Regulation of TH17 markers early in life through maternal farm exposure

Journal of Allergy and Clinical Immunology

Volumn 133, Issue 3, 2014, Pages 864-871

  Lluis, Anna ^a   Ballenberger, Nikolaus ^a   Illi, Sabina ^a   Schieck, Maximilian ^b   Kabesch, Michael ^b   Illig, Thomas ^c,d   Schleich, Isolde ^a   Von Mutius, Erika ^a   Schaub, Bianca ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Cord blood; cytokines; farming; innate; regulatory T cells; single nucleotide polymorphism; T H17 cells

Indexed keywords

GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INTERLEUKIN 13; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 22; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 5; INTERLEUKIN 6; MARKER; MESSENGER RNA; PEPTIDOGLYCAN; PHYTOHEMAGGLUTININ; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; BIOLOGICAL MARKER; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; AGRICULTURAL WORKER; ARTICLE; CYTOKINE RELEASE; ENVIRONMENTAL EXPOSURE; FEMALE; GENE EXPRESSION; GENETIC PREDISPOSITION; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; PRENATAL EXPOSURE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SINGLE NUCLEOTIDE POLYMORPHISM; TH1 CELL; TH17 CELL; TH2 CELL; UMBILICAL CORD BLOOD; ANIMAL; BLOOD; DOMESTIC ANIMAL; FETUS BLOOD; GENETICS; HYPERSENSITIVITY; IMMUNOLOGY; INNATE; PREGNANCY; T(H)17 CELLS;

CORD BLOOD; CYTOKINES; FARMING; INNATE; REGULATORY T CELLS; SINGLE NUCLEOTIDE POLYMORPHISM; T(H)17 CELLS;

ANIMALS; ANIMALS, DOMESTIC; BIOLOGICAL MARKERS; ENVIRONMENTAL EXPOSURE; FEMALE; FETAL BLOOD; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; HYPERSENSITIVITY; MATERNAL EXPOSURE; POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84896722345     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2013.09.030     Document Type: Article

References (47)

1. M.J. McGeachy, and D.J. Cua Th17 cell differentiation: the long and winding road Immunity 28 2008 445 453
2. B. Stockinger, and M. Veldhoen Differentiation and function of Th17 T cells Curr Opin Immunol 19 2007 281 286
3. L. Cosmi, F. Liotta, E. Maggi, S. Romagnani, and F. Annunziato Th17 cells: new players in asthma pathogenesis Allergy 66 2011 989 998
4. D.M. Bullens, E. Truyen, L. Coteur, E. Dilissen, P.W. Hellings, and L.J. Dupont et al. IL-17 mRNA in sputum of asthmatic patients: linking T cell driven inflammation and granulocytic influx? Respir Res 7 2006 135
5. G. Ciprandi, M. De Amici, G. Murdaca, D. Fenoglio, F. Ricciardolo, and G. Marseglia et al. Serum interleukin-17 levels are related to clinical severity in allergic rhinitis Allergy 64 2009 1375 1378
6. M. Toda, D.Y. Leung, S. Molet, M. Boguniewicz, R. Taha, and P. Christodoulopoulos et al. Polarized in vivo expression of IL-11 and IL-17 between acute and chronic skin lesions J Allergy Clin Immunol 111 2003 875 881
7. M.S. Gold, and A.S. Kemp Atopic disease in childhood Med J Aust 182 2005 298 304
8. C.A. Liu, C.L. Wang, H. Chuang, C.Y. Ou, T.Y. Hsu, and K.D. Yang Prenatal prediction of infant atopy by maternal but not paternal total IgE levels J Allergy Clin Immunol 112 2003 899 904
9. M.M. Moore, S.L. Rifas-Shiman, J.W. Rich-Edwards, K.P. Kleinman, C.A. Camargo Jr., and D.R. Gold et al. Perinatal predictors of atopic dermatitis occurring in the first six months of life Pediatrics 113 2004 468 474
10. T. Alfven, C. Braun-Fahrlander, B. Brunekreef, E. von Mutius, J. Riedler, and A. Scheynius et al. Allergic diseases and atopic sensitization in children related to farming and anthroposophic lifestyle - the PARSIFAL study Allergy 61 2006 414 421
11. M.J. Ege, M. Mayer, A.C. Normand, J. Genuneit, W.O. Cookson, and C. Braun-Fahrlander et al. Exposure to environmental microorganisms and childhood asthma N Engl J Med 364 2011 701 709
12. J. Riedler, C. Braun-Fahrlander, W. Eder, M. Schreuer, M. Waser, and S. Maisch et al. Exposure to farming in early life and development of asthma and allergy: a cross-sectional survey Lancet 358 2001 1129 1133
13. M. Waser, K.B. Michels, C. Bieli, H. Floistrup, G. Pershagen, and E. von Mutius et al. Inverse association of farm milk consumption with asthma and allergy in rural and suburban populations across Europe Clin Exp Allergy 37 2007 661 670
14. G. Loss, S. Apprich, M. Waser, W. Kneifel, J. Genuneit, and G. Buchele et al. The protective effect of farm milk consumption on childhood asthma and atopy: the GABRIELA study J Allergy Clin Immunol 128 2011 766 773.e4
15. M.J. Ege, C. Bieli, R. Frei, R.T. van Strien, J. Riedler, and E. Ublagger et al. Prenatal farm exposure is related to the expression of receptors of the innate immunity and to atopic sensitization in school-age children J Allergy Clin Immunol 117 2006 817 823
16. B. Schaub, J. Liu, S. Hoppler, I. Schleich, J. Huehn, and S. Olek et al. Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells J Allergy Clin Immunol 123 2009 774 782.e5
17. D. Mucida, Y. Park, G. Kim, O. Turovskaya, I. Scott, and M. Kronenberg et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid Science 317 2007 256 260
18. E.M. Eisenstein, and C.B. Williams The T(reg)/Th17 cell balance: a new paradigm for autoimmunity Pediatr Res 65 2009 26R 31R
19. B. Schaub, J. Liu, S. Hoppler, S. Haug, C. Sattler, and A. Lluis et al. Impairment of T-regulatory cells in cord blood of atopic mothers J Allergy Clin Immunol 121 2008 1491 1499 e1-13
20. U.E. Gibson, C.A. Heid, and P.M. Williams A novel method for real time quantitative RT-PCR Genome Res 6 1996 995 1001
21. J. Liu, A. Lluis, S. Illi, L. Layland, S. Olek, and E. von Mutius et al. T regulatory cells in cord blood - FOXP3 demethylation as reliable quantitative marker PLoS One 5 2010 e13267
22. M.F. Moffatt, M. Kabesch, L. Liang, A.L. Dixon, D. Strachan, and S. Heath et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma Nature 448 2007 470 473
23. S. Purcell, B. Neale, K. Todd-Brown, L. Thomas, M.A. Ferreira, and D. Bender et al. PLINK: a tool set for whole-genome association and population-based linkage analyses Am J Hum Genet 81 2007 559 575
24. J.L. Espinoza, A. Takami, K. Nakata, M. Onizuka, T. Kawase, and H. Akiyama et al. A genetic variant in the IL-17 promoter is functionally associated with acute graft-versus-host disease after unrelated bone marrow transplantation PLoS One 6 2011 e26229
25. J. Chen, Y. Deng, J. Zhao, Z. Luo, W. Peng, and J. Yang et al. The polymorphism of IL-17 G-152A was associated with childhood asthma and bacterial colonization of the hypopharynx in bronchiolitis J Clin Immunol 30 2010 539 545
26. M. Schedel, D. Carr, N. Klopp, B. Woitsch, T. Illig, and D. Stachel et al. A signal transducer and activator of transcription 6 haplotype influences the regulation of serum IgE levels J Allergy Clin Immunol 114 2004 1100 1105
27. N. Ballenberger, A. Lluis, E. von Mutius, S. Illi, and B. Schaub Novel statistical approaches for non-normal censored immunological data: analysis of cytokine and gene expression data PLoS One 7 2012 e46423
28. E.L. Kaplan, and P. Meier Nonparametric estimation from incomplete observations J Am Stat Assoc 53 1958 457 481
29. Prentice RL. Linear rank tests with right censored data. Biometrika 1978;65:167-79.
30. P.C. O'Brien, and T.R. Fleming A paired Prentice-Wilcoxon test for censored paired data Biometrics 43 1987 169 180
31. J. Tobin Estimation of Relationships for Limited Dependent Variables Econometrica 26 1958 24 36
32. D.R. Helsel Nondetects and data analysis 2005 John Wiley & Sons Hoboken
33. A. Lluis, and B. Schaub Lesson from the farm environment Curr Opin Allergy Clin Immunol 12 2012 158 163
34. E. von Mutius, and D. Vercelli Farm living: effects on childhood asthma and allergy Nat Rev Immunol 10 2010 861 868
35. A. Bai, N. Lu, Y. Guo, Z. Liu, J. Chen, and Z. Peng All-trans retinoic acid down-regulates inflammatory responses by shifting the Treg/Th17 profile in human ulcerative and murine colitis J Leukoc Biol 86 2009 959 969
36. Schieck M, Michel S, Suttner K, Illig T, Zeilinger S, Franke A, et al. Genetic variation in TH17 pathway genes, childhood asthma, and total serum IgE levels. J Allergy Clin Immunol [E-pub 1 Nov 2013].
37. S. Sakaguchi, and F. Powrie Emerging challenges in regulatory T cell function and biology Science 317 2007 627 629
38. P. Ratajczak, A. Janin, R. Peffault de Latour, C. Leboeuf, A. Desveaux, and K. Keyvanfar et al. Th17/Treg ratio in human graft-versus-host disease Blood 116 2010 1165 1171
39. Y. Chen, C.J. Haines, I. Gutcher, K. Hochweller, W.M. Blumenschein, and T. McClanahan et al. Foxp3(+) regulatory T cells promote T helper 17 cell development in vivo through regulation of interleukin-2 Immunity 34 2011 409 421
40. A. Kimura, and T. Kishimoto IL-6: regulator of Treg/Th17 balance Eur J Immunol 40 2010 1830 1835
41. F. Zhang, G. Meng, and W. Strober Interactions among the transcription factors Runx1, RORgammat and Foxp3 regulate the differentiation of interleukin 17-producing T cells Nat Immunol 9 2008 1297 1306
42. K. Ichiyama, H. Yoshida, Y. Wakabayashi, T. Chinen, K. Saeki, and M. Nakaya et al. Foxp3 inhibits RORgammat-mediated IL-17A mRNA transcription through direct interaction with RORgammat J Biol Chem 283 2008 17003 17008
43. K.S. Voo, Y.H. Wang, F.R. Santori, C. Boggiano, K. Arima, and L. Bover et al. Identification of IL-17-producing FOXP3+ regulatory T cells in humans Proc Natl Acad Sci U S A 106 2009 4793 4798
44. I. Dzhagalov, V. Giguere, and Y.W. He Lymphocyte development and function in the absence of retinoic acid-related orphan receptor alpha J Immunol 173 2004 2952 2959
45. J. Nolting, C. Daniel, S. Reuter, C. Stuelten, P. Li, and H. Sucov et al. Retinoic acid can enhance conversion of naive into regulatory T cells independently of secreted cytokines J Exp Med 206 2009 2131 2139
46. R.H. Duerr, K.D. Taylor, S.R. Brant, J.D. Rioux, M.S. Silverberg, and M.J. Daly et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene Science 314 2006 1461 1463
47. M. Schedel, L.A. Pinto, B. Schaub, P. Rosenstiel, D. Cherkasov, and L. Cameron et al. IRF-1 gene variations influence IgE regulation and atopy Am J Respir Crit Care Med 177 2008 613 621