczema, Am. J. Clin. Nutr. 71, 367S-372S.PubMedGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle Scholar
  5. 5.
    Calder, P.C., and Miles, E.A. (2000) Fatty Acids and Atopic Disease, Pediatr. Allergy Immunol. 11 (Suppl. 13), 29–36.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle Scholar
  18. 18.
    Chatgilialoglu, C., and Ferreri, C. (2005) Trans Lipids: The Free Radical Path, Acc. Chem. Res. 38, 441–448.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedGoogle 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.PubMedGoogle 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.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.Google Scholar
  30. 30.
    Baldwin, S.A., and Lienhard, G.E. (1989) Purification and Reconsititution of Glucose Transporter from Human Erythrocytes, Methods Enzymol. 174, 39–45.PubMedCrossRefGoogle 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.PubMedGoogle 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.CrossRefGoogle Scholar
  33. 33.
    Wright, S. (1985) Atopic Dermatitis and Essential Fatty Acids. A Biochemical Basis for Atopy, Acta Derm. Venereol. 114 (suppl.), 143–145.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.PubMedGoogle Scholar
  35. 35.
    Duchén, K., and Björktén, B. (2001) Polyunsaturated n-3 Fatty Acids and the Development of Atopic Disease, Lipids 36, 1033–1042.PubMedCrossRefGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.PubMedCrossRefGoogle 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.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.CrossRefGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle 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.PubMedGoogle 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.PubMedGoogle 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.PubMedCrossRefGoogle Scholar

Copyright information

© AOCS Press 2005

Authors and Affiliations

  • Carla Ferreri
    • 1
    Email author
  • Federica Angelini
    • 2
  • Chryssostomos Chatgilialoglu
    • 1
  • Sergio Dellonte
    • 1
  • Viviana Moschese
    • 2
  • Paolo Rossi
    • 2
  • Loredana Chini
    • 2
  1. 1.Istituto per la Sintesi Organica e la Fotoreattività (ISOF)Consiglio Nazionale delle RicercheBolognaItaly
  2. 2.Dipartimento di Pediatria, Policlinico Tor VergataUniversità di Roma “Tor Vergata”RomaItaly

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