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Perinatal programming of murine immune responses by polyunsaturated fatty acids

Published online by Cambridge University Press:  22 December 2010

N. van Vlies*
Affiliation:
Division of Pharmacology, Department of Pharmaceutical Sciences, Utrecht University, The Netherlands
A. Hogenkamp
Affiliation:
Division of Pharmacology, Department of Pharmaceutical Sciences, Utrecht University, The Netherlands
A. L. Fear
Affiliation:
Institute of Human Nutrition, Department of School of Medicine, University of Southampton, Southampton, United Kingdom
B. C. van Esch
Affiliation:
Division of Pharmacology, Department of Pharmaceutical Sciences, Utrecht University, The Netherlands
A. Oosting
Affiliation:
Platform Immunology, Danone Research, Centre for Specialized Nutrition, Wageningen, The Netherlands
B. van de Heijning
Affiliation:
Platform Immunology, Danone Research, Centre for Specialized Nutrition, Wageningen, The Netherlands
E. van der Beek
Affiliation:
Platform Immunology, Danone Research, Centre for Specialized Nutrition, Wageningen, The Netherlands
P. C. Calder
Affiliation:
Institute of Human Nutrition, Department of School of Medicine, University of Southampton, Southampton, United Kingdom
J. Garssen
Affiliation:
Division of Pharmacology, Department of Pharmaceutical Sciences, Utrecht University, The Netherlands Platform Immunology, Danone Research, Centre for Specialized Nutrition, Wageningen, The Netherlands
*
*Address for correspondence: N. van Vlies, Division of Pharmacology, Department of Pharmaceutical Sciences, Utrecht University, The Netherlands. (Email n.vanvlies@uu.nl)

Abstract

Linoleic acid and α-linolenic acid are essential fatty acids (eFAs) and have to be acquired from the diet. eFAs are the precursors for long-chain polyunsaturated fatty acids (lcPUFAs), which are important immune-modulating compounds. lcPUFAs can be converted into eicosanoids and other mediators. They affect membrane structure and fluidity and can alter gene expression. There has been a marked change in dietary fatty acid intake over the last several decades. Since eFAs are acquired from the diet and immune development occurs mainly perinatally, the maternal diet may influence fetal and neonatal eFA levels, and thereby lcPUFA status, and thus immune development and function. To study whether early exposure to eFAs can program immune function, mice were fed diets varying in the ratio of ω-3 to ω-6-eFAs during pregnancy and/or lactation. After weaning, pups received a Western-style diet. At 11 weeks of age, the effects of maternal diet on the offspring's allergic and vaccination responses were examined using the T-helper 2 driven ovalbumin-induced allergy model and the T-helper 1 driven influenza-vaccination model, respectively. Offspring of dams fed a high α-linolenic acid diet during lactation showed an enhanced vaccination response. As diets with either low or high ω-3/ω-6-eFA ratio attenuated the T-helper 2 allergic response, the high α-linolenic acid diet fed during lactation had the most pronounced effect. These results indicate that there is a programming effect of maternal diet on the offspring's immune response and that in mice the window of greatest susceptibility to maternal dietary intervention is the lactation/suckling period.

Type
Original Articles
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2010

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References

1. Eder, W, Ege, MJ, von Mutius, E. The asthma epidemic. N Engl J Med. 2006; 355, 22262235.CrossRefGoogle ScholarPubMed
2. Holt, P, Naspitz, C, Warner, JO. Early immunological influences. Chem Immunol Allergy. 2004; 84, 102127.CrossRefGoogle ScholarPubMed
3. Prescott, SL, Dunstan, JA. Prenatal fatty acid status and immune development: the pathways and the evidence. Lipids. 2007; 42, 801810.CrossRefGoogle ScholarPubMed
4. Hersoug, LG, Linneberg, A. The link between the epidemics of obesity and allergic diseases: does obesity induce decreased immune tolerance? Allergy. 2007; 62, 12051213.CrossRefGoogle ScholarPubMed
5. Dolinoy, DC, Das, R, Weidman, JR, Jirtle, RL. Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr Res. 2007; 61, 30R37R.CrossRefGoogle ScholarPubMed
6. Burdge, GC, Hanson, MA, Slater-Jefferies, JL, Lillycrop, KA. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br J Nutr. 2007; 97, 10361046.CrossRefGoogle ScholarPubMed
7. Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359, 6173.CrossRefGoogle ScholarPubMed
8. Enke, U, Seyfarth, L, Schleussner, E, Markert, UR. Impact of PUFA on early immune and fetal development. Br J Nutr. 2008; 100, 11581168.CrossRefGoogle ScholarPubMed
9. Simopoulos, AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother. 2002; 56, 365379.CrossRefGoogle ScholarPubMed
10. Brassard, P, Larbi, A, Grenier, A, et al. . Modulation of T-cell signalling by non-esterified fatty acids. Prostaglandins Leukot Essent Fatty Acids. 2007; 77, 337343.CrossRefGoogle ScholarPubMed
11. Chapkin, RS, Wang, N, Fan, YY, Lupton, JR, Prior, IA. Docosahexaenoic acid alters the size and distribution of cell surface microdomains. Biochim Biophys Acta. 2008; 1778, 466471.CrossRefGoogle ScholarPubMed
12. Shaikh, SR, Edidin, M. Polyunsaturated fatty acids, membrane organization, T cells, and antigen presentation. Am J Clin Nutr. 2006; 84, 12771289.CrossRefGoogle ScholarPubMed
13. Sierra, S, Lara-Villoslada, F, Comalada, M, Olivares, M, Xaus, J. Dietary fish oil n-3 fatty acids increase regulatory cytokine production and exert anti-inflammatory effects in two murine models of inflammation. Lipids. 2006; 41, 11151125.CrossRefGoogle ScholarPubMed
14. Duplus, E, Forest, C. Is there a single mechanism for fatty acid regulation of gene transcription? Biochem Pharmacol. 2002; 64, 893901.CrossRefGoogle Scholar
15. Duplus, E, Glorian, M, Forest, C. Fatty acid regulation of gene transcription. J Biol Chem. 2000; 275, 3074930752.CrossRefGoogle ScholarPubMed
16. Hihi, AK, Michalik, L, Wahli, W. PPARs: transcriptional effectors of fatty acids and their derivatives. Cell Mol Life Sci. 2002; 59, 790798.CrossRefGoogle ScholarPubMed
17. Krauss-Etschmann, S, Hartl, D, Rzehak, P, et al. . Decreased cord blood IL-4, IL-13, and CCR4 and increased TGF-beta levels after fish oil supplementation of pregnant women. J Allergy Clin Immunol. 2008; 121, 464470. e466.CrossRefGoogle ScholarPubMed
18. 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, 442448.CrossRefGoogle ScholarPubMed
19. 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, 11781184.CrossRefGoogle ScholarPubMed
20. Lauritzen, L, Hoppe, C, Straarup, EM, Michaelsen, KF. Maternal fish oil supplementation in lactation and growth during the first 2.5 years of life. Pediatr Res. 2005; 58, 235242.CrossRefGoogle ScholarPubMed
21. Salam, MT, Li, YF, Langholz, B, Gilliland, FD. Maternal fish consumption during pregnancy and risk of early childhood asthma. J Asthma. 2005; 42, 513518.CrossRefGoogle ScholarPubMed
22. Romieu, I, Torrent, M, Garcia-Esteban, R, et al. . Maternal fish intake during pregnancy and atopy and asthma in infancy. Clin Exp Allergy. 2007; 37, 518525.CrossRefGoogle ScholarPubMed
23. Gottrand, F. Long-chain polyunsaturated fatty acids influence the immune system of infants. J Nutr. 2008; 138, 1807S1812S.CrossRefGoogle ScholarPubMed
24. Gibson, RA, Neumann, MA, Makrides, M. Effect of increasing breast milk docosahexaenoic acid on plasma and erythrocyte phospholipid fatty acids and neural indices of exclusively breast fed infants. Eur J Clin Nutr. 1997; 51, 578584.CrossRefGoogle ScholarPubMed
25. Nasser, R, Stephen, AM, Goh, YK, Clandinin, MT. The effect of a controlled manipulation of maternal dietary fat intake on medium and long chain fatty acids in human breast milk in Saskatoon, Canada. Int Breastfeed J. 2010; 5, 38.CrossRefGoogle ScholarPubMed
26. Troina, AA, Figueiredo, MS, Moura, EG, et al. . Maternal flaxseed diet during lactation alters milk composition and programs the offspring body composition, lipid profile and sexual function. Food Chem Toxicol. 2010; 48, 697703.CrossRefGoogle ScholarPubMed
27. Korotkova, M, Gabrielsson, B, Lonn, M, Hanson, LA, Strandvik, B. Leptin levels in rat offspring are modified by the ratio of linoleic to alpha-linolenic acid in the maternal diet. J Lipid Res. 2002; 43, 17431749.CrossRefGoogle ScholarPubMed
28. D'Asti, E, Long, H, Tremblay-Mercier, J, et al. . Maternal dietary fat determines metabolic profile and the magnitude of endocannabinoid inhibition of the stress response in neonatal rat offspring. Endocrinology. 2010; 151, 16851694.CrossRefGoogle ScholarPubMed
29. Deurloo, DT, van Esch, BC, Hofstra, CL, Nijkamp, FP, van Oosterhout, AJ. CTLA4-IgG reverses asthma manifestations in a mild but not in a more “severe” ongoing murine model. Am J Respir Cell Mol Biol. 2001; 25, 751760.CrossRefGoogle Scholar
30. Vos, AP, Haarman, M, Buco, A, et al. . A specific prebiotic oligosaccharide mixture stimulates delayed-type hypersensitivity in a murine influenza vaccination model. Int Immunopharmacol. 2006; 6, 12771286.CrossRefGoogle Scholar
31. Bligh, EG, Dyer, WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959; 37, 911917.CrossRefGoogle ScholarPubMed
32. Faber, J, Vos, P, Kegler, D, et al. . Beneficial immune modulatory effects of a specific nutritional combination in a murine model for cancer cachexia. Br J Cancer. 2008; 99, 20292036.CrossRefGoogle Scholar
33. Oosting, A, Kegler, D, Boehm, G, et al. N-3 Long-chain polyunsaturated fatty acids prevent excessive fat deposition in adulthood in a mouse model of postnatal nutritional programming. Pediatr Res. epub 2010.CrossRefGoogle Scholar
34. Katan, MB, Deslypere, JP, van Birgelen, AP, Penders, M, Zegwaard, M. Kinetics of the incorporation of dietary fatty acids into serum cholesteryl esters, erythrocyte membranes, and adipose tissue: an 18-month controlled study. J Lipid Res. 1997; 38, 20122022.CrossRefGoogle ScholarPubMed
35. Moser, B, Clark-Lewis, I, Zwahlen, R, Baggiolini, M. Neutrophil-activating properties of the melanoma growth-stimulatory activity. J Exp Med. 1990; 171, 17971802.CrossRefGoogle ScholarPubMed
36. Schumacher, C, Clark-Lewis, I, Baggiolini, M, Moser, B. High- and low-affinity binding of GRO alpha and neutrophil-activating peptide 2 to interleukin 8 receptors on human neutrophils. Proc Natl Acad Sci U S A. 1992; 89, 1054210546.CrossRefGoogle ScholarPubMed
37. Heinzel, FP, Sadick, MD, Holaday, BJ, Coffman, RL, Locksley, RM. Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J Exp Med. 1989; 169, 5972.CrossRefGoogle ScholarPubMed
38. Mills, CD, Kincaid, K, Alt, JM, Heilman, MJ, Hill, AM. M-1/M-2 macrophages and the Th1/Th2 paradigm. J Immunol. 2000; 164, 61666173.CrossRefGoogle ScholarPubMed
39. Repa, A, Wild, C, Hufnagl, K, et al. . Influence of the route of sensitization on local and systemic immune responses in a murine model of type I allergy. Clin Exp Immunol. 2004; 137, 1218.CrossRefGoogle Scholar
40. Chapman, C, Morgan, LM, Murphy, MC. Maternal and early dietary fatty acid intake: changes in lipid metabolism and liver enzymes in adult rats. J Nutr. 2000; 130, 146151.CrossRefGoogle ScholarPubMed
41. Merzouk, H, Khan, NA. Implication of lipids in macrosomia of diabetic pregnancy: can n-3 polyunsaturated fatty acids exert beneficial effects? Clin Sci (Lond). 2003; 105, 519529.CrossRefGoogle ScholarPubMed