Dietary long chain n-3 polyunsaturated fatty acids prevent allergic sensitization to cow's milk protein in mice

Clinical and Experimental Allergy

Volumn 43, Issue 7, 2013, Pages 798-810

  Van den Elsen, L W J ^a   Van Esch, B C A M ^a,b   Hofman, G A ^a   Kant, J ^a   Van de Heijning, B J M ^b   Garssen, J ^a,b   Willemsen, L E M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b DANONE RESEARCH   (Netherlands)

Author keywords

Acute allergic skin response; Allergic sensitization; Cow's milk allergy; Dendritic cell; Fish oil; Immunoglobulins; Long chain n 3 polyunsaturated fatty acids; Mast cell; Regulatory T cell; T cell subsets

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CD8 ANTIGEN; DOCOSAHEXAENOIC ACID; FISH OIL; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G1; MILK PROTEIN; OMEGA 3 FATTY ACID; TRANSCRIPTION FACTOR FOXP3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DIET SUPPLEMENTATION; DISEASE PREDISPOSITION; FAT INTAKE; HUMORAL IMMUNITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; LIPID COMPOSITION; MESENTERY LYMPH NODE; MILK ALLERGY; MOUSE; NONHUMAN; PRIMARY PREVENTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SENSITIZATION; SKIN ALLERGY; SMALL INTESTINE; SPLEEN; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH2 CELL;

ANIMALS; CATTLE; DENDRITIC CELLS; DIETARY FATS, UNSATURATED; DISEASE MODELS, ANIMAL; FATTY ACIDS, UNSATURATED; FEMALE; FISH OILS; IMMUNOGLOBULINS; INTESTINES; MICE; MILK HYPERSENSITIVITY; SPLEEN; T-LYMPHOCYTES, REGULATORY;

EID: 84879519566     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12111     Document Type: Article

References (63)

1. Pascual CY, Crespo JF, Perez PG, Esteban MM. Food allergy and intolerance in children and adolescents, an update. Eur J Clin Nutr 2000; 54(Suppl 1):S75-8.
2. Wang J, Sampson HA. Food allergy. J Clin Invest 2011; 121:827-35.
3. Rona RJ, Keil T, Summers C et al. The prevalence of food allergy: a meta-analysis. J Allergy Clin Immunol 2007; 120:638-46.
4. Venter C, Arshad SH. Epidemiology of food allergy. Pediatr Clin North Am 2011; 58:327-49.
5. Fiocchi A, Brozek J, Schunemann H et al. World Allergy Organization (WAO) Diagnosis and Rationale for Action against Cow's Milk Allergy (DRACMA) Guidelines. Pediatr Allergy Immunol 2010; 21(Suppl 21):1-125.
6. Kattan JD, Cocco RR, Jarvinen KM. Milk and soy allergy. Pediatr Clin North Am 2011; 58:407-26.
7. Burks AW, Tang M, Sicherer S et al. ICON: food allergy. J Allergy Clin Immunol 2012; 129:906-20.
8. Rhodes HL, Sporik R, Thomas P, Holgate ST, Cogswell JJ. Early life risk factors for adult asthma: a birth cohort study of subjects at risk. J Allergy Clin Immunol 2001; 108:720-5.
9. Black PN, Sharpe S. Dietary fat and asthma: is there a connection? Eur Respir J 1997; 10:6-12.
10. Blumer N, Renz H. Consumption of omega3-fatty acids during perinatal life: role in immuno-modulation and allergy prevention. J Perinat Med 2007; 35(Suppl 1):S12-8.
11. Kankaanpaa P, Sutas Y, Salminen S, Lichtenstein A, Isolauri E. Dietary fatty acids and allergy. Ann Med 1999; 31:282-7.
12. Nakagomi T, Itaya H, Tominaga T, Yamaki M, Hisamatsu S, Nakagomi O. Is atopy increasing? Lancet 1994; 343:121-2.
13. Sugano M, Hirahara F. Polyunsaturated fatty acids in the food chain in Japan. Am J Clin Nutr 2000; 71:S189-S96.
14. Yu G, Bjorksten B. Polyunsaturated fatty acids in school children in relation to allergy and serum IgE levels. Pediatr Allergy Immunol 1998; 9:133-8.
15. Poysa L, Korppi M, Pietikainen M, Remes K, Juntunen-Backman K. Asthma, allergic rhinitis and atopic eczema in Finnish children and adolescents. Allergy 1991; 46:161-5.
16. Moilanen T, Nikkari T, Viikari J et al. Atherosclerosis precursors in Finnish children and adolescents. V. Fatty acid composition of serum cholesteryl esters: regional differences in Finland. Acta Paediatr Scand Suppl 1985; 318:111-7.
17. Furuhjelm C, Warstedt K, Larsson J et al. Fish oil supplementation in pregnancy and lactation may decrease the risk of infant allergy. Acta Paediatr 2009; 98:1461-7.
18. Reeves PG, Nielsen FH, Fahey GC Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 1993; 123:1939-51.
19. Schouten B, van Esch BC, Hofman GA et al. Oligosaccharide-induced whey-specific CD25(+) regulatory T-cells are involved in the suppression of cow milk allergy in mice. J Nutr 2010; 140:835-41.
20. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37:911-7.
21. Levant B, Ozias MK, Carlson SE. Diet (n-3) polyunsaturated fatty acid content and parity affect liver and erythrocyte phospholipid fatty acid composition in female rats. J Nutr 2007; 137:2425-30.
22. van den Elsen L, Garssen J, Willemsen L. Long chain N-3 polyunsaturated fatty acids in the prevention of allergic and cardiovascular disease. Curr Pharm Des 2012; 18:2375-92.
23. van den Elsen LW, Nusse Y, Balvers M et al. n-3 Long-chain PUFA reduce allergy-related mediator release by human mast cells in vitro via inhibition of reactive oxygen species. Br J Nutr 2012; 1-11. http://dx.doi.org/10.1017/S0007114512003959.
24. Coombes JL, Powrie F. Dendritic cells in intestinal immune regulation. Nat Rev Immunol 2008; 8:435-46.
25. Johansson C, Kelsall BL. Phenotype and function of intestinal dendritic cells. Semin Immunol 2005; 17:284-94.
26. Groom JR, Luster AD. CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 2011; 89:207-15.
27. Kim CH, Nagata K, Butcher EC. Dendritic cells support sequential reprogramming of chemoattractant receptor profiles during naive to effector T cell differentiation. J Immunol 2003; 171:152-8.
28. Sallusto F, Lenig D, Mackay CR, Lanzavecchia A. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med 1998; 187:875-83.
29. Xu D, Chan WL, Leung BP et al. Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J Exp Med 1998; 187:787-94.
30. Lohning M, Stroehmann A, Coyle AJ et al. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc Natl Acad Sci U S A 1998; 95:6930-5.
31. Fujimoto K, Karuppuchamy T, Takemura N et al. A new subset of CD103 + CD8alpha+ dendritic cells in the small intestine expresses TLR3, TLR7, and TLR9 and induces Th1 response and CTL activity. J Immunol 2011; 186:6287-95.
32. Uematsu S, Fujimoto K, Jang MH et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 2008; 9:769-76.
33. Dunstan JA, Mori TA, Barden A et al. Fish oil supplementation in pregnancy modifies neonatal allergen-specific immune responses and clinical outcomes in infants at high risk of atopy: a randomized, controlled trial. J Allergy Clin Immunol 2003; 112:1178-84.
34. Furuhjelm C, Warstedt K, Fageras M et al. Allergic disease in infants up to 2 years of age in relation to plasma omega-3 fatty acids and maternal fish oil supplementation in pregnancy and lactation. Pediatr Allergy Immunol 2011; 22:505-14.
35. Palmer DJ, Sullivan T, Gold MS et al. Effect of n-3 long chain polyunsaturated fatty acid supplementation in pregnancy on infants' allergies in first year of life: randomised controlled trial. BMJ 2012; 344:e184.
36. Klemens CM, Berman DR, Mozurkewich EL. The effect of perinatal omega-3 fatty acid supplementation on inflammatory markers and allergic diseases: a systematic review. BJOG 2011; 118:916-25.
37. Marks GB, Mihrshahi S, Kemp AS et al. Prevention of asthma during the first 5 years of life: a randomized controlled trial. J Allergy Clin Immunol 2006; 118:53-61.
38. Mihrshahi S, Peat JK, Webb K et al. The childhood asthma prevention study (CAPS): design and research protocol of a randomized trial for the primary prevention of asthma. Control Clin Trials 2001; 22:333-54.
39. D'Vaz N, Meldrum SJ, Dunstan JA et al. Fish oil supplementation in early infancy modulates developing infant immune responses. Clin Exp Allergy 2012; 42:1206-16.
40. Simopoulos AP. Importance of the omega-6/omega-3 balance in health and disease: evolutionary aspects of diet. World Rev Nutr Diet 2012; 102:10-21.
41. Krause TG, Koch A, Poulsen LK, Kristensen B, Olsen OR, Melbye M. Atopic sensitization among children in an arctic environment. Clin Exp Allergy 2002; 32:367-72.
42. Bang HO, Dyerberg J, Sinclair HM. The composition of the Eskimo food in north western Greenland. Am J Clin Nutr 1980; 33:2657-61.
43. Dyerberg J, Bang HO, Hjorne N. Fatty acid composition of the plasma lipids in Greenland Eskimos. Am J Clin Nutr 1975; 28:958-66.
44. Schouten B, van Esch BC, Hofman GA, van den Elsen LW, Willemsen LE, Garssen J. Acute allergic skin reactions and intestinal contractility changes in mice orally sensitized against casein or whey. Int Arch Allergy Immunol 2008; 147:125-34.
45. Kaur K, Harris SG, Padilla J, Graf BA, Phipps RP. Prostaglandin E2 as a modulator of lymphocyte mediated inflammatory and humoral responses. Adv Exp Med Biol 1999; 469:409-12.
46. Dunstan JA, Mori TA, Barden A et al. Maternal fish oil supplementation in pregnancy reduces interleukin-13 levels in cord blood of infants at high risk of atopy. Clin Exp Allergy 2003; 33:442-8.
47. Mizota T, Fujita-Kambara C, Matsuya N et al. Effect of dietary fatty acid composition on Th1/Th2 polarization in lymphocytes. JPEN J Parenter Enteral Nutr 2009; 33:390-6.
48. Weise C, Hilt K, Milovanovic M, Ernst D, Ruhl R, Worm M. Inhibition of IgE production by docosahexaenoic acid is mediated by direct interference with STAT6 and NFkappaB pathway in human B cells. J Nutr Biochem 2011; 22:269-75.
49. Calder PC. N-3 polyunsaturated fatty acids and immune cell function. Adv Enzyme Regul 1997; 37:197-237.
50. Johansson S, Lonnqvist A, Ostman S, Sandberg AS, Wold AE. Long-chain polyunsaturated fatty acids are consumed during allergic inflammation and affect T helper type 1 (Th1)- and Th2-mediated hypersensitivity differently. Clin Exp Immunol 2010; 160:411-9.
51. de Matos OG, Amaral SS, Pereira da Silva PE et al. Dietary supplementation with omega-3-PUFA-rich fish oil reduces signs of food allergy in ovalbumin-sensitized mice. Clin Dev Immunol 2012; 236564 [Epub ahead of print].
52. Draper E, Reynolds CM, Canavan M, Mills KH, Loscher CE, Roche HM. Omega-3 fatty acids attenuate dendritic cell function via NF-kappaB independent of PPARgamma. J Nutr Biochem 2011; 22:784-90.
53. Gallai V, Sarchielli P, Trequattrini A et al. Cytokine secretion and eicosanoid production in the peripheral blood mononuclear cells of MS patients undergoing dietary supplementation with n-3 polyunsaturated fatty acids. J Neuroimmunol 1995; 56:143-53.
54. Meydani SN, Endres S, Woods MM et al. Oral (n-3) fatty acid supplementation suppresses cytokine production and lymphocyte proliferation: comparison between young and older women. J Nutr 1991; 121:547-55.
55. Shinoda K, Tokoyoda K, Hanazawa A et al. Type II membrane protein CD69 regulates the formation of resting T-helper memory. Proc Natl Acad Sci U S A 2012; 109:7409-14.
56. Jensen GS, Patel D, Benson KF. A novel extract from bovine colostrum whey supports innate immune functions. II. Rapid changes in cellular immune function in humans. Prev Med 2012; 54(Suppl):S124-9.
57. Di Genova G, Savelyeva N, Suchacki A, Thirdborough SM, Stevenson FK. Bystander stimulation of activated CD4 + T cells of unrelated specificity following a booster vaccination with tetanus toxoid. Eur J Immunol 2010; 40:976-85.
58. Akdis CA, Akdis M. Mechanisms and treatment of allergic disease in the big picture of regulatory T cells. J Allergy Clin Immunol 2009; 123:735-46, quiz 47-8.
59. Ding Y, Xu J, Bromberg JS. Regulatory T cell migration during an immune response. Trends Immunol 2012; 33:174-80.
60. del Rio ML, Bernhardt G, Rodriguez-Barbosa JI, Forster R. Development and functional specialization of CD103 + dendritic cells. Immunol Rev 2010; 234:268-81.
61. Calder PC, Krauss-Etschmann S, de Jong EC et al. Early nutrition and immunity - progress and perspectives. Br J Nutr 2006; 96:774-90.
62. Kleemann R, Scott FW, Worz-Pagenstert U. Nimal Ratnayake WM, Kolb H. Impact of dietary fat on Th1/Th2 cytokine gene expression in the pancreas and gut of diabetes-prone BB rats. J Autoimmun 1998; 11:97-103.
63. Yaqoob P, Calder PC. The effects of dietary lipid manipulation on the production of murine T cell-derived cytokines. Cytokine 1995; 7:548-53.