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The Impact of Vitamin E Isoforms on Asthma and Allergy

  • Joan M. Cook-MillsEmail author
Chapter
Part of the Nutrition and Health book series (NH)

Abstract

Asthma and allergic disease result from complex environmental and genetic interactions. These factors have been identified by epidemiological studies, randomized prevention trials, and animal models. Vitamin E is one of the environmental factors that can regulate responses to challenge with allergens. Reports for vitamin E have seemingly varied outcomes regarding benefits of vitamin E, but these differences are consistent with the differential functions of the isoforms of vitamin E. Mechanistic studies have identified opposing functions of the vitamin E isoforms α-tocopherol and γ-tocopherol. Moreover, differences in global prevalence of asthma may be an outcome, at least in part, of differences in amount of isoforms of tocopherols. In order to interpret human and preclinical studies, reports need to include measurements of the tocopherol isoforms in the treatments, in vehicles for the treatments, and in the plasma and/or tissues before and after intervention. Studies of differential regulation of inflammation by tocopherol isoforms provide a foundation for development of interventions to improve lung function in disease and raise the possibility of early life dietary interventions to limit the development of lung disease.

Keywords

Allergy Asthma Vitamin E α-Tocopherol γ-Tocopherol Human Animal models 

References

  1. 1.
    Martinez FD. Genes, environments, development and asthma: a reappraisal. Eur Respir J. 2007;29(1):179–84.PubMedCrossRefGoogle Scholar
  2. 2.
    Palli D, Masala G, Vineis P, Garte S, Saieva C, Krogh V, et al. Biomarkers of dietary intake of micronutrients modulate DNA adduct levels in healthy adults. Carcinogenesis. 2003;24(4):739–46.PubMedCrossRefGoogle Scholar
  3. 3.
    Fiscus LC, Van Herpen J, Steeber DA, Tedder TF, Tang ML. L-Selectin is required for the development of airway hyperresponsiveness but not airway inflammation in a murine model of asthma. J Allergy Clin Immunol. 2001;107(6):1019–24.PubMedCrossRefGoogle Scholar
  4. 4.
    Hakugawa J, Bae SJ, Tanaka Y, Katayama I. The inhibitory effect of anti-adhesion molecule antibodies on eosinophil infiltration in cutaneous late phase response in Balb/c mice sensitized with ovalbumin (OVA). J Dermatol. 1997;24:73–9.PubMedCrossRefGoogle Scholar
  5. 5.
    Sagara H, Matsuda H, Wada N, Yagita H, Fukuda T, Okumura K, et al. A monoclonal antibody against very late activation antigen-4 inhibits eosinophil accumulation and late asthmatic response in a guinea pig model of asthma. Int Arch Allergy Immunol. 1997;112:287–94.PubMedCrossRefGoogle Scholar
  6. 6.
    Chin JE, Hatfield CA, Winterrowd GE, Brashler JR, Vonderfecht SL, Fidler SF, et al. Airway recruitment of leukocytes in mice is dependent on alpha4-integrins and vascular cell adhesion molecule-1. Am J Physiol. 1997;272:L219–L29.PubMedCrossRefGoogle Scholar
  7. 7.
    Cook-Mills JM, Deem TL. Active participation of endothelial cells in inflammation. J Leukoc Biol. 2005;77(4):487–95.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Vestweber D. Novel insights into leukocyte extravasation. Curr Opin Hematol. 2012;19(3):212–7.PubMedCrossRefGoogle Scholar
  9. 9.
    Muller WA. Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol. 2011;6:323–44.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Yang L, Cohn L, Zhang DH, Homer R, Ray A, Ray P. Essential role of nuclear factor kappaB in the induction of eosinophilia in allergic airway inflammation. J Exp Med. 1998;188:1739–50.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Mould AW, Ramsay AJ, Matthaei KI, Young IG, Rothenberg ME, Foster PS. The effect of IL-5 and eotaxin expression in the lung on eosinophil trafficking and degranulation and the induction of bronchial hyperreactivity. J Immunol. 2000;164:2142–50.PubMedCrossRefGoogle Scholar
  12. 12.
    Bousquet J, Bousquet PJ, Godard P, Daures JP. The public health implications of asthma. Bull World Health Organ. 2005;83(7):548–54.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Vollmer WM, Osborne ML, Buist AS. 20-year trends in the prevalence of asthma and chronic airflow obstruction in an HMO. Am J Respir Crit Care Med. 1998;157(4 Pt 1):1079–84.PubMedCrossRefGoogle Scholar
  14. 14.
    Friebele E. The attack of asthma. Environ Health Perspect. 1996;104(1):22–5.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    van Schayck CP, Smit HA. The prevalence of asthma in children: a reversing trend. Eur Respir J. 2005;26(4):647–50.PubMedCrossRefGoogle Scholar
  16. 16.
    CDC National Asthma Control Program. http://www.cdc.gov/asthma/impacts_nation/asthmafactsheet.pdf (2012).
  17. 17.
    Akinbami LJ, Moorman JE, Bailey C, Zahran HS, King M, Johnson CA, et al. Trends in asthma prevalence, health care use, and mortality in the United States, 2001–2010. NCHS Data Brief. 2012;(94):1–8.Google Scholar
  18. 18.
    Center For Disease Control Report. http://www.cdc.gov/nchs/data/databriefs/db121.pdf (2013).
  19. 19.
    Uauy R, Hoffman DR, Birch EE, Birch DG, Jameson DM, Tyson J. Safety and efficacy of omega-3 fatty acids in the nutrition of very low birth weight infants: soy oil and marine oil supplementation of formula. J Pediatr. 1994;124(4):612–20.PubMedCrossRefGoogle Scholar
  20. 20.
    Cook-Mills JM, McCary CA. Isoforms of vitamin E differentially regulate inflammation. Endocr Metab Immune Disord Drug Targets. 2010;10:348–66.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Bousquet J, Anto J, Auffray C, Akdis M, Cambon-Thomsen A, Keil T, et al. MeDALL (Mechanisms of the development of ALLergy): an integrated approach from phenotypes to systems medicine. Allergy. 2011;66(5):596–604.PubMedCrossRefGoogle Scholar
  22. 22.
    Fedulov AV, Leme A, Yang Z, Dahl M, Lim R, Mariani TJ, et al. Pulmonary exposure to particles during pregnancy causes increased neonatal asthma susceptibility. Am J Respir Cell Mol Biol. 2008;38(1):57–67.PubMedCrossRefGoogle Scholar
  23. 23.
    Odaka Y, Nakano M, Tanaka T, Kaburagi T, Yoshino H, Sato-Mito N, et al. The influence of a high-fat dietary environment in the fetal period on postnatal metabolic and immune function. Obesity (Silver Spring). 2010;18(9):1688–94.CrossRefGoogle Scholar
  24. 24.
    Lim RH, Kobzik L, Dahl M. Risk for asthma in offspring of asthmatic mothers versus fathers: a meta-analysis. PLoS One. 2010;5(4):e10134.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Izzotti A, Balansky RM, Cartiglia C, Camoirano A, Longobardi M, De Flora S. Genomic and transcriptional alterations in mouse fetus liver after transplacental exposure to cigarette smoke. FASEB J. 2003;17(9):1127–9.PubMedCrossRefGoogle Scholar
  26. 26.
    Vanhees K, Coort S, Ruijters EJ, Godschalk RW, van Schooten FJ. Barjesteh van Waalwijk van Doorn-Khosrovani S. Epigenetics: prenatal exposure to genistein leaves a permanent signature on the hematopoietic lineage. FASEB J. 2011;25(2):797–807.PubMedCrossRefGoogle Scholar
  27. 27.
    Rebholz SL, Jones T, Burke KT, Jaeschke A, Tso P, D’Alessio DA, et al. Multiparity leads to obesity and inflammation in mothers and obesity in male offspring. Am J Physiol Endocrinol Metab. 2012;302:E449–57.PubMedCrossRefGoogle Scholar
  28. 28.
    Burke KT, Colvin PL, Myatt L, Graf GA, Schroeder F, Woollett LA. Transport of maternal cholesterol to the fetus is affected by maternal plasma cholesterol concentrations in the golden Syrian hamster. J Lipid Res. 2009;50(6):1146–55.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Woollett LA. Maternal cholesterol in fetal development: transport of cholesterol from the maternal to the fetal circulation. Am J Clin Nutr. 2005;82(6):1155–61.PubMedCrossRefGoogle Scholar
  30. 30.
    Lim RH, Kobzik L. Maternal transmission of asthma risk. Am J Reprod Immunol. 2009;61(1):1–10.PubMedCrossRefGoogle Scholar
  31. 31.
    Liu X, Agerbo E, Schlunssen V, Wright RJ, Li J, Munk-Olsen T. Maternal asthma severity and control during pregnancy and risk of offspring asthma. J Allergy Clin Immunol. 2017;27(17):30854–0.Google Scholar
  32. 32.
    Abdala-Valencia H, Berdnikovs S, Soveg F, Cook-Mills JM. Alpha-Tocopherol supplementation of allergic female mice inhibits development of CD11c+CD11b+ dendritic cells in utero and allergic inflammation in neonates. Am J Physiol Lung Cell Mol Physiol. 2014;307(00132):L482–96.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Abdala-Valencia H, Soveg F, Cook-Mills JM. γ-Tocopherol supplementation of allergic female mice augments development of CD11c+CD11b+ dendritic cells in utero and allergic inflammation in neonates. Am J Physiol Lung Cell Mol Physiol. 2016;310(8):L759–L71.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Hamada K, Suzaki Y, Goldman A, Ning YY, Goldsmith C, Palecanda A, et al. Allergen-independent maternal transmission of asthma susceptibility. J Immunol. 2003;170(4):1683–9.PubMedCrossRefGoogle Scholar
  35. 35.
    Fedulov AV, Leme AS, Kobzik L. Duration of allergic susceptibility in maternal transmission of asthma risk. Am J Reprod Immunol. 2007;58(2):120–8.PubMedCrossRefGoogle Scholar
  36. 36.
    Hubeau C, Apostolou I, Kobzik L. Targeting of CD25 and glucocorticoid-induced TNF receptor family-related gene-expressing T cells differentially modulates asthma risk in offspring of asthmatic and normal mother mice. J Immunol. 2007;178(3):1477–87.PubMedCrossRefGoogle Scholar
  37. 37.
    Hubeau C, Apostolou I, Kobzik L. Adoptively transferred allergen-specific T cells cause maternal transmission of asthma risk. Am J Pathol. 2006;168(6):1931–9.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Herz U, Joachim R, Ahrens B, Scheffold A, Radbruch A, Renz H. Allergic sensitization and allergen exposure during pregnancy favor the development of atopy in the neonate. Int Arch Allergy Immunol. 2001;124(1-3):193–6.PubMedCrossRefGoogle Scholar
  39. 39.
    Herz U, Joachim R, Ahrens B, Scheffold A, Radbruch A, Renz H. Prenatal sensitization in a mouse model. Am J Respir Crit Care Med. 2000;162(3 Pt 2):S62–5.PubMedCrossRefGoogle Scholar
  40. 40.
    Jarrett E, Hall E. Selective suppression of IgE antibody responsiveness by maternal influence. Nature. 1979;280(5718):145–7.PubMedCrossRefGoogle Scholar
  41. 41.
    Hunter SC, Cahoon EB. Enhancing vitamin E in oilseeds: unraveling tocopherol and tocotrienol biosynthesis. Lipids. 2007;42(2):97–108.PubMedCrossRefGoogle Scholar
  42. 42.
    Wolf G. How an increased intake of alpha-tocopherol can suppress the bioavailability of gamma-tocopherol. Nutr Rev. 2006;64(6):295–9.PubMedCrossRefGoogle Scholar
  43. 43.
    Leonard SW, Paterson E, Atkinson JK, Ramakrishnan R, Cross CE, Traber MG. Studies in humans using deuterium-labeled alpha- and gamma-tocopherols demonstrate faster plasma gamma-tocopherol disappearance and greater gamma-metabolite production. Free Radic Biol Med. 2005;38(7):857–66.PubMedCrossRefGoogle Scholar
  44. 44.
    Bella DL, Schock BC, Lim Y, Leonard SW, Berry C, Cross CE, et al. Regulation of the alpha-tocopherol transfer protein in mice: lack of response to dietary vitamin E or oxidative stress. Lipids. 2006;41(2):105–12.PubMedCrossRefGoogle Scholar
  45. 45.
    Cook-Mills JM, Abdala-Valencia H, Hartert T. Two faces of vitamin e in the lung. Am J Respir Crit Care Med. 2013;188(3):279–84.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Muller-Schmehl K, Beninde J, Finckh B, Florian S, Dudenhausen JW, Brigelius-Flohe R, et al. Localization of alpha-tocopherol transfer protein in trophoblast, fetal capillaries’ endothelium and amnion epithelium of human term placenta. Free Radic Res. 2004;38(4):413–20.PubMedCrossRefGoogle Scholar
  47. 47.
    Jishage K, Tachibe T, Ito T, Shibata N, Suzuki S, Mori T, et al. Vitamin E is essential for mouse placentation but not for embryonic development itself. Biol Reprod. 2005;73(5):983–7.PubMedCrossRefGoogle Scholar
  48. 48.
    Yoshida Y, Saito Y, Jones LS, Shigeri Y. Chemical reactivities and physical effects in comparison between tocopherols and tocotrienols: physiological significance and prospects as antioxidants. J Biosci Bioeng. 2007;104(6):439–45.PubMedCrossRefGoogle Scholar
  49. 49.
    Keiko Nishio MH, Akazawa Y, Shichiri M, Iwahashi H, Yoshihisa Hagihara YY, Niki E. Attenuation of lipopolysaccharide (LPS)-induced cytotoxicity by tocopherols and tocotrienols. Redox Biol. 2013;1:97–103.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    McCary CA, Yoon Y, Panagabko C, Cho W, Atkinson J, Cook-Mills JM. Vitamin E isoforms directly bind PKCalpha and differentially regulate activation of PKCalpha. Biochem J. 2012;441:189–98.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Berdnikovs S, Abdala-Valencia H, McCary C, Somand M, Cole R, Garcia A, et al. Isoforms of Vitamin E have Opposing Immunoregulatory Functions during Inflammation by Regulating Leukocyte Recruitment. J Immunol. 2009;182:4395–405.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Abdala-Valencia H, Berdnikovs S, Cook-Mills JM. Vitamin E isoforms differentially regulate intercellular adhesion molecule-1 activation of PKCalpha in human microvascular endothelial cells. PLoS One. 2012;7(7):e41054.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Jourd’heuil D, Morise Z, Conner EM, Kurose I, Grisham MB. Oxidant-regulation of gene expression in the chronically inflamed intestine. Keio J Med. 1997;46(1):10–5.PubMedCrossRefGoogle Scholar
  54. 54.
    de Luis DA, Armentia A, Aller R, Asensio A, Sedano E, Izaola O, et al. Dietary intake in patients with asthma: a case control study. Nutrition. 2005;21(3):320–4.PubMedCrossRefGoogle Scholar
  55. 55.
    Patel A, Liebner F, Netscher T, Mereiter K, Rosenau T. Vitamin E chemistry. Nitration of non-alpha-tocopherols: products and mechanistic considerations. J Org Chem. 2007;72(17):6504–12.PubMedCrossRefGoogle Scholar
  56. 56.
    Fakhrzadeh L, Laskin JD, Laskin DL. Ozone-induced production of nitric oxide and TNF-alpha and tissue injury are dependent on NF-kappaB p50. Am J Physiol Lung Cell Mol Physiol. 2004;287(2):L279–85.. Epub 2004 Apr 2.PubMedCrossRefGoogle Scholar
  57. 57.
    Wardlaw A. Eosinophil trafficking: new answers to old questions. Clin Exp Allergy. 2004;34(5):676–9.PubMedCrossRefGoogle Scholar
  58. 58.
    Hernandez ML, Wagner JG, Aline Kala R, Mills K, Wells HB, Alexis NE, et al. Vitamin E gamma-tocopherol reduces airway neutrophil recruitment after inhaled endotoxin challenge in rats and in healthy volunteers. Free Radic Biol Med. 2013;8(13):00054–3.Google Scholar
  59. 59.
    Wiser J, Alexis NE, Jiang Q, Wu W, Robinette C, Roubey R, et al. In vivo gamma-tocopherol supplementation decreases systemic oxidative stress and cytokine responses of human monocytes in normal and asthmatic subjects. Free Radic Biol Med. 2008;45(1):40–9.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Wagner JG, Harkema JR, Jiang Q, Illek B, Ames BN, Peden DB. Gamma-tocopherol attenuates ozone-induced exacerbation of allergic rhinosinusitis in rats. Toxicol Pathol. 2009;37(4):481–91.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Burbank AJ, Duran CG, Pan Y, Burns P, Jones S, Jiang Q, et al. Gamma tocopherol-enriched supplement reduces sputum eosinophilia and endotoxin-induced sputum neutrophilia in volunteers with asthma. J Allergy Clin Immunol. 2017;20(17):31110–7.Google Scholar
  62. 62.
    Duan L, Li J, Ma P, Yang X, Xu S. Vitamin E antagonizes ozone-induced asthma exacerbation in Balb/c mice through the Nrf2 pathway. Food Chem Toxicol. 2017;107(Pt A):47–56.PubMedCrossRefGoogle Scholar
  63. 63.
    Wagner JG, Jiang Q, Harkema JR, Ames BN, Illek B, Roubey RA, et al. Gamma-tocopherol prevents airway eosinophilia and mucous cell hyperplasia in experimentally induced allergic rhinitis and asthma. Clin Exp Allergy. 2008;38(3):501–11.PubMedCrossRefGoogle Scholar
  64. 64.
    Peh HY, Ho WE, Cheng C, Chan TK, Seow AC, Lim AY, et al. Vitamin E isoform gamma-tocotrienol downregulates house dust mite-induced asthma. J Immunol. 2015;195(2):437–44.PubMedCrossRefGoogle Scholar
  65. 65.
    Barthel SR, Johansson MW, McNamee DM, Mosher DF. Roles of integrin activation in eosinophil function and the eosinophilic inflammation of asthma. J Leukoc Biol. 2008;83(1):1–12.PubMedCrossRefGoogle Scholar
  66. 66.
    Marchese ME, Kumar R, Colangelo LA, Avila PC, Jacobs DR Jr, Gross M, et al. The vitamin E isoforms alpha-tocopherol and gamma-tocopherol have opposite associations with spirometric parameters: the CARDIA study. Respir Res. 2014;15(1):31.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Jordan JM, De Roos AJ, Renner JB, Luta G, Cohen A, Craft N, et al. A case-control study of serum tocopherol levels and the alpha- to gamma-tocopherol ratio in radiographic knee osteoarthritis: the Johnston County Osteoarthritis Project. Am J Epidemiol. 2004;159(10):968–77.PubMedCrossRefGoogle Scholar
  68. 68.
    Dietrich M, Traber MG, Jacques PF, Cross CE, Hu Y, Block G. Does gamma-tocopherol play a role in the primary prevention of heart disease and cancer? A review. J Am Coll Nutr. 2006;25(4):292–9.PubMedCrossRefGoogle Scholar
  69. 69.
    Munteanu A, Zingg JM. Cellular, molecular and clinical aspects of vitamin E on atherosclerosis prevention. Mol Asp Med. 2007;28(5-6):538–90.CrossRefGoogle Scholar
  70. 70.
    Siekmeier R, Steffen C, Marz W. Role of oxidants and antioxidants in atherosclerosis: results of in vitro and in vivo investigations. J Cardiovasc Pharmacol Ther. 2007;12(4):265–82.PubMedCrossRefGoogle Scholar
  71. 71.
    Meydani M. Vitamin E modulation of cardiovascular disease. Ann N Y Acad Sci. 2004;1031:271–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Dutta A, Dutta SK. Vitamin E and its role in the prevention of atherosclerosis and carcinogenesis: a review. J Am Coll Nutr. 2003;22(4):258–68.PubMedCrossRefGoogle Scholar
  73. 73.
    Cook-Mills JM, Marchese ME, Abdala-Valencia H. Vascular cell adhesion molecule-1 expression and signaling during disease: regulation by reactive oxygen species and antioxidants. Antioxid Redox Signal. 2011;15(6):1607–38.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Cook-Mills JM. Eosinophil-endothelial cell interactions. Eosinophils in health and disease. In: Lee J, Rosenberg HF, editors. Eosinophils in health and disease. Atlanta: Elsevier; 2012. p. 139–53.Google Scholar
  75. 75.
    McCary CA, Abdala-Valencia H, Berdnikovs S, Cook-Mills JM. Supplemental and highly elevated tocopherol doses differentially regulate allergic inflammation: reversibility of alpha-tocopherol and gamma-tocopherol’s effects. J Immunol. 2011;186(6):3674–85.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Redlich CA, Grauer JN, Van Bennekum AM, Clever SL, Ponn RB, Blaner WS. Characterization of carotenoid, vitamin A, and alpha-tocopherol levels in human lung tissue and pulmonary macrophages. Am J Respir Crit Care Med. 1996;154:1436–43.PubMedCrossRefGoogle Scholar
  77. 77.
    Cook-Mills JM, Avila PC. Vitamin E and D regulation of allergic asthma immunopathogenesis. Int Immunopharmacol. 2014;29(14):007.Google Scholar
  78. 78.
    Jiang Q, Christen S, Shigenaga MK, Ames BN. gamma-tocopherol, the major form of vitamin E in the US diet, deserves more attention. Am J Clin Nutr. 2001;74(6):714–22.PubMedCrossRefGoogle Scholar
  79. 79.
    Talegawkar SA, Johnson EJ, Carithers T, Taylor HA Jr, Bogle ML, Tucker KL. Total alpha-tocopherol intakes are associated with serum alpha-tocopherol concentrations in African American adults. J Nutr. 2007;137(10):2297–303.PubMedCrossRefGoogle Scholar
  80. 80.
    Abdala-Valencia H, Berdnikovs S, Cook-Mills JM. Vitamin E isoforms as modulators of lung inflammation. Nutrients. 2013;5(11):4347–63.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Bieri JG, Evarts RP. Tocopherols and fatty acids in American diets. The recommended allowance for vitamin E. J Am Diet Assoc. 1973;62(2):147–51.PubMedGoogle Scholar
  82. 82.
    Bieri JG, Evarts RP. Vitamin E adequacy of vegetable oils. J Am Diet Assoc. 1975;66(2):134–9.PubMedGoogle Scholar
  83. 83.
    Choo JH, Nagata M, Sutani A, Kikuchi I, Sakamoto Y. Theophylline attenuates the adhesion of eosinophils to endothelial cells. Int Arch Allergy Immunol. 2003;131(Suppl 1):40–5.PubMedCrossRefGoogle Scholar
  84. 84.
    Miller M, Sung KL, Muller WA, Cho JY, Roman M, Castaneda D, et al. Eosinophil tissue recruitment to sites of allergic inflammation in the lung is platelet endothelial cell adhesion molecule independent. J Immunol. 2001;167(4):2292–7.PubMedCrossRefGoogle Scholar
  85. 85.
    Davenpeck KL, Berens KL, Dixon RA, Dupre B, Bochner BS. Inhibition of adhesion of human neutrophils and eosinophils to P-selectin by the sialyl Lewis antagonist TBC1269: preferential activity against neutrophil adhesion in vitro. J Allergy Clin Immunol. 2000;105(4):769–75.PubMedCrossRefGoogle Scholar
  86. 86.
    Meydani SN, Shapiro AC, Meydani M, Macauley JB, Blumberg JB. Effect of age and dietary fat (fish, corn and coconut oils) on tocopherol status of C57BL/6Nia mice. Lipids. 1987;22:345–50.PubMedCrossRefGoogle Scholar
  87. 87.
    Myou S, Zhu X, Boetticher E, Myo S, Meliton A, Lambertino A, et al. Blockade of focal clustering and active conformation in beta 2-integrin-mediated adhesion of eosinophils to intercellular adhesion molecule-1 caused by transduction of HIV TAT-dominant negative Ras. J Immunol. 2002;169(5):2670–6.PubMedCrossRefGoogle Scholar
  88. 88.
    Gobel Y, Koletzko B, Bohles HJ, Engelsberger I, Forget D, Le Brun A, et al. Parenteral fat emulsions based on olive and soybean oils: a randomized clinical trial in preterm infants. J Pediatr Gastroenterol Nutr. 2003;37(2):161–7.PubMedCrossRefGoogle Scholar
  89. 89.
    Weiss ST. Diet as a risk factor for asthma. Ciba Found Symp. 1997;206:244–57.PubMedGoogle Scholar
  90. 90.
    Troisi RJ, Willett WC, Weiss ST, Trichopoulos D, Rosner B, Speizer FE. A prospective study of diet and adult-onset asthma [see comments]. Am J Respir Crit Care Med. 1995;151:1401–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Dow L, Tracey M, Villar A, Coggon D, Margetts BM, Campbell MJ, et al. Does dietary intake of vitamins C and E influence lung function in older people? Am J Respir Crit Care Med. 1996;154:1401–4.PubMedCrossRefGoogle Scholar
  92. 92.
    Smit HA, Grievink L, Tabak C. Dietary influences on chronic obstructive lung disease and asthma: a review of the epidemiological evidence. Proc Nutr Soc. 1999;58:309–19.PubMedCrossRefGoogle Scholar
  93. 93.
    Tabak C, Smit HA, Rasanen L, Fidanza F, Menotti A, Nissinen A, et al. Dietary factors and pulmonary function: a cross sectional study in middle aged men from three European countries. Thorax. 1999;54(11):1021–6.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Devereux G. Early life events in asthma--diet. Pediatr Pulmonol. 2007;42(8):663–73.PubMedCrossRefGoogle Scholar
  95. 95.
    Martindale S, McNeill G, Devereux G, Campbell D, Russell G, Seaton A. Antioxidant intake in pregnancy in relation to wheeze and eczema in the first two years of life. Am J Respir Crit Care Med. 2005;171(2):121–8.PubMedCrossRefGoogle Scholar
  96. 96.
    Hoskins A, Roberts JL 2nd, Milne G, Choi L, Dworski R. Natural-source d-alpha-tocopheryl acetate inhibits oxidant stress and modulates atopic asthma in humans in vivo. Allergy. 2012;67(5):676–82.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Devaraj S, Tang R, Adams-Huet B, Harris A, Seenivasan T, de Lemos JA, et al. Effect of high-dose alpha-tocopherol supplementation on biomarkers of oxidative stress and inflammation and carotid atherosclerosis in patients with coronary artery disease. Am J Clin Nutr. 2007;86(5):1392–8.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Allen S, Britton JR, Leonardi-Bee JA. Association between antioxidant vitamins and asthma outcome measures: systematic review and meta-analysis. Thorax. 2009;64(7):610–9.PubMedCrossRefGoogle Scholar
  99. 99.
    Kurti SP, Murphy JD, Ferguson CS, Brown KR, Smith JR, Harms CA. Improved lung function following dietary antioxidant supplementation in exercise-induced asthmatics. Respir Physiol Neurobiol. 2016;220:95–101.PubMedCrossRefGoogle Scholar
  100. 100.
    Devereux G, Seaton A. Diet as a risk factor for atopy and asthma. J Allergy Clin Immunol. 2005;115(6):1109–17.PubMedCrossRefGoogle Scholar
  101. 101.
    Pearson PJ, Lewis SA, Britton J, Fogarty A. Vitamin E supplements in asthma: a parallel group randomised placebo controlled trial. Thorax. 2004;59(8):652–6.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Hernandez M, Zhou H, Zhou B, Robinette C, Crissman K, Hatch G, et al. Combination treatment with high-dose vitamin C and alpha-tocopherol does not enhance respiratory-tract lining fluid vitamin C levels in asthmatics. Inhal Toxicol. 2009;21(3):173–81.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Zahran HS, Bailey C. Factors associated with asthma prevalence among racial and ethnic groups-United States, 2009-2010 Behavioral Risk Factor Surveillance System. J Asthma. 2013;11:11.Google Scholar
  104. 104.
    Cook-Mills J, Gebretsadik T, Abdala-Valencia H, Green J, Larkin EK, Dupont WD, et al. Interaction of vitamin E isoforms on asthma and allergic airway disease. Thorax. 2016;71(10):954–6.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Jacobs RR, Boehlecke B, van Hage-Hamsten M, Rylander R. Bronchial reactivity, atopy, and airway response to cotton dust. Am Rev Respir Dis. 1993;148(1):19–24.PubMedCrossRefGoogle Scholar
  106. 106.
    Delfino RJ, Quintana PJ, Floro J, Gastanaga VM, Samimi BS, Kleinman MT, et al. Association of FEV1 in asthmatic children with personal and microenvironmental exposure to airborne particulate matter. Environ Health Perspect. 2004;112(8):932–41.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Koskela H, Tukiainen H, Kononoff A, Pekkarinen H. Effect of whole-body exposure to cold and wind on lung function in asthmatic patients. Chest. 1994;105(6):1728–31.PubMedCrossRefGoogle Scholar
  108. 108.
    Blanc PD, Eisner MD, Katz PP, Yen IH, Archea C, Earnest G, et al. Impact of the home indoor environment on adult asthma and rhinitis. J Occup Environ Med. 2005;47(4):362–72.PubMedCrossRefGoogle Scholar
  109. 109.
    Hess KL, Babcock GF, Askew DS, Cook-Mills JM. A novel flow cytometric method for quantifying phagocytosis of apoptotic cells. Cytometry. 1997;27:145–52.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Elenius V, Palomares O, Waris M, Turunen R, Puhakka T, Ruckert B, et al. The relationship of serum vitamins A, D, E and LL-37 levels with allergic status, tonsillar virus detection and immune response. PLoS One. 2017;12(2):e0172350.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Hamalainen N, Nwaru BI, Erlund I, Takkinen HM, Ahonen S, Toppari J, et al. Serum carotenoid and tocopherol concentrations and risk of asthma in childhood: a nested case-control study. Clin Exp Allergy. 2017;47(3):401–9.PubMedCrossRefGoogle Scholar
  112. 112.
    Kalayci O, Besler T, Kilinc K, Sekerel BE, Saraclar Y. Serum levels of antioxidant vitamins (alpha tocopherol, beta carotene, and ascorbic acid) in children with bronchial asthma. Turk J Peds. 2000;42:17–21.Google Scholar
  113. 113.
    Kelly FJ, Mudway I, Blomberg A, Frew A, Sandstrom T. Altered lung antioxidant status in patients with mild asthma. Lancet. 1999;354:482–3.PubMedCrossRefGoogle Scholar
  114. 114.
    Schunemann HJ, Grant BJ, Freudenheim JL, Muti P, Browne RW, Drake JA, et al. The relation of serum levels of antioxidant vitamins C and E, retinol and carotenoids with pulmonary function in the general population. Am J Respir Crit Care Med. 2001;163:1246–55.PubMedCrossRefGoogle Scholar
  115. 115.
    Al-Abdulla NO, Al Naama LM, Hassan MK. Antioxidant status in acute asthmatic attack in children. J Pak Med Assoc. 2010;60(12):1023–7.PubMedGoogle Scholar
  116. 116.
    Ratnasinghe D, Tangrea JA, Forman MR, Hartman T, Gunter EW, Qiao YL, et al. Serum tocopherols, selenium and lung cancer risk among tin miners in China. Cancer Causes Control. 2000;11(2):129–35.PubMedCrossRefGoogle Scholar
  117. 117.
    Kleiber M. Metabolic turnover rate: a physiological meaning of the metabolic rate per unit body weight. J Theor Biol. 1975;53(1):199–204.PubMedCrossRefGoogle Scholar
  118. 118.
    Terpstra AH. Differences between humans and mice in efficacy of the body fat lowering effect of conjugated linoleic acid: role of metabolic rate. J Nutr. 2001;131(7):2067–8.PubMedCrossRefGoogle Scholar
  119. 119.
    Bachmanov AA, Reed DR, Beauchamp GK, Tordoff MG. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav Genet. 2002;32(6):435–43.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Villar J, Purwar M, Merialdi M, Zavaleta N, Ngoc TNN, Anthony J, et al. World Health Organisation multicentre randomised trial of supplementation with vitamins C and E among pregnant women at high risk for pre-eclampsia in populations of low nutritional status from developing countries. BJOG. 2009;116(6):780–8.PubMedCrossRefGoogle Scholar
  121. 121.
    McCance DR, Holmes VA, Maresh MJ, Patterson CC, Walker JD, Pearson DW, et al. Vitamins C and E for prevention of pre-eclampsia in women with type 1 diabetes (DAPIT): a randomised placebo-controlled trial. Lancet. 2010;376(9737):259–66.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Hauth JC, Clifton RG, Roberts JM, Spong CY, Myatt L, Leveno KJ, et al. Vitamin C and E supplementation to prevent spontaneous preterm birth: a randomized controlled trial. Obstet Gynecol. 2010;116(3):653–8.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Greenough A, Shaheen SO, Shennan A, Seed PT, Poston L. Respiratory outcomes in early childhood following antenatal vitamin C and E supplementation. Thorax. 2010;65(11):998–1003.PubMedCrossRefGoogle Scholar
  124. 124.
    Kalpdev A, Saha SC, Dhawan V. Vitamin C and E supplementation does not reduce the risk of superimposed PE in pregnancy. Hypertens Pregnancy. 2011;30(4):447–56.PubMedCrossRefGoogle Scholar
  125. 125.
    Gungorduk K, Asicioglu O, Gungorduk OC, Yildirim G, Besimoglu B, Ark C. Does vitamin C and vitamin E supplementation prolong the latency period before delivery following the preterm premature rupture of membranes? A randomized controlled study. Am J Perinatol. 2014;31(3):195–202.PubMedGoogle Scholar
  126. 126.
    Betti M, Ambrogini P, Minelli A, Floridi A, Lattanzi D, Ciuffoli S, et al. Maternal dietary loads of alpha-tocopherol depress protein kinase C signaling and synaptic plasticity in rat postnatal developing hippocampus and promote permanent deficits in adult offspring. J Nutr Biochem. 2011;22(1):60–70.PubMedCrossRefGoogle Scholar
  127. 127.
    Suchankova J, Voprsalova M, Kottova M, Semecky V, Visnovsky P. Effects of oral alpha-tocopherol on lung response in rat model of allergic asthma. Respirology. 2006;11(4):414–21.PubMedCrossRefGoogle Scholar
  128. 128.
    Okamoto N, Murata T, Tamai H, Tanaka H, Nagai H. Effects of alpha tocopherol and probucol supplements on allergen-induced airway inflammation and hyperresponsiveness in a mouse model of allergic asthma. Int Arch Allergy Immunol. 2006;141(2):172–80.PubMedCrossRefGoogle Scholar
  129. 129.
    Mabalirajan U, Aich J, Leishangthem GD, Sharma SK, Dinda AK, Ghosh B. Effects of vitamin E on mitochondrial dysfunction and asthma features in an experimental allergic murine model. J Appl Physiol. 2009;107(4):1285–92.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Mamdouh Z, Mikhailov A, Muller WA. Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment. J Exp Med. 2009;206(12):2795–808.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Mustacich DJ, Leonard SW, Devereaux MW, Sokol RJ, Traber MG. Alpha-tocopherol regulation of hepatic cytochrome P450s and ABC transporters in rats. Free Radic Biol Med. 2006;41(7):1069–78.PubMedCrossRefPubMedCentralGoogle Scholar
  132. 132.
    Abdala-Valencia H, Berdnikovs S, McCary CA, Urick D, Mahadevia R, Marchese ME, et al. Inhibition of allergic inflammation by supplementation with 5-hydroxytryptophan. Am J Physiol Lung Cell Mol Physiol. 2012;303:L642–L60.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Abdala-Valencia H, Earwood J, Bansal S, Jansen M, Babcock G, Garvy B, et al. Nonhematopoietic NADPH oxidase regulation of lung eosinophilia and airway hyperresponsiveness in experimentally induced asthma. Am J Physiol Lung Cell Mol Physiol. 2007;292(5):L1111–25.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Keshavan P, Deem TL, Schwemberger SJ, Babcock GF, Cook-Mills JM, Zucker SD. Unconjugated bilirubin inhibits VCAM-1-mediated transendothelial leukocyte migration. J Immunol. 2005;174:3709–18.PubMedCrossRefGoogle Scholar
  135. 135.
    Wagner KH, Kamal-Eldin A, Elmadfa I. Gamma-tocopherol – an underestimated vitamin? Ann Nutr Metab. 2004;48(3):169–88.PubMedCrossRefGoogle Scholar
  136. 136.
    Abdala-Valencia H, Cook-Mills JM. VCAM-1 signals activate endothelial cell protein kinase Ca via oxidation. J Immunol. 2006;177:6379–87.PubMedPubMedCentralCrossRefGoogle Scholar
  137. 137.
    Boyle FG, Yuhas RJ, Lien EL. Red blood cell and tissue phospholipid fatty acid profiles of weanling rats fed infant formula fat blends containing soy and/or corn oil. Ann Nutr Metab. 1996;40(4):234–42.PubMedCrossRefGoogle Scholar
  138. 138.
    Nelson SE, Rogers RR, Frantz JA, Ziegler EE. Palm olein in infant formula: absorption of fat and minerals by normal infants. Am J Clin Nutr. 1996;64(3):291–6.PubMedCrossRefGoogle Scholar
  139. 139.
    Blumer N, Herz U, Wegmann M, Renz H. Prenatal lipopolysaccharide-exposure prevents allergic sensitization and airway inflammation, but not airway responsiveness in a murine model of experimental asthma. Clin Exp Allergy. 2005;35(3):397–402.PubMedCrossRefGoogle Scholar
  140. 140.
    Devereux G, Barker RN, Seaton A. Antenatal determinants of neonatal immune responses to allergens. Clin Exp Allergy. 2002;32(1):43–50.PubMedCrossRefGoogle Scholar
  141. 141.
    Uthoff H, Spenner A, Reckelkamm W, Ahrens B, Wolk G, Hackler R, et al. Critical role of preconceptional immunization for protective and nonpathological specific immunity in murine neonates. J Immunol. 2003;171(7):3485–92.PubMedCrossRefGoogle Scholar
  142. 142.
    Beckhaus AA, Garcia-Marcos L, Forno E, Pacheco-Gonzalez RM, Celedon JC, Castro-Rodriguez JA. Maternal nutrition during pregnancy and risk of asthma, wheeze, and atopic diseases during childhood: a systematic review and meta-analysis. Allergy. 2015;70(12):1588–604.PubMedCrossRefGoogle Scholar
  143. 143.
    Miller DR, Turner SW, Spiteri-Cornish D, Scaife AR, Danielian PJ, Devereux GS, et al. Maternal vitamin D and E intakes during early pregnancy are associated with airway epithelial cell responses in neonates. Clin Exp Allergy. 2015;45(5):920–7.PubMedCrossRefGoogle Scholar
  144. 144.
    Allan KM, Prabhu N, Craig LC, McNeill G, Kirby B, McLay J, et al. Maternal vitamin D and E intakes during pregnancy are associated with asthma in children. Eur Respir J. 2015;45(4):1027–36.PubMedCrossRefGoogle Scholar
  145. 145.
    Kurukulaaratchy RJ, Waterhouse L, Matthews SM, Arshad SH. Are influences during pregnancy associated with wheezing phenotypes during the first decade of life? Acta Paediatr. 2005;94(5):553–8.PubMedCrossRefGoogle Scholar
  146. 146.
    Celedon JC, Litonjua AA, Ryan L, Platts-Mills T, Weiss ST, Gold DR. Exposure to cat allergen, maternal history of asthma, and wheezing in first 5 years of life. Lancet. 2002;360(9335):781–2.PubMedCrossRefGoogle Scholar
  147. 147.
    Kurukulaaratchy RJ, Matthews S, Waterhouse L, Arshad SH. Factors influencing symptom expression in children with bronchial hyperresponsiveness at 10 years of age. J Allergy Clin Immunol. 2003;112(2):311–6.PubMedCrossRefGoogle Scholar
  148. 148.
    Latzin P, Frey U, Roiha HL, Baldwin DN, Regamey N, Strippoli MP, et al. Prospectively assessed incidence, severity, and determinants of respiratory symptoms in the first year of life. Pediatr Pulmonol. 2007;42(1):41–50.PubMedCrossRefGoogle Scholar
  149. 149.
    Martinez FD, Wright AL, Taussig LM, Holberg CJ, Halonen M, Morgan WJ. Asthma and wheezing in the first six years of life. The Group Health Medical Associates. N Engl J Med. 1995;332(3):133–8.PubMedCrossRefGoogle Scholar
  150. 150.
    Litonjua AA, Carey VJ, Burge HA, Weiss ST, Gold DR. Parental history and the risk for childhood asthma. Does mother confer more risk than father? Am J Respir Crit Care Med. 1998;158(1):176–81.PubMedCrossRefGoogle Scholar
  151. 151.
    Folsgaard NV, Chawes BL, Rasmussen MA, Bischoff AL, Carson CG, Stokholm J, et al. Neonatal cytokine profile in the airway mucosal lining fluid is skewed by maternal atopy. Am J Respir Crit Care Med. 2012;185(3):275–80.PubMedCrossRefGoogle Scholar
  152. 152.
    Sonnenschein-van der Voort AM, Jaddoe VW, Moll HA, Hofman A, van der Valk RJ, de Jongste JC, et al. Influence of maternal and cord blood C-reactive protein on childhood respiratory symptoms and eczema. Pediatr Allergy Immunol. 2013;24(5):469–75.PubMedCrossRefGoogle Scholar
  153. 153.
    Wassall HJ, Devereux G, Seaton A, Barker RN. Complex effects of vitamin E and vitamin C supplementation on in vitro neonatal mononuclear cell responses to allergens. Nutrients. 2013;5(9):3337–51.PubMedPubMedCentralCrossRefGoogle Scholar
  154. 154.
    Turner SW, Campbell D, Smith N, Craig LC, McNeill G, Forbes SH, et al. Associations between fetal size, maternal {alpha}-tocopherol and childhood asthma. Thorax. 2010;65(5):391–7.PubMedCrossRefGoogle Scholar
  155. 155.
    Islam S, Narra V, Cote GM, Manganaro TF, Donahoe PK, Schnitzer JJ. Prenatal vitamin E treatment improves lung growth in fetal rats with congenital diaphragmatic hernia. J Pediatr Surg. 1999;34(1):172–6. discussion 6-7.PubMedCrossRefGoogle Scholar
  156. 156.
    Erkkola M, Karppinen M, Javanainen J, Rasanen L, Knip M, Virtanen SM. Validity and reproducibility of a food frequency questionnaire for pregnant Finnish women. Am J Epidemiol. 2001;154(5):466–76.PubMedCrossRefGoogle Scholar
  157. 157.
    West CE, Dunstan J, McCarthy S, Metcalfe J, D’Vaz N, Meldrum S, et al. Associations between maternal antioxidant intakes in pregnancy and infant allergic outcomes. Nutrients. 2012;4(11):1747–58.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Maslova E, Hansen S, Strom M, Halldorsson TI, Olsen SF. Maternal intake of vitamins A, E and K in pregnancy and child allergic disease: a longitudinal study from the Danish National Birth Cohort. Br J Nutr. 2014;111(6):1096–108.PubMedCrossRefGoogle Scholar
  159. 159.
    Leme AS, Hubeau C, Xiang Y, Goldman A, Hamada K, Suzaki Y, et al. Role of breast milk in a mouse model of maternal transmission of asthma susceptibility. J Immunol. 2006;176(2):762–9.PubMedCrossRefGoogle Scholar
  160. 160.
    Fedulov AV, Kobzik L. Allergy risk is mediated by dendritic cells with congenital epigenetic changes. Am J Respir Cell Mol Biol. 2011;44:285–92.PubMedCrossRefGoogle Scholar
  161. 161.
    Lim RH, Kobzik L. Transplacental passage of interleukins 4 and 13? PLoS One. 2009;4(3):e4660.PubMedPubMedCentralCrossRefGoogle Scholar
  162. 162.
    Zourbas S, Dubanchet S, Martal J, Chaouat G. Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy. Clin Exp Immunol. 2001;126(3):519–28.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Ostojic S, Dubanchet S, Chaouat G, Abdelkarim M, Truyens C, Capron F. Demonstration of the presence of IL-16, IL-17 and IL-18 at the murine fetomaternal interface during murine pregnancy. Am J Reprod Immunol. 2003;49(2):101–12.PubMedCrossRefGoogle Scholar
  164. 164.
    Bowen JM, Chamley L, Mitchell MD, Keelan JA. Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta. 2002;23(4):239–56.PubMedCrossRefGoogle Scholar
  165. 165.
    Gregor H, Egarter C, Levin D, Sternberger B, Heinze G, Leitich H, et al. The passage of granulocyte-macrophage colony-stimulating factor across the human placenta perfused in vitro. J Soc Gynecol Investig. 1999;6(6):307–10.PubMedCrossRefGoogle Scholar
  166. 166.
    Barrett EG, Rudolph K, Bowen LE, Bice DE. Parental allergic status influences the risk of developing allergic sensitization and an asthmatic-like phenotype in canine offspring. Immunology. 2003;110(4):493–500.PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    van Rijt LS, Lambrecht BN. Dendritic cells in asthma: a function beyond sensitization. Clin Exp Allergy. 2005;35(9):1125–34.PubMedCrossRefGoogle Scholar
  168. 168.
    Williams JW, Tjota MY, Clay BS, Vander Lugt B, Bandukwala HS, Hrusch CL, et al. Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat Commun. 2013;4:2990.PubMedPubMedCentralCrossRefGoogle Scholar
  169. 169.
    Abdala-Valencia H, Berdnikovs S, Soveg F, Cook-Mills JM. Alpha-tocopherol supplementation of allergic female mice inhibits development of CD11c+CD11b+ dendritic cells in utero and allergic inflammation in neonates. Am J Physiol Lung Cell Mol Physiol. 2014;307(6):L482–96.Google Scholar
  170. 170.
    Mikhaylova L, Zhang Y, Kobzik L, Fedulov AV. Link between epigenomic alterations and genome-wide aberrant transcriptional response to allergen in dendritic cells conveying maternal asthma risk. PLoS One. 2013;8(8):e70387.PubMedPubMedCentralCrossRefGoogle Scholar
  171. 171.
    Lim RH, Arredouani MS, Fedulov A, Kobzik L, Hubeau C. Maternal allergic contact dermatitis causes increased asthma risk in offspring. Respir Res. 2007;8:56.PubMedPubMedCentralCrossRefGoogle Scholar
  172. 172.
    Gerhold K, Avagyan A, Seib C, Frei R, Steinle J, Ahrens B, et al. Prenatal initiation of endotoxin airway exposure prevents subsequent allergen-induced sensitization and airway inflammation in mice. J Allergy Clin Immunol. 2006;118(3):666–73.PubMedCrossRefGoogle Scholar
  173. 173.
    Gerhold K, Bluemchen K, Franke A, Stock P, Hamelmann E. Exposure to endotoxin and allergen in early life and its effect on allergen sensitization in mice. J Allergy Clin Immunol. 2003;112(2):389–96.PubMedCrossRefGoogle Scholar
  174. 174.
    Tulic MK, Knight DA, Holt PG, Sly PD. Lipopolysaccharide inhibits the late-phase response to allergen by altering nitric oxide synthase activity and interleukin-10. Am J Respir Cell Mol Biol. 2001;24(5):640–6.PubMedCrossRefGoogle Scholar
  175. 175.
    Gerhold K, Blumchen K, Bock A, Seib C, Stock P, Kallinich T, et al. Endotoxins prevent murine IgE production, T(H)2 immune responses, and development of airway eosinophilia but not airway hyperreactivity. J Allergy Clin Immunol. 2002;110:110–6.PubMedCrossRefGoogle Scholar
  176. 176.
    Lima C, Souza VM, Faquim-Mauro EL, Hoshida MS, Bevilacqua E, Macedo MS, et al. Modulation of the induction of lung and airway allergy in the offspring of IFN-gamma-treated mother mice. J Immunol. 2005;175(6):3554–9.PubMedCrossRefGoogle Scholar
  177. 177.
    Fedulov A, Silverman E, Xiang Y, Leme A, Kobzik L. Immunostimulatory CpG oligonucleotides abrogate allergic susceptibility in a murine model of maternal asthma transmission. J Immunol. 2005;175(7):4292–300.PubMedCrossRefGoogle Scholar
  178. 178.
    de Brito CA, Fusaro AE, Victor JR, Rigato PO, Goldoni AL, Muniz BP, et al. CpG-induced Th1-type response in the downmodulation of early development of allergy and inhibition of B7 expression on T cells of newborn mice. J Clin Immunol. 2010;30(2):280–91.PubMedCrossRefGoogle Scholar
  179. 179.
    Stoney RM, Woods RK, Hosking CS, Hill DJ, Abramson MJ, Thien FC. Maternal breast milk long-chain n-3 fatty acids are associated with increased risk of atopy in breastfed infants. Clin Exp Allergy. 2004;34(2):194–200.PubMedCrossRefGoogle Scholar
  180. 180.
    Reichardt P, Muller D, Posselt U, Vorberg B, Diez U, Schlink U, et al. Fatty acids in colostrum from mothers of children at high risk of atopy in relation to clinical and laboratory signs of allergy in the first year of life. Allergy. 2004;59(4):394–400.PubMedCrossRefGoogle Scholar
  181. 181.
    Miyake Y, Okubo H, Sasaki S, Tanaka K, Hirota Y. Maternal dietary patterns during pregnancy and risk of wheeze and eczema in Japanese infants aged 16–24 months: the Osaka Maternal and Child Health Study. Pediatr Allergy Immunol. 2011;22(7):734–41.PubMedCrossRefGoogle Scholar
  182. 182.
    Verhasselt V, Milcent V, Cazareth J, Kanda A, Fleury S, Dombrowicz D, et al. Breast milk-mediated transfer of an antigen induces tolerance and protection from allergic asthma. Nat Med. 2008;14(2):170–5.PubMedCrossRefGoogle Scholar
  183. 183.
    Mosconi E, Rekima A, Seitz-Polski B, Kanda A, Fleury S, Tissandie E, et al. Breast milk immune complexes are potent inducers of oral tolerance in neonates and prevent asthma development. Mucosal Immunol. 2010;3(5):461–74.PubMedCrossRefGoogle Scholar
  184. 184.
    Lim R, Fedulov AV, Kobzik L. Maternal stress during pregnancy increases neonatal allergy susceptibility: role of glucocorticoids. Am J Physiol Lung Cell Mol Physiol. 2014;307(2):L141–8.PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Costa-Pinto FA, Basso AS, Britto LR, Malucelli BE, Russo M. Avoidance behavior and neural correlates of allergen exposure in a murine model of asthma. Brain Behav Immun. 2005;19(1):52–60.PubMedCrossRefGoogle Scholar
  186. 186.
    Costa-Pinto FA, Basso AS, De Sa-Rocha LC, Britto LR, Russo M, Palermo-Neto J. Neural correlates of IgE-mediated allergy. Ann N Y Acad Sci. 2006;1088:116–31.PubMedCrossRefGoogle Scholar
  187. 187.
    Portela Cde P, Massoco Cde O, de Lima WT, Palermo-Neto J. Stress-induced increment on total bronchoalveolar cell count in OVA-sensitized rats. Physiol Behav. 2001;72(3):415–20.PubMedCrossRefGoogle Scholar
  188. 188.
    Portela CP, Leick-Maldonado EA, Kasahara DI, Prado CM, Calvo-Tiberio IF, Martins MA, et al. Effects of stress and neuropeptides on airway responses in ovalbumin-sensitized rats. Neuroimmunomodulation. 2007;14(2):105–11.PubMedCrossRefGoogle Scholar
  189. 189.
    Portela Cde P, Tiberio Ide F, Leick-Maldonado EA, Martins MA, Palermo-Neto J. Effects of diazepam and stress on lung inflammatory response in OVA-sensitized rats. Am J Physiol Lung Cell Mol Physiol. 2002;282(6):L1289–95.PubMedCrossRefGoogle Scholar
  190. 190.
    Tonelli LH, Katz M, Kovacsics CE, Gould TD, Joppy B, Hoshino A, et al. Allergic rhinitis induces anxiety-like behavior and altered social interaction in rodents. Brain Behav Immun. 2009;23(6):784–93.PubMedPubMedCentralCrossRefGoogle Scholar
  191. 191.
    Lu Y, Liu M, Shi S, Jiang H, Yang L, Liu X, et al. Effects of stress in early life on immune functions in rats with asthma and the effects of music therapy. J Asthma. 2010;47(5):526–31.PubMedCrossRefGoogle Scholar
  192. 192.
    Chida Y, Sudo N, Sonoda J, Hiramoto T, Kubo C. Early-life psychological stress exacerbates adult mouse asthma via the hypothalamus-pituitary-adrenal axis. Am J Respir Crit Care Med. 2007;175(4):316–22.PubMedCrossRefGoogle Scholar
  193. 193.
    Strine TW, Mokdad AH, Balluz LS, Gonzalez O, Crider R, Berry JT, et al. Depression and anxiety in the United States: findings from the 2006 Behavioral Risk Factor Surveillance System. Psychiatr Serv. 2008;59(12):1383–90.PubMedCrossRefGoogle Scholar
  194. 194.
    Cheung TK, Lam B, Lam KF, Ip M, Ng C, Kung R, et al. Gastroesophageal reflux disease is associated with poor asthma control, quality of life, and psychological status in Chinese asthma patients. Chest. 2009;135(5):1181–5.PubMedCrossRefGoogle Scholar
  195. 195.
    Sansone RA, Sansone LA. Asthma: wheezing, woes, and worries. Psychiatry (Edgmont). 2008;5(10):48–52.Google Scholar
  196. 196.
    Di Marco F, Verga M, Santus P, Giovannelli F, Busatto P, Neri M, et al. Close correlation between anxiety, depression, and asthma control. Respir Med. 2010;104(1):22–8.PubMedCrossRefGoogle Scholar
  197. 197.
    Cordina M, Fenech AG, Vassallo J, Cacciottolo JM. Anxiety and the management of asthma in an adult outpatient population. Ther Adv Respir Dis. 2009;3(5):227–33.PubMedCrossRefGoogle Scholar
  198. 198.
    von Hertzen LC. Maternal stress and T-cell differentiation of the developing immune system: possible implications for the development of asthma and atopy. J Allergy Clin Immunol. 2002;109(6):923–8.CrossRefGoogle Scholar
  199. 199.
    Huang CC, Shih MC, Hsu NC, Chien Y, Chung BC. Fetal glucocorticoid synthesis is required for development of fetal adrenal medulla and hypothalamus feedback suppression. Endocrinology. 2012;153(10):4749–56.PubMedPubMedCentralCrossRefGoogle Scholar
  200. 200.
    Norbiato G, Bevilacqua M, Vago T, Clerici M. Glucocorticoids and Th-1, Th-2 type cytokines in rheumatoid arthritis, osteoarthritis, asthma, atopic dermatitis and AIDS. Clin Exp Rheumatol. 1997;15(3):315–23.PubMedGoogle Scholar
  201. 201.
    Ramirez F, Fowell DJ, Puklavec M, Simmonds S, Mason D. Glucocorticoids promote a TH2 cytokine response by CD4+ T cells in vitro. J Immunol. 1996;156(7):2406–12.PubMedGoogle Scholar
  202. 202.
    Groer MW, Humenick S, Hill PD. Characterizations and psychoneuroimmunologic implications of secretory immunoglobulin A and cortisol in preterm and term breast milk. J Perinat Neonatal Nurs. 1994;7(4):42–51.PubMedCrossRefGoogle Scholar
  203. 203.
    Murphy VE, Zakar T, Smith R, Giles WB, Gibson PG, Clifton VL. Reduced 11beta-hydroxysteroid dehydrogenase type 2 activity is associated with decreased birth weight centile in pregnancies complicated by asthma. J Clin Endocrinol Metab. 2002;87(4):1660–8.PubMedGoogle Scholar
  204. 204.
    Murphy VE, Gibson PG, Giles WB, Zakar T, Smith R, Bisits AM, et al. Maternal asthma is associated with reduced female fetal growth. Am J Respir Crit Care Med. 2003;168(11):1317–23.PubMedCrossRefGoogle Scholar
  205. 205.
    Shvedova AA, Kisin ER, Kagan VE, Karol MH. Increased lipid peroxidation and decreased antioxidants in lungs of guinea pigs following an allergic pulmonary response. Toxicol Appl Pharmacol. 1995;132:72–81.PubMedCrossRefGoogle Scholar
  206. 206.
    Hardy CL, Rolland JM, O’Hehir RE. The immunoregulatory and fibrotic roles of activin A in allergic asthma. Clin Exp Allergy. 2015;45(10):1510–22.PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Hedger MP, Winnall WR, Phillips DJ, de Kretser DM. The regulation and functions of activin and follistatin in inflammation and immunity. Vitam Horm. 2011;85:255–97.PubMedCrossRefGoogle Scholar
  208. 208.
    Sheikh A, Steiner MF, Cezard G, Bansal N, Fischbacher C, Simpson CR, et al. Ethnic variations in asthma hospital admission, readmission and death: a retrospective, national cohort study of 4.62 million people in Scotland. BMC Med. 2016;14(1):3.PubMedPubMedCentralCrossRefGoogle Scholar
  209. 209.
    Kim HB, Zhou H, Kim JH, Habre R, Bastain TM, Gilliland FD. Lifetime prevalence of childhood eczema and the effect of indoor environmental factors: analysis in Hispanic and non-Hispanic white children. Allergy Asthma Proc. 2016;37(1):64–71.PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Herman B Wells Center for Pediatric Research, Department of Pediatrics, Department of Microbiology and ImmunologyIndiana University School of MedicineIndianapolisUSA

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