Maternal immune response to helminth infection during pregnancy determines offspring susceptibility to allergic airway inflammation

Journal of Allergy and Clinical Immunology

Volumn 134, Issue 6, 2014, Pages 1271-1279.e10

  Straubinger, Kathrin ^a   Paul, Sabine ^a   Prazeres Da Costa, Olivia ^a   Ritter, Manuel ^a   Buch, Thorsten ^a   Busch, Dirk H ^a   Layland, Laura E ^b   Prazeres Da Costa, Clarissa U ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

allergic airway inflammation; hygiene hypothesis; Maternal helminth infection; offspring; pregnancy in utero programming

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; ALLERGEN; CYTOKINE; IMMUNOGLOBULIN E; OVALBUMIN;

ALLERGIC AIRWAY INFLAMMATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DISEASE TRANSMISSION; EMBRYO; FEMALE; FERTILIZATION IN VITRO; FETOPLACENTAL UNIT; FETUS WEIGHT; GENE CONTROL; GENE EXPRESSION; HELMINTHIASIS; IMMUNE RESPONSE; IMMUNOMODULATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OVALBUMIN-INDUCED AIRWAY INFLAMMATION; PHENOTYPE; PREGNANCY RATE; SCHISTOSOMA MANSONI; TH1 CELL; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; GENETICS; IMMUNOLOGY; NEWBORN; PNEUMONIA; PREGNANCY; RESPIRATORY TRACT ALLERGY; SCHISTOSOMIASIS MANSONI; TRANSGENIC MOUSE;

ALLERGENS; ANIMALS; ANIMALS, NEWBORN; CYTOKINES; DISEASE SUSCEPTIBILITY; FEMALE; IMMUNOGLOBULIN E; MICE, INBRED BALB C; MICE, TRANSGENIC; OVALBUMIN; PNEUMONIA; PREGNANCY; RESPIRATORY HYPERSENSITIVITY; SCHISTOSOMIASIS MANSONI;

EID: 84919869119     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.05.034     Document Type: Article

References (43)

1. L.E. Layland, J. Mages, C. Loddenkemper, A. Hoerauf, H. Wagner, and R. Lang Pronounced phenotype in activated regulatory T cells during a chronic helminth infection J Immunol 184 2010 713 724
2. L.E. Layland, R. Rad, H. Wagner, and C.U. da Costa Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2 Eur J Immunol 37 2007 2174 2184
3. N.E. Mangan, R.E. Fallon, P. Smith, N. van Rooijen, A.N. McKenzie, and P.G. Fallon Helminth infection protects mice from anaphylaxis via IL-10-producing B cells J Immunol 173 2004 6346 6356
4. E.J. Pearce Priming of the immune response by schistosome eggs Parasite Immunol 27 2005 265 270
5. M.I. Asher, S. Montefort, B. Björkstén, C.K. Lai, D.P. Strachan, and S.K. Weiland Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys Lancet 368 2006 733 743
6. M. Yazdanbakhsh, and L.C. Rodrigues Allergy and the hygiene hypothesis: the Th1/Th2 counterregulation can not provide an explanation Wien Klin Wochenschr 113 2001 899 902
7. A.H. van den Biggelaar, R. van Ree, L.C. Rodrigues, B. Lell, A.M. Deelder, and P.G. Kremsner Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10 Lancet 356 2000 1723 1727
8. P. Zaccone, O. Burton, N. Miller, F.M. Jones, D.W. Dunne, and A. Cooke Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice Eur J Immunol 39 2009 1098 1107
9. H.H. Smits, H. Hammad, M. van Nimwegen, T. Soullie, M.A. Willart, and E. Lievers Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection J Allergy Clin Immunol 120 2007 932 940
10. N.E. Mangan, N. van Rooijen, A.N. McKenzie, and P.G. Fallon Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness J Immunol 176 2006 138 147
11. + Treg cells PLoS Negl Trop Dis 7 2013 e2379
12. R.M. Maizels, E.J. Pearce, D. Artis, M. Yazdanbakhsh, and T.A. Wynn Regulation of pathogenesis and immunity in helminth infections J Exp Med 206 2009 2059 2066
13. J. Rowe, M. Kusel, B.J. Holt, D. Suriyaarachchi, M. Serralha, and E. Hollams Prenatal versus postnatal sensitization to environmental allergens in a high-risk birth cohort J Allergy Clin Immunol 119 2007 1164 1173
14. M.J. Ege, M. Mayer, A.C. Normand, J. Genuneit, W.O. Cookson, and C. Braun-Fahrländer Exposure to environmental microorganisms and childhood asthma N Engl J Med 364 2011 701 709
15. M.J. Ege, D.P. Strachan, W.O. Cookson, M.F. Moffatt, I. Gut, and M. Lathrop Gene-environment interaction for childhood asthma and exposure to farming in Central Europe J Allergy Clin Immunol 127 2011 138 144
16. M.L. Conrad, R. Ferstl, R. Teich, S. Brand, N. Blümer, and A.O. Yildirim Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78 J Exp Med 206 2009 2869 2877
17. R.H. Lim, L. Kobzik, and M. Dahl Risk for asthma in offspring of asthmatic mothers versus fathers: a meta-analysis PLoS One 5 2010 e10134
18. B. Schaub, J. Liu, S. Hoppler, I. Schleich, J. Huehn, and S. Olek Maternal farm exposure modulates neonatal immune mechanisms through regulatory T cells J Allergy Clin Immunol 123 2009 774 782.e5
19. P.I. Pfefferle, O. Pinkenburg, and H. Renz Fetal epigenetic mechanisms and innate immunity in asthma Curr Allergy Asthma Rep 10 2010 434 443
20. N. Blümer, U. Herz, M. Wegmann, and H. Renz Prenatal lipopolysaccharide-exposure prevents allergic sensitization and airway inflammation, but not airway responsiveness in a murine model of experimental asthma Clin Exp Allergy 35 2005 397 402
21. C. Lima, V.M. Souza, E.L. Faquim-Mauro, M.S. Hoshida, E. Bevilacqua, and M.S. Macedo Modulation of the induction of lung and airway allergy in the offspring of IFN-gamma-treated mother mice J Immunol 175 2005 3554 3559
22. M. Korthals, M.J. Ege, C.C. Tebbe, E. von Mutius, and J. Bauer Application of PCR-SSCP for molecular epidemiological studies on the exposure of farm children to bacteria in environmental dust J Microbiol Methods 73 2008 49 56
23. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, and S. Dudoit Bioconductor: open software development for computational biology and bioinformatics Genome Biol 5 2004 R80
24. L. Gautier, L. Cope, B.M. Bolstad, and R.A. Irizarry affy-analysis of Affymetrix GeneChip data at the probe level Bioinformatics 20 2004 307 315
25. G.K. Smyth Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat Appl Genet Mol Biol 3 2004 Article3
26. A.A. Akhiani, N. Lycke, L.A. Nilsson, S. Olling, and O. Ouchterlony Lack of interferon-gamma receptor does not influence the outcome of infection in murine schistosomiasis mansoni Scand J Immunol 43 1996 257 262
27. Y.A. Ghaffar, M. Kamel, M. el-Sobky, R. Bahnasy, and G.T. Strickland Response to hepatitis B vaccine in infants born to mothers with schistosomiasis Lancet 2 1989 272
28. S. Bassily, A. Kotkat, K.C. Hyams, F.G. Youssef, N.A. El-Masry, and R. Arthur Immunogenicity of recombinant hepatitis B vaccine among infants of mothers with active schistosomiasis Am J Trop Med Hyg 57 1997 197 199
29. H.H. Smits, B. Everts, F.C. Hartgers, and M. Yazdanbakhsh Chronic helminth infections protect against allergic diseases by active regulatory processes Curr Allergy Asthma Rep 10 2010 3 12
30. A.M. Attallah, A.T. Abbas, M.I. Dessouky, H.M. El-emshaty, and H.M. Elsheikha Susceptibility of neonate mice born to Schistosoma mansoni-infected and noninfected mothers to subsequent S. mansoni infection Parasitol Res 99 2006 137 145
31. Pd Santos, I.R. Sales, G.V. Schirato, V.M. Costa, M.C. Albuquerque, and V.M. Souza Influence of maternal schistosomiasis on the immunity of adult offspring mice Parasitol Res 107 2010 95 102
32. H. Mpairwe, E.L. Webb, L. Muhangi, J. Ndibazza, D. Akishule, and M. Nampijja Anthelminthic treatment during pregnancy is associated with increased risk of infantile eczema: randomised-controlled trial results Pediatr Allergy Immunol 22 2011 305 312
33. M. Ritter, O. Gross, S. Kays, J. Ruland, F. Nimmerjahn, and S. Saijo Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses Proc Natl Acad Sci U S A 107 2010 20459 20464
34. R. Tweyongyere, P.A. Mawa, M. Kihembo, F.M. Jones, E.L. Webb, and S. Cose Effect of praziquantel treatment of Schistosoma mansoni during pregnancy on immune responses to schistosome antigens among the offspring: results of a randomised, placebo-controlled trial BMC Infect Dis 11 2011 234
35. A.M. Attallah, G.E. Ghanem, H. Ismail, and A.M. El Waseef Placental and oral delivery of Schistosoma mansoni antigen from infected mothers to their newborns and children Am J Trop Med Hyg 68 2003 647 651
36. J.C. Jimenez-Chillaron, E. Isganaitis, M. Charalambous, S. Gesta, T. Pentinat-Pelegrin, and R.R. Faucette Intergenerational transmission of glucose intolerance and obesity by in utero undernutrition in mice Diabetes 58 2009 460 468
37. S.F. Ng, R.C. Lin, D.R. Laybutt, R. Barres, J.A. Owens, and M.J. Morris Chronic high-fat diet in fathers programs ß-cell dysfunction in female rat offspring Nature 467 2010 963 966
38. P.C. Arck, and K. Hecher Fetomaternal immune cross-talk and its consequences for maternal and offspring's health Nat Med 19 2013 548 556
39. J.D. Kurtis, A. Higashi, H.W. Wu, F. Gundogan, E.A. McDonald, and S. Sharma Maternal Schistosomiasis japonica is associated with maternal, placental, and fetal inflammation Infect Immun 79 2011 1254 1261
40. Y.A. Bobetsis, S.P. Barros, D.M. Lin, R.M. Arce, and S. Offenbacher Altered gene expression in murine placentas in an infection-induced intrauterine growth restriction model: a microarray analysis J Reprod Immunol 85 2010 140 148
41. N.Q. Liu, A.T. Kaplan, V. Lagishetty, Y.B. Ouyang, Y. Ouyang, and C.F. Simmons Vitamin D and the regulation of placental inflammation J Immunol 186 2011 5968 5974
42. A. Wittke, V. Weaver, B.D. Mahon, A. August, and M.T. Cantorna Vitamin D receptor-deficient mice fail to develop experimental allergic asthma J Immunol 173 2004 3432 3436
43. S. Brand, R. Teich, T. Dicke, H. Harb, A.Ö. Yildirim, and J. Tost Epigenetic regulation in murine offspring as a novel mechanism for transmaternal asthma protection induced by microbes J Allergy Clin Immunol 128 2011 618 625 e1-7