The Protective and Recovery Effects of Fish Oil Supplementation on Cedar Pollen-Induced Allergic Reactions in Mice

Akiko Hirao, Naoki Furutani, Hiroki Nagahama, Misa Itokawa, Shigenobu Shibata

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DOI: 10.4236/fns.2012.31008                

Abstract

Obesity is associated with the production of pro-inflammatory cytokines and therefore can lead to worsening of allergic reactions. Thus, there is cross-talk between obesity and allergic reactions. In this study, we investigated whether the anti-obesity action of fish oil supplementation is involved in the anti-allergic action also induced by fish oil. We observed attenuation of cedar pollen-induced IgE serum increases in two experimental protocols: 15% fish oil supplementation for 8 weeks, which attenuated body weight increases compared with 15% soybean supplementation, and 4% fish oil supplementation for 2 weeks, which did not affect body weight increases compared with 4% soybean or 4% lard supplementation. The former but not the latter protocol attenuated sneezing after pollen challenge. Gene expression of TNF-α and IL-13, a Th2 cytokine, was moderately reduced in the trachea and nasal mucosa in mice fed fish oil supple- ments. In a third protocol, fish oil was administered for up to 15 weeks after a cedar pollen sensitization and challenge-induced increase in IgE levels. These levels decreased following fish oil supplementation but were almost unaffected by soybean oil supplementation. Surprisingly, the IL-13 gene expression level in the nasal mucosa and trachea was higher in the fish oil group than in the soybean oil group. These results suggest that fish oil supplementation before, during, or after antigen sensitization and challenge in mice helped to reduce cedar pollen-induced allergic reactions in- dependent of its anti-obesity action. Fish oil supplementation can also exhibit pro- or anti-inflammatory action against IL-13 expression depending on the experimental protocol.

Keywords

Cytokine; Fish Oil; IgE; Obesity; Pollen Allergy

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	H. Y. Xu, Glenn T. Barnes, Q. Yang, G. Tan, D. S. Yang, C. J. Chou, J. Sole, A. Nichols, J. S. Ross, L. A. Tartaglia and H. Chen, “Chronic Inflammation in Fat Plays a Crucial Role in the Development of Obesi Obesity-Related Insulin Resistance,” Journal of Clinical Investigationt, Vol. 112, No. 12, 2003, pp. 1821-1830. doi:10.1172/JCI19451
[2]	S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel and A. W. Ferrante Jr., “Obesity is Associated with Macrophage Accumulation in Adipose Tissue,” Journal of Clinical Investigationt, Vol. 112, No. 12, 2003, pp. 1796-1808. doi:10.1172/JCI200319246
[3]	P. Peraldi, G. S. Hotamisligil, W. A. Buurman, M. F. White and B. M. Spiegelman, “Tumor Necrosis Factor (TNF)-Alpha Inhibits Insulin Signaling through Stimulation of the p55 TNF Receptor and Activation of Sphingomyelinase,” The Journal of Biological Chemistry, Vol. 271, No. 22, 1996, pp. 13018-13022.doi:10.1074/jbc.271.22.13018
[4]	J. Ruzickova, M. Rossmeisl, T.Prazak, P. Flachs, J. Sponarova, M. Vecka, E. Tvrzicka, M. Bryhn and J. Kopecky, “Omega-3 PUFA of Marine Origin Limit Diet-Induced Obesity in Mice by Reducing Cellularity of Adipose Tissue,” Lipids, Vol. 39, No. 12, 2004, pp. 1177-1185. doi:10.1007/s11745-004-1345-9
[5]	L. M. Browning, “n-3 Polyunsaturated Fatty Acids, Inflammation and Obesity-Related Disease,” Proceedings of the Nutrition Society, Vol. 62, No. 2, 2003, pp. 447-453. doi:10.1079/PNS2003252
[6]	S. Mihrshahi, J. K. Peat, K. Webb, W. Oddy, G. B. Marks and C. M. Mellis, “Effect of Omega-3 Fatty Acid Concentrations in Plasma on Symptoms of Asthma at 18 Months of Age,” Pediatric Allergy and Immunology, Vol. 15, No. 6, 2004, pp. 517-522. doi:10.1111/j.1399-3038.2004.00187.x
[7]	K. F. Chung, “Evaluation of Selective Prostaglandin E2 (PGE2) Receptor Agonists as Therapeutic Agents for the Treatment of Asthma,” Science’s STKE, Vol. 2005, No. 303, 2005, pp. pe47. doi:10.1126/stke.3032005pe47
[8]	T. D. Mickleborough and K. W. Rundell, “Dietary Polyunsaturated Fatty Acids in Asthma- and Exerciseinduced Bronchoconstriction,” European Journal of Clinical Nu- trition, Vol. 59, No. 12, 2005, pp. 1335-1346. doi:10.1038/sj.ejcn.1602250
[9]	S. L. Prescott and P. C. Calder, “n-3 Polyunsaturated Fatty Acids and Allergic Disease,” Current Opinion in Clinical Nutrition and Metabolic Care, Vol. 7, No. 2, 2004, pp. 123-129.
[10]	J. K. Peat, S. Mihrshahi, A. S. Kemp, G. B. Marks, E. R. Tovey, K. Webb, C. M. Mellis and S. R. Leeder, “Three-Year Outcomes of Dietary Fatty Acid Modification and House Dust Mite Reduction in the Childhood Asthma Prevention Study,” The Journal of Allergy and Clinical Immunology, Vol. 114, No.4, 2004, pp. 807-813. doi:10.1016/j.jaci.2004.06.057
[11]	T. D. Mickleborough, A. A. Ionescu and K. W. Rundell, “Omega-3 Fatty Acids and Airway Hyperresponsiveness in Asthma,” The Journal of Alternative and Complementary Medicine, Vol. 10, No. 6, 2004, pp. 1067-1075. doi:10.1089/acm.2004.10.1067
[12]	G. Devereux and Anthony Seaton, “Diet as a Risk Factor for Atopy and Asthma,” The Journal of Allergy and Clinical Immunology, Vol. 115, No. 6, 2005, pp. 1109-1117. doi:10.1016/j.jaci.2004.12.1139
[13]	K. W. Wong, “Clinical Efficacy of n-3 Fatty acid Supplementation in Patients with Asthma,” Journal of the American Dietetic Association, Vol. 105, No.1, 2005, pp. 98-105. doi:10.1016/j.jada.2004.10.009
[14]	C. Almqvist, F. Garden, W. Xuan, S. Mihrshahi, S. R. Leeder, W. Oddy, K. Webb and G. B. Marks, “Omega-3 and Omega-6 Fatty Acid Exposure from Early Life Does Not Affect Atopy and Asthma at age 5 Years,” The Journal of allergy and clinical immunology, Vol. 119, No, 6, 2007, pp. 1438-1444. doi:10.1016/j.jaci.2007.01.046
[15]	H. R. Chang, D. Arsenijevic, J. C. Pechère, P. F. Piguet, N. Mensi, L. Girardier and A.G. Dulloo, “Dietary Supplementation with Fish Oil Enhances in Vivo Synthesis of Tumor Necrosis Factor,” Immunology Letters, Vol. 34, No. 1, 1992, pp. 13-17. doi:10.1016/0165-2478(92)90021-F
[16]	P. S. Tappia, W. J. Man and R. F. Grimble, “Influence of Unsaturated Fatty Acids on the Production of Tumor Necrosis Factor and Interleukin-6 by Rat Peritoneal Macrophages,” Molecular and Cellular Biochemistry, Vol. 143, No. 2, 1995, pp. 89-98. doi:10.1007/BF01816941
[17]	D. H. Petursdottir, I. Olafsdottir and I. Hardardottir, “Necrosis Factor Secretion but Decreases Interleukin-10 Secretion by Murine Peritoneal Macrophages,” The Journal of Nutrition, Vol. 132, No. 12, 2002, pp. 3740-3743.
[18]	A. Pupe, R. Moison, P. De Haes, G. B. van Henegouwen, Lesley Rhodes, H. Degreef and M. Garmyn, “Eicosapentaenoic Acid, a n-3 Polyunsaturated Fatty Acid Differentially Modulates TNF-α, IL-1α, IL-6 and PGE2 Expression in UVB-Irradiated Human Keratinocytes,” The Journal of Investigative Dermatology, Vol. 118, No. 4, 2002, pp. 692-698. doi:10.1046/j.1523-1747.2002.01615.x
[19]	M. D. Barber, K. C. H. Fearon and J. A. Ross, “Eicosapentaenoic Acid Modulates the Immune Response but Has No Effect on a Mimic of Antigen-Specific Responses,” Ntrition, Vol. 21, No. 5, 2005, pp. 588-593. doi:10.1016/j.nut.2004.09.017
[20]	W. C. Chang, C. H. Chen, W. T. K. Cheng and S. T. Ding, “The Effect of Dietary Docosahexaenoic Acid Enrichment on the Expression of Porcine Hepatic Genes,” Asian-Australasian Journal of Animal Sciences, Vol. 20, No. 5, 2007, pp. 768-774.
[21]	C. H. Chen, P. H. Wang, B. H. Liu, H. H. Hsu, H. J. Mersmann and S. T. Ding, “Serum Amyloid A Protein Regulates the Expression of Porcine Genes Related to Lipid Metabolism,” The Journal of Nutrition, Vol. 138, No. 4, 2008, pp. 674-679.
[22]	Y. C. Wang, W. H. Kuo, C. Y. Chen, H. Y. Lin, H. T. Wu, B. H. Liu, C. H. Chen, H. J. Mersmann, K. J. Chang and S. T. Ding, “Docosahexaenoic Acid Regulates Serum Amyloid A Protein to Promote Lipolysis through down Regulation of Perilipin,” The Journal of Nutritional Biochemistry, Vol. 21, No. 21, 2010, pp. 317-324. doi:10.1016/j.jnutbio.2009.01.004
[23]	P. A. Baeuerle and T. Henkel, “Function and Activation of NF-Kappa B in the Immune System,” Annual review of immunology, Vol. 12, No. 1, 1994, pp. 141-179. doi:10.1146/annurev.iy.12.040194.001041
[24]	Y. Zhao, S.Joshi-Barve, S.Barve and L. H. Chen, “Eicosapentaenoic Acid Prevents LPS Induced TNF-alpha Expression by Preventing NF-kappaB Activation,” Journal of the American College of Nutrition, Vol. 23, No. 1, 2004, pp. 71-78.
[25]	S. M. Weldon, A. C. Mullen, C. E. Loscher, L. A. Hurley and H. M. Roche, “Docosahexaenoic Acid Induces an Anti-Inflammatory Profile in Lipopolysaccharide-Stimulated Human THP-1 Macrophages More Effectively than Eicosapentaenoic Acid,” The Journal of Nutritional Biochemistry, Vol. 18, No. 4, 2007, pp. 250-258. doi:10.1016/j.jnutbio.2006.04.003
[26]	R. Kitz, M. A. Rose, R. Schubert, C. Beermann, A. Kaufmann, H. J. B?hles, J. Schulze and S. Zielen, “Omega-3 Polyunsaturated Fatty Acids and Bronchial Inflammation in Grass Pollen Allergy after Allergen Challenge,” Res- piratory medicine, Vol. 104, No. 12, 2010, pp. 1793-1798. doi:10.1016/j.rmed.2010.06.019
[27]	M. W. Wu, L. J. Xian, X. M. Li, I. Pasquale and L. Francis, “Circadian Expression of Dihydropyrimidine Dehydrogenase, Thymidylate Synthase, c-myc and p53 mRNA in Mouse Livertissue,” Ai Zheng, Vol. 23, No. 3, 2004, pp. 235-242.
[28]	A. Hirao, H. Nagahama, T. Tsuboi, M. Hirao, Y. Tahara and S. Shibata, “Combination of Starvation Interval and Food Volume Determines the Phase of Liver Circadian Rhythm in Per2::Luc Knock-In Mice under Two Meals Per Day Feeding,” American Journal of Physiology. Gastrointestinal and Liver Physiology, Vol. 299, No. 5, 2010, pp. G1045-G1053. doi:10.1152/ajpgi.00330.2010
[29]	W. S. Harris, “Fish Oils and Plasma Lipid and Lipoprotein Metabolism in Humans: A Critical Review,” The Journal of Lipid Research, Vol. 30, No. 6, 1989, pp. 785-807.
[30]	W. S. Harris, “n-3 Fatty Acids and Serum Lipoproteins: Human Studies,” American Journal of Clinical Nutrition, Vol. 65, No. 5, 1997, pp. 1645S-1654S.
[31]	F. Belzung, T. Raclot and R. Groscolas, “Fish Oil n-3 Fatty Acids Selectively Limit the Hypertrophy of Abdominal Fat Depots in Growing Rats Fed High-Fat Diets,” American Journal of Physiology, Vol. 264, No. 6, 1993, pp. R1111-R1118.
[32]	J. O. Hill, J. C. Peters, D. Lin, F. Yakubu, H. Greene and L. Swift, “Lipid Accumulation and Body Fat Distribution Is Influenced by Type of Dietary Fat Fed to Rats,” Inter- national Journal of Obesity and Related Metabolic Disorders, Vol. 17, No. 4, 1993, pp. 223-236.
[33]	S. Ikemoto, M. Takahashi, N. Tsunoda, K. Maruyama, H. Itakura and O. Ezaki, “High-Fat Diet-Induced Hyperglycemia and Obesity in Mice: Differential Effects of Dietary Oils,” Metabolism, Vol. 45, No. 12, 1996, pp. 1539-1546. doi:10.1016/S0026-0495(96)90185-7
[34]	N. Mito, C. Kitada, T. Hosoda and K. Sato, “Effect of Diet-Induced Obesity on Ovalbumin-Specific Immune Response in a Murine Asthma Model,” Metabolism, Vol. 51, No. 10, 2002, pp. 1241-1246. doi:10.1053/meta.2002.35196
[35]	H. Yina, W. Liu, K. Goleniewska, N. A. Porter, J. D. Morrow and R. Stokes Peebles Jr., “Dietary Supplementation of Omega-3 Fatty Acid-Containing Fish Oil Suppresses F2-Isoprostanes but Enhances Inflammatory Cytokine Response in a Mouse Model of Ovalbumin-Induced Allergic Lung Inflammation,” Free Radical Biology and Medicine, Vol. 47, No. 5, 2009, pp. 622-628. doi:10.1016/j.freeradbiomed.2009.05.033