Table of Contents Author Guidelines Submit a Manuscript
Journal of Nutrition and Metabolism
Volume 2016, Article ID 3124960, 10 pages
http://dx.doi.org/10.1155/2016/3124960
Review Article

Role of T-Cell Polarization and Inflammation and Their Modulation by n-3 Fatty Acids in Gestational Diabetes and Macrosomia

1INSERM U866, Université de Bourgogne, 21000 Dijon, France
2Service de Physiologie et Explorations Fonctionnelles, Faculté de Médecine de Sousse, 4000 Sousse, Tunisia
3Laboratoire des Produits Naturels (LAPRONA), Département de Biologie Moléculaire et Cellulaire, Faculté des Sciences, Université Abou Bekr Belkaid, 25000 Tlemcen, Algeria

Received 24 December 2015; Revised 10 April 2016; Accepted 5 May 2016

Academic Editor: Michael B. Zemel

Copyright © 2016 A. Hichami et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. A. Khan, “Role of lipids and fatty acids in macrosomic offspring of diabetic pregnancy,” Cell Biochemistry and Biophysics, vol. 48, no. 2-3, pp. 79–88, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Merzouk, S. Madani, A. Hichami, J. Prost, J. Belleville, and N. A. Khan, “Age-related changes in fatty acids in obese offspring of streptozotocin-induced diabetic rats,” Obesity Research, vol. 10, no. 7, pp. 703–714, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. A. A. Meshari, S. De Silva, and I. Rahman, “Fetal macrosomia—maternal risks and fetal outcome,” International Journal of Gynecology and Obstetrics, vol. 32, no. 3, pp. 215–222, 1990. View at Publisher · View at Google Scholar · View at Scopus
  4. J. M. Miller Jr., H. L. Brown, J. G. Pastorek II, and H. A. Gabert, “Fetal overgrowth: diabetic versus nondiabetic,” Journal of Ultrasound in Medicine, vol. 7, no. 10, pp. 577–579, 1988. View at Google Scholar · View at Scopus
  5. C. Napoli, F. P. D'Armiento, F. P. Mancini et al., “Fatty streak formation occurs in human fetal aortas and is greatly enhanced maternal, hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atheroeclerotic lesions,” Journal of Clinical Investigation, vol. 100, no. 11, pp. 2680–2690, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. R. A. Vogel, M. C. Corretti, and G. D. Plotnick, “Effect of a single high-fat meal on endothelial function in healthy subjects,” American Journal of Cardiology, vol. 79, no. 3, pp. 350–354, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Přibylová and L. Dvořáková, “Long-term prognosis of infants of diabetic mothers: relationship between metabolic disorders in newborns and adult offspring,” Acta Diabetologica, vol. 33, no. 1, pp. 30–34, 1996. View at Publisher · View at Google Scholar · View at Scopus
  8. H. Merzouk, S. Madani, J. Prost, B. Loukidi, M. Meghelli-Bouchenak, and J. Belleville, “Changes in serum lipid and lipoprotein concentrations and compositions at birth and after 1 month of life in macrosomic infants of insulin-dependent diabetic mothers,” European Journal of Pediatrics, vol. 158, no. 9, pp. 750–756, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Merzouk, S. Madani, D. C. Sari, J. Prost, M. Bouchenak, and J. Belleville, “Time course of changes in serum glucose, insulin, lipids and tissue lipase activities in macrosomic offspring of rats with streptozotocin-induced diabetes,” Clinical Science, vol. 98, no. 1, pp. 21–30, 2000. View at Google Scholar · View at Scopus
  10. A. L. Fowden, “The role of insulin in prenatal growth,” Journal of Developmental Physiology, vol. 12, no. 4, pp. 173–182, 1989. View at Google Scholar · View at Scopus
  11. F. Foufelle and P. Ferré, “New perspectives in the regulation of hepatic glycolytic and lipogenic genes by insulin and glucose: a role for the transcription factor sterol regulatory element binding protein-1c,” Biochemical Journal, vol. 366, no. 2, pp. 377–391, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. D. J. P. Barker, “Fetal origins of coronary heart disease,” British Medical Journal, vol. 311, no. 6998, pp. 171–174, 1995. View at Publisher · View at Google Scholar · View at Scopus
  13. J. M. Friedman and J. L. Halaas, “Leptin and the regulation of body weight in mammals,” Nature, vol. 395, no. 6704, pp. 763–770, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. S. G. Bouret, S. J. Draper, and R. B. Simerly, “Trophic action of leptin on hypothalamic neurons that regulate feeding,” Science, vol. 304, no. 5667, pp. 108–110, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Yura, H. Itoh, N. Sagawa et al., “Neonatal exposure to leptin augments diet-induced obesity in leptin-deficient ob/ob mice,” Obesity, vol. 16, no. 6, pp. 1289–1295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Maffei, L. Volpe, G. Di Cianni et al., “Plasma leptin levels in newborns from normal and diabetic mothers,” Hormone and Metabolic Research, vol. 30, no. 9, pp. 575–580, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. S. H. Zeisel, “Dietary choline deficiency causes DNA strand breaks and alters epigenetic marks on DNA and histones,” Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, vol. 733, no. 1-2, pp. 34–38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. J. A. Joles, “Crossing borders: linking environmental and genetic developmental factors,” Microcirculation, vol. 18, no. 4, pp. 298–303, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. O. Grissa, A. Yessoufou, I. Mrisak et al., “Growth factor concentrations and their placental mRNA expression are modulated in gestational diabetes mellitus: possible interactions with macrosomia,” BMC Pregnancy and Childbirth, vol. 10, article 7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Giordano, “Immunobiology of normal and diabetic pregnancy,” Immunology Today, vol. 11, no. 9, pp. 301–303, 1990. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Lapolla, M. G. Dalfrà, M. Sanzari et al., “Lymphocyte subsets and cytokines in women with gestational diabetes mellitus and their newborn,” Cytokine, vol. 31, no. 4, pp. 280–287, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Murgia, M. Orrù, E. Portoghese et al., “Autoimmunity in gestational diabetes mellitus in Sardinia: a preliminary case-control report,” Reproductive Biology and Endocrinology, vol. 6, article 24, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. J. H. Warram, B. C. Martin, and A. S. Krolewski, “Risk of IDDM in children of diabetic mothers decreases with increasing maternal age at pregnancy,” Diabetes, vol. 40, no. 12, pp. 1679–1684, 1991. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Koczwara, E. Bonifacio, and A.-G. Ziegler, “Transmission of maternal islet antibodies and risk of autoimmune diabetes in offspring of mothers with type 1 diabetes,” Diabetes, vol. 53, no. 1, pp. 1–4, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. U. Di Mario, F. Dotta, P. Gargiulo et al., “Immunology in diabetic pregnancy: activated T cells in diabetic mothers and neonates,” Diabetologia, vol. 30, no. 2, pp. 66–71, 1987. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Badr, S. Alwasel, H. Ebaid, M. Mohany, and I. Alhazza, “Perinatal supplementation with thymoquinone improves diabetic complications and T cell immune responses in rat offspring,” Cellular Immunology, vol. 267, no. 2, pp. 133–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Guermouche, A. Yessoufou, N. Soulimane et al., “n-3 fatty acids modulate T-cell calcium signaling in obese macrosomic rats,” Obesity Research, vol. 12, no. 11, pp. 1744–1753, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. U. Roll, J. Scheeser, E. Standl, and A. G. Ziegler, “Alerations of lymphocyte subsets in children of diabetic mothers,” Diabetologia, vol. 37, no. 11, pp. 1132–1141, 1994. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Lapolla, M. C. Sanzari, F. Zancanaro et al., “A study on lymphocyte subpopulation in diabetic mothers at delivery and in their newborn,” Diabetes, Nutrition and Metabolism—Clinical and Experimental, vol. 12, no. 6, pp. 394–399, 1999. View at Google Scholar · View at Scopus
  30. J. Rengarajan, S. J. Szabo, and L. H. Glimcher, “Transcriptional regulation of Th1/Th2 polarization,” Immunology Today, vol. 21, no. 10, pp. 479–483, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. R. S. Liblau, S. M. Singer, and H. O. McDevitt, “Th1 and Th2 CD4+ T cells in the pathogenesis of organ-specific autoimmune diseases,” Immunology Today, vol. 16, no. 1, pp. 34–38, 1995. View at Publisher · View at Google Scholar · View at Scopus
  32. I. Mrizak, O. Grissa, B. Henault et al., “Placental infiltration of inflammatory markers in gestational diabetic women,” General Physiology and Biophysics, vol. 33, no. 2, pp. 169–176, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. N. A. Khan, A. Yessoufou, M. Kim, and A. Hichami, “N-3 fatty acids modulate Th1 and Th2 dichotomy in diabetic pregnancy and macrosomia,” Journal of Autoimmunity, vol. 26, no. 4, pp. 268–277, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Raghupathy, “Pregnancy: success and failure within the Th1/Th2/Th3 paradigm,” Seminars in Immunology, vol. 13, no. 4, pp. 219–227, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Makhseed, R. Raghupathy, F. Azizieh, A. Omu, E. Al-Shamali, and L. Ashkanani, “Th1 and Th2 cytokine profiles in recurrent aborters with successful pregnancy and with subsequent abortions,” Human Reproduction, vol. 16, no. 10, pp. 2219–2226, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Reinhard, A. Noll, H. Schlebusch, P. Mallmann, and A. V. Ruecker, “Shifts in the TH1/TH2 balance during human pregnancy correlate with apoptotic changes,” Biochemical and Biophysical Research Communications, vol. 245, no. 3, pp. 933–938, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. N. A. Khan, A. Khan, H. F. J. Savelkoul, and R. Benner, “Inhibition of diabetes in NOD mice by human pregnancy factor,” Human Immunology, vol. 62, no. 12, pp. 1315–1323, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. N. A. Soulimane-Mokhtari, B. Guermouche, A. Yessoufou et al., “Modulation of lipid metabolism by n-3 polyunsaturated fatty acids in gestational diabetic rats and their macrosomic offspring,” Clinical Science, vol. 109, no. 3, pp. 287–295, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. J.-M. Atègbo, O. Grissa, A. Yessoufou et al., “Modulation of adipokines and cytokines in gestational diabetes and macrosomia,” The Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 10, pp. 4137–4143, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Sasaki, M. Sakai, S. Miyazaki, S. Higuma, A. Shiozaki, and S. Saito, “Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases,” Molecular Human Reproduction, vol. 10, no. 5, pp. 347–353, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Sakaguchi, “Naturally arising Foxp3-expressing CD25+ CD4+ regulatory T cells in immunological tolerance to self and non-self,” Nature Immunology, vol. 6, no. 4, pp. 345–352, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Matrougui, A. E. Zakaria, M. Kassan et al., “Natural regulatory T cells control coronary arteriolar endothelial dysfunction in hypertensive mice,” The American Journal of Pathology, vol. 178, no. 1, pp. 434–441, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Thuere, M. L. Zenclussen, A. Schumacher et al., “Kinetics of regulatory T cells during murine pregnancy,” American Journal of Reproductive Immunology, vol. 58, no. 6, pp. 514–523, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. V. R. Aluvihare, M. Kallikourdis, and A. G. Betz, “Regulatory T cells mediate maternal tolerance to the fetus,” Nature Immunology, vol. 5, no. 3, pp. 266–271, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. M. J. Jasper, K. P. Tremellen, and S. A. Robertson, “Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue,” Molecular Human Reproduction, vol. 12, no. 5, pp. 301–308, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. F. F. Mahmoud, D. D. Haines, H. T. Abul, A. E. Omu, and M. B. Abu-donia, “Butyrylcholinesterase activity in gestational diabetes: correlation with lymphocyte subpopulations in peripheral blood,” American Journal of Reproductive Immunology, vol. 56, no. 3, pp. 185–192, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Mahmoud, H. Abul, A. Omu, and D. Haines, “Lymphocyte sub-populations in gestational diabetes,” American Journal of Reproductive Immunology, vol. 53, no. 1, pp. 21–29, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. B. C. Holm, J. Svensson, C. Åkesson et al., “Evidence for immunological priming and increased frequency of CD4+ CD25+ cord blood T cells in children born to mothers with type 1 diabetes,” Clinical and Experimental Immunology, vol. 146, no. 3, pp. 493–502, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. J. W. Putney Jr., “Type 3 inositol 1,4,5-trisphosphate receptor and capacitative calcium entry,” Cell Calcium, vol. 21, no. 3, pp. 257–261, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Schober, D. Radnai, J. Spratte et al., “The role of regulatory T cell (Treg) subsets in gestational diabetes mellitus,” Clinical and Experimental Immunology, vol. 177, no. 1, pp. 76–85, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Cipolletta, D. Kolodin, C. Benoist, and D. Mathis, “Tissular tregs: a unique population of adipose-tissue-resident Foxp3+CD4+ T cells that impacts organismal metabolism,” Seminars in Immunology, vol. 23, no. 6, pp. 431–437, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Feuerer, L. Herrero, D. Cipolletta et al., “Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters,” Nature Medicine, vol. 15, no. 8, pp. 930–939, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. S. C. Chow and M. Jondal, “Ca2+ entry in T cells is activated by emptying the inositol 1,4,5-trisphosphate sensitive Ca2+ pool,” Cell Calcium, vol. 11, no. 10, pp. 641–646, 1990. View at Publisher · View at Google Scholar · View at Scopus
  54. P. Dandona, A. Aljada, and A. Bandyopadhyay, “Inflammation: the link between insulin resistance, obesity and diabetes,” Trends in Immunology, vol. 25, no. 1, pp. 4–7, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. B. J. Rollins, “Monocyte chemoattractant protein 1: a potential regulator of monocyte recruitment in inflammatory disease,” Molecular Medicine Today, vol. 2, no. 5, pp. 198–204, 1996. View at Publisher · View at Google Scholar · View at Scopus
  56. K. Klein, M. Satler, M. Elhenicky et al., “Circulating levels of MCP-1 are increased in women with gestational diabetes,” Prenatal Diagnosis, vol. 28, no. 9, pp. 845–851, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. E. M. Sternberg, G. P. Chrousos, R. L. Wilder, and P. W. Gold, “The stress response and the regulation of inflammatory disease,” Annals of Internal Medicine, vol. 117, no. 10, pp. 854–866, 1992. View at Publisher · View at Google Scholar
  58. K. Esposito, F. Nappo, R. Marfella et al., “Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress,” Circulation, vol. 106, no. 16, pp. 2067–2072, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Yu, Y.-M. Xue, C.-Z. Li et al., “Association of serum interleukin-6 and high-sensitivity C-reactive protein levels with insulin resistance in gestational diabetes mellitus,” Nan Fang Yi Ke Da Xue Xue Bao, vol. 27, no. 6, pp. 799–801, 2007. View at Google Scholar · View at Scopus
  60. T. K. Hansen, S. Thiel, S. T. Knudsen et al., “Elevated levels of mannan-binding lectin in patients with type 1 diabetes,” The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 10, pp. 4857–4861, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Takebayashi, Y. Aso, and T. Inukai, “Initiation of insulin therapy reduces serum concentrations of high-sensitivity C-reactive protein in patients with type 2 diabetes,” Metabolism: Clinical and Experimental, vol. 53, no. 6, pp. 693–699, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. J. H. Kim, R. A. Bachmann, and J. Chen, “Interleukin-6 and insulin resistance,” Vitamins & Hormones, vol. 80, pp. 613–633, 2009. View at Google Scholar
  63. M. Kuzmicki, B. Telejko, J. Szamatowicz et al., “High resistin and interleukin-6 levels are associated with gestational diabetes mellitus,” Gynecological Endocrinology, vol. 25, no. 4, pp. 258–263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. G. S. Hotamisligil, D. L. Murray, L. N. Choy, and B. M. Spiegelman, “Tumor necrosis factor α inhibits signaling from the insulin receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 11, pp. 4854–4858, 1994. View at Publisher · View at Google Scholar · View at Scopus
  65. M. E. E. Shams, M. M. H. Al-Gayyar, and E. A. M. E. Barakat, “Type 2 diabetes mellitus-induced hyperglycemia in patients with NAFLD and normal LFTs: relationship to lipid profile, oxidative stress and pro-inflammatory cytokines,” Scientia Pharmaceutica, vol. 79, no. 3, pp. 623–634, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. F. Lago, C. Dieguez, J. Gómez-Reino, and O. Gualillo, “Adipokines as emerging mediators of immune response and inflammation,” Nature Clinical Practice Rheumatology, vol. 3, no. 12, pp. 716–724, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. P. Dandona, A. Aljada, P. Mohanty et al., “Insulin inhibits intranuclear nuclear factor κB and stimulates IκB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect?” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 7, pp. 3257–3265, 2001. View at Publisher · View at Google Scholar · View at Scopus
  68. B. Mattioli, E. Straface, M. G. Quaranta, L. Giordani, and M. Viora, “Leptin promotes differentiation and survival of human dendritic cells and licenses them for Th1 priming,” The Journal of Immunology, vol. 174, no. 11, pp. 6820–6824, 2005. View at Publisher · View at Google Scholar
  69. J. J. Díez and P. Iglesias, “The role of the novel adipocyte-derived hormone adiponectin in human disease,” European Journal of Endocrinology, vol. 148, no. 3, pp. 293–300, 2003. View at Publisher · View at Google Scholar · View at Scopus
  70. S. W. Coppack, “Pro-inflammatory cytokines and adipose tissue,” Proceedings of the Nutrition Society, vol. 60, no. 3, pp. 349–356, 2001. View at Google Scholar · View at Scopus
  71. A. Kautzky-Willer, G. Pacini, A. Tura et al., “Increased plasma leptin in gestational diabetes,” Diabetologia, vol. 44, no. 2, pp. 164–172, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. D. Simmons and B. H. Breier, “Fetal overnutrition in polynesian pregnancies and in gestational diabetes may lead to dysregulation of the adipoinsular axis in offspring,” Diabetes Care, vol. 25, no. 9, pp. 1539–1544, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Festa, N. Shnawa, W. Krugluger, P. Hopmeier, G. Schernthaner, and S. M. Haffner, “Relative hypoleptinaemia in women with mild gestational diabetes mellitus,” Diabetic Medicine, vol. 16, no. 8, pp. 656–662, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Loukovaara, P. Leinonen, K. Teramo, H. Alfthan, U.-H. Stenman, and S. Andersson, “Fetal hypoxia is associated with elevated cord serum C-reactive protein levels in diabetic pregnancies,” Biology of the Neonate, vol. 85, no. 4, pp. 237–242, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. E. Soyland, M. S. Nenseter, L. Braathen, and C. A. Drevon, “Very long chain n-3 and n-6 polyunsaturated fatty acids inhibit proliferation of human T-lymphocytes in vitro,” European Journal of Clinical Investigation, vol. 23, no. 2, pp. 112–121, 1993. View at Publisher · View at Google Scholar · View at Scopus
  76. F. A. Wallace, E. A. Miles, C. Evans, T. E. Stock, P. Yaqoob, and P. C. Calder, “Dietary fatty acids influence the production of Th1- but not Th2-type cytokines,” Journal of Leukocyte Biology, vol. 69, no. 3, pp. 449–457, 2001. View at Google Scholar · View at Scopus
  77. Y. T. Konttinen, V. Bergroth, E. Kinnunen, D. Nordström, and T. Kouri, “Activated T lymphocytes in patients with multiple sclerosis in clinical remission,” Journal of the Neurological Sciences, vol. 81, no. 2-3, pp. 133–139, 1987. View at Publisher · View at Google Scholar · View at Scopus
  78. J. N. W. N. Barker, “The pathophysiology of psoriasis,” The Lancet, vol. 338, no. 8761, pp. 227–230, 1991. View at Publisher · View at Google Scholar · View at Scopus
  79. J. E. Merrill, C. Mohlstrom, C. Uittenbogaart, V. Kermaniarab, G. W. Ellison, and L. W. Myers, “Response to and production of interleukin 2 by peripheral blood and cerebrospinal fluid lymphocytes of patients with multiple sclerosis,” The Journal of Immunology, vol. 133, no. 4, pp. 1931–1937, 1984. View at Google Scholar · View at Scopus
  80. R. E. Wolf and W. G. Brelsford, “Soluble interleukin-2 receptors in systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 31, no. 6, pp. 729–735, 1988. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Bellenger, S. Bellenger, A. Bataille et al., “High pancreatic n-3 fatty acids prevent STZ-induced diabetes in fat-1 mice: inflammatory pathway inhibition,” Diabetes, vol. 60, no. 4, pp. 1090–1099, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. T. A. Babcock, W. S. Helton, D. Hong, and N. J. Espat, “Omega-3 fatty acid lipid emulsion reduces LPS-stimulated macrophage TNF-α production,” Surgical Infections, vol. 3, no. 2, pp. 145–149, 2002. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Denys, A. Hichami, and N. A. Khan, “Eicosapentaenoic acid and docosahexaenoic acid modulate MAP kinase enzyme activity in human T-cells,” Molecular and Cellular Biochemistry, vol. 232, no. 1-2, pp. 143–148, 2002. View at Publisher · View at Google Scholar · View at Scopus
  84. P. C. Calder, J. A. Bond, S. J. Bevan, S. V. Hunt, and E. A. Newsholme, “Effect of fatty acids on the proliferation of concanavalin a-stimulated rat lymph node lymphocytes,” International Journal of Biochemistry, vol. 23, no. 5-6, pp. 579–588, 1991. View at Publisher · View at Google Scholar · View at Scopus
  85. W. M. Tsang, C. Weyman, and A. D. Smith, “Effect of fatty acid mixtures on phytohaemagglutinin-stimulated lymphocytes of different species,” Biochemical Society Transactions, vol. 5, no. 1, pp. 153–154, 1977. View at Publisher · View at Google Scholar · View at Scopus
  86. P. C. Calder, S. J. Bevan, and E. A. Newsholme, “The inhibition of T-lymphocyte proliferation by fatty acids is via an eicosanoid-independent mechanism,” Immunology, vol. 75, no. 1, pp. 108–115, 1992. View at Google Scholar · View at Scopus
  87. A. Yessoufou, A. Plé, K. Moutairou, A. Hichami, and N. A. Khan, “Docosahexaenoic acid reduces suppressive and migratory functions of CD4+CD25+ regulatory T-cells,” Journal of Lipid Research, vol. 50, no. 12, pp. 2377–2388, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. B. Li, A. Samanta, X. Song et al., “FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 11, pp. 4571–4576, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Kipnis, M. Cardon, H. Avidan et al., “Dopamine, through the extracellular signal-regulated kinase pathway, downregulates CD4+CD25+ regulatory T-cell activity: implications for neurodegeneration,” The Journal of Neuroscience, vol. 24, no. 27, pp. 6133–6143, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. L. Li, W. R. Godfrey, S. B. Porter et al., “CD4+CD25+ regulatory T-cell lines from human cord blood have functional and molecular properties of T-cell anergy,” Blood, vol. 106, no. 9, pp. 3068–3073, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. C. J. Sherr, “Cancer cell cycles,” Science, vol. 274, no. 5293, pp. 1672–1677, 1996. View at Publisher · View at Google Scholar · View at Scopus
  92. C. Triboulot, A. Hichami, A. Denys, and N. A. Khan, “Dietary (n-3) polyunsaturated fatty acids exert antihypertensive effects by modulating calcium signaling in T cells of rats,” Journal of Nutrition, vol. 131, no. 9, pp. 2364–2369, 2001. View at Google Scholar · View at Scopus
  93. N. A. Khan and A. Hichami, “Role of n-3 polyunsaturated fatty acids in T-cell signalling,” in Recent Advances in Research in Lipids, vol. 6, pp. 65–78, Transworld Publications, 2002. View at Google Scholar
  94. S. Madani, A. Hichami, A. Legrand, J. Belleville, and N. A. Khan, “Implication of acyl chain of diacylglycerols in activation of different isoforms of protein kinase C,” The FASEB Journal, vol. 15, no. 14, pp. 2595–2601, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. A. Hichami, C. Morin, E. Rousseau, and N. A. Khan, “Diacylglycerol-containing docosahexaenoic acid in acyl chain modulates airway smooth muscle tone,” American Journal of Respiratory Cell and Molecular Biology, vol. 33, no. 4, pp. 378–386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Madani, A. Hichami, M. Charkaoui-Malki, and N. A. Khan, “Diacylglycerols containing omega 3 and omega 6 Fatty acids bind to RasGRP and modulate MAP kinase activation,” Journal of Biological Chemistry, vol. 279, no. 2, pp. 1176–1183, 2004. View at Publisher · View at Google Scholar · View at Scopus
  97. USDA D, Dietary Guidelines Advisory Committee Report 2005, http://health.gov/dietaryguidelines/dga2005/report/.
  98. J. Who and F. E. Consultation, “Diet, nutrition and the prevention of chronic diseases,” Technical Report Series 916, World Health Organization, Geneva, Switzerland, 2003. View at Google Scholar
  99. M. A. Leslie, D. J. A. Cohen, D. M. Liddle, L. E. Robinson, and D. W. L. Ma, “A review of the effect of omega-3 polyunsaturated fatty acids on blood triacylglycerol levels in normolipidemic and borderline hyperlipidemic individuals,” Lipids in Health and Disease, vol. 14, no. 1, article 53, 2015. View at Publisher · View at Google Scholar · View at Scopus