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Published in: Allergy, Asthma & Clinical Immunology 1/2017

Open Access 01-12-2017 | Research

Preconception allergen sensitization can induce B10 cells in offspring: a potential main role for maternal IgG

Authors: Marília Garcia de Oliveira, Luana de Mendonça Oliveira, Aline Aparecida de Lima Lira, Fábio da Ressureição Sgnotto, Alberto José da Silva Duarte, Maria Notomi Sato, Jefferson Russo Victor

Published in: Allergy, Asthma & Clinical Immunology | Issue 1/2017

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Abstract

Background

The mechanisms through which allergies can be inhibited after preconception immunization with allergens are not fully understood. We aimed to evaluate whether maternal immunization can induce a regulatory B (B10) cell population in offspring in concert with allergy inhibition.

Methods

C57BL/6 females were or were not immunized with OVA and were mated with normal WT males. Their offspring were evaluated at 3 days of age or 20 days after neonatal immunization. Human peripheral B cells from atopic and non-atopic individuals were also evaluated.

Results

Preconception OVA immunization induced B10 cells in offspring, and IL-10 production appeared to be critical for FcγRIIB upregulation in offspring B cells. Murine and human IL-10-producing B cells responded in vitro to IgG according to the atopic repertoire of the cells.

Conclusions

Our results reveal that maternal immunization induces allergen-specific B10 cells in offspring and a pivotal role for the IgG repertoire in IL-10 production by murine and human B cells.
Appendix
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Literature
1.
go back to reference Fusaro A, Maciel M, Victor J, Oliveira C, Duarte A, Sato M. Influence of maternal murine immunization with Dermatophagoides pteronyssinus extract on the type I hypersensitivity response in offspring. Int Arch Allergy Immunol. 2002;127:208–16.CrossRefPubMed Fusaro A, Maciel M, Victor J, Oliveira C, Duarte A, Sato M. Influence of maternal murine immunization with Dermatophagoides pteronyssinus extract on the type I hypersensitivity response in offspring. Int Arch Allergy Immunol. 2002;127:208–16.CrossRefPubMed
2.
go back to reference Fusaro AE, Brito CA, Victor JR, Rigato PO, Goldoni AL, Duarte AJS, et al. Maternal-fetal interaction: preconception immunization in mice prevents neonatal sensitization induced by allergen exposure during pregnancy and breastfeeding. Immunology. 2007;122:107–15.CrossRefPubMedPubMedCentral Fusaro AE, Brito CA, Victor JR, Rigato PO, Goldoni AL, Duarte AJS, et al. Maternal-fetal interaction: preconception immunization in mice prevents neonatal sensitization induced by allergen exposure during pregnancy and breastfeeding. Immunology. 2007;122:107–15.CrossRefPubMedPubMedCentral
3.
go back to reference Fusaro AE, de Brito CA, Taniguchi EF, Muniz BP, Victor JR, Orii NM, et al. Balance between early life tolerance and sensitization in allergy: dependence on the timing and intensity of prenatal and postnatal allergen exposure of the mother. Immunology. 2009;128:e541–50.CrossRefPubMedPubMedCentral Fusaro AE, de Brito CA, Taniguchi EF, Muniz BP, Victor JR, Orii NM, et al. Balance between early life tolerance and sensitization in allergy: dependence on the timing and intensity of prenatal and postnatal allergen exposure of the mother. Immunology. 2009;128:e541–50.CrossRefPubMedPubMedCentral
4.
go back to reference Rigato PO, Fusaro AE, Victor JR, Sato MN. Maternal immunization to modulate the development of allergic response and pathogen infections. Immunotherapy. 2009;1:141–56.CrossRefPubMed Rigato PO, Fusaro AE, Victor JR, Sato MN. Maternal immunization to modulate the development of allergic response and pathogen infections. Immunotherapy. 2009;1:141–56.CrossRefPubMed
5.
go back to reference Victor J, Fusaro A, Duarte A, Sato M. Preconception maternal immunization to dust mite inhibits the type I hypersensitivity response of offspring. J Allergy Clin Immunol. 2003;111:269–77.CrossRefPubMed Victor J, Fusaro A, Duarte A, Sato M. Preconception maternal immunization to dust mite inhibits the type I hypersensitivity response of offspring. J Allergy Clin Immunol. 2003;111:269–77.CrossRefPubMed
6.
go back to reference Muniz BP, Victor JR, Oliveira LdM, de Lima Lira AA, Perini A, Olivo CR, et al. Tolerogenic microenvironment in neonatal period induced by maternal immunization with ovalbumin. Immunobiology. 2014;219:377–84.CrossRefPubMed Muniz BP, Victor JR, Oliveira LdM, de Lima Lira AA, Perini A, Olivo CR, et al. Tolerogenic microenvironment in neonatal period induced by maternal immunization with ovalbumin. Immunobiology. 2014;219:377–84.CrossRefPubMed
7.
go back to reference Victor JR, Muniz BP, Fusaro AE, de Brito CA, Taniguchi EF, Duarte AJS, et al. Maternal immunization with ovalbumin prevents neonatal allergy development and up-regulates inhibitory receptor Fc gamma RIIB expression on B cells. BMC Immunol. 2010;11:11.CrossRefPubMedPubMedCentral Victor JR, Muniz BP, Fusaro AE, de Brito CA, Taniguchi EF, Duarte AJS, et al. Maternal immunization with ovalbumin prevents neonatal allergy development and up-regulates inhibitory receptor Fc gamma RIIB expression on B cells. BMC Immunol. 2010;11:11.CrossRefPubMedPubMedCentral
8.
go back to reference Seeger M, Thierse HJ, Lange H, Shaw L, Hansen H, Lemke H. Antigen-independent suppression of the IgE immune response to bee venom phospholipase A2 by maternally derived monoclonal IgG antibodies. Eur J Immunol. 1998;28:2124–30.CrossRefPubMed Seeger M, Thierse HJ, Lange H, Shaw L, Hansen H, Lemke H. Antigen-independent suppression of the IgE immune response to bee venom phospholipase A2 by maternally derived monoclonal IgG antibodies. Eur J Immunol. 1998;28:2124–30.CrossRefPubMed
9.
go back to reference Rabinovitch N, Gelfand EW. Expression of functional activating and inhibitory Fc gamma receptors on human B cells. Int Arch Allergy Immunol. 2004;133:285–94.CrossRefPubMed Rabinovitch N, Gelfand EW. Expression of functional activating and inhibitory Fc gamma receptors on human B cells. Int Arch Allergy Immunol. 2004;133:285–94.CrossRefPubMed
11.
go back to reference Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, Fallon PG. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol. 2010;125(1114–24):e8. Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, Fallon PG. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol. 2010;125(1114–24):e8.
12.
13.
go back to reference Lira AA, de Oliveira MG, de Oliveira LM, Duarte AJ, Sato MN, Victor JR. Maternal immunization with ovalbumin or Dermatophagoides pteronyssinus has opposing effects on FcγRIIb expression on offspring B cells. Allergy Asthma Clin Immunol. 2014;10:47.CrossRefPubMedPubMedCentral Lira AA, de Oliveira MG, de Oliveira LM, Duarte AJ, Sato MN, Victor JR. Maternal immunization with ovalbumin or Dermatophagoides pteronyssinus has opposing effects on FcγRIIb expression on offspring B cells. Allergy Asthma Clin Immunol. 2014;10:47.CrossRefPubMedPubMedCentral
14.
go back to reference van Rijt LS, Kuipers H, Vos N, Hijdra D, Hoogsteden HC, Lambrecht BN. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma. J Immunol Methods. 2004;288:111–21.CrossRefPubMed van Rijt LS, Kuipers H, Vos N, Hijdra D, Hoogsteden HC, Lambrecht BN. A rapid flow cytometric method for determining the cellular composition of bronchoalveolar lavage fluid cells in mouse models of asthma. J Immunol Methods. 2004;288:111–21.CrossRefPubMed
15.
go back to reference 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;14:170–5.CrossRefPubMed 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;14:170–5.CrossRefPubMed
16.
go back to reference Li J, Shen C, Liu Y, Li Y, Sun L, Jiao L, et al. Impaired function of CD5 + CD19 + CD1dhi B10 cells on IgE secretion in an atopic dermatitis-like mouse model. PLoS ONE. 2015;10:e0132173.CrossRefPubMedPubMedCentral Li J, Shen C, Liu Y, Li Y, Sun L, Jiao L, et al. Impaired function of CD5 + CD19 + CD1dhi B10 cells on IgE secretion in an atopic dermatitis-like mouse model. PLoS ONE. 2015;10:e0132173.CrossRefPubMedPubMedCentral
17.
go back to reference Lira AADL, Oliveira MGD, Oliveira LMD, Duarte AJDS, Sato MN, Victor JR. Opposite effect on offspring Fc gamma RIIb B cells expression on dependency of maternal immunisation with OVA or Dermatophagoides pteronyssinus: different mechanisms for different allergens? Allergy. 2014;69:344. Lira AADL, Oliveira MGD, Oliveira LMD, Duarte AJDS, Sato MN, Victor JR. Opposite effect on offspring Fc gamma RIIb B cells expression on dependency of maternal immunisation with OVA or Dermatophagoides pteronyssinus: different mechanisms for different allergens? Allergy. 2014;69:344.
18.
go back to reference Victor JR. Influence of maternal immunization with allergens on the thymic maturation of lymphocytes with regulatory potential in children: a broad field for further exploration. J Immunol Res. 2014;2014:780386.CrossRefPubMedPubMedCentral Victor JR. Influence of maternal immunization with allergens on the thymic maturation of lymphocytes with regulatory potential in children: a broad field for further exploration. J Immunol Res. 2014;2014:780386.CrossRefPubMedPubMedCentral
19.
go back to reference Bento-de-Souza L, Victor JR, Bento-de-Souza LC, Arrais-Santos M, Rangel-Santos AC, Pereira-Costa É, et al. Constitutive expression of genes encoding notch receptors and ligands in developing lymphocytes, nTreg cells and dendritic cells in the human thymus. Results Immunol. 2016;6:15–20.CrossRefPubMedPubMedCentral Bento-de-Souza L, Victor JR, Bento-de-Souza LC, Arrais-Santos M, Rangel-Santos AC, Pereira-Costa É, et al. Constitutive expression of genes encoding notch receptors and ligands in developing lymphocytes, nTreg cells and dendritic cells in the human thymus. Results Immunol. 2016;6:15–20.CrossRefPubMedPubMedCentral
20.
go back to reference Stadler BM, Zürcher AW, Miescher S, Kricek F, Vogel M. Mimotope and anti-idiotypic vaccines to induce an anti-IgE response. Int Arch Allergy Immunol. 1999;118:119–21.CrossRefPubMed Stadler BM, Zürcher AW, Miescher S, Kricek F, Vogel M. Mimotope and anti-idiotypic vaccines to induce an anti-IgE response. Int Arch Allergy Immunol. 1999;118:119–21.CrossRefPubMed
21.
go back to reference Jin G, Hamaguchi Y, Matsushita T, Hasegawa M, Le Huu D, Ishiura N, et al. B-cell linker protein expression contributes to controlling allergic and autoimmune diseases by mediating IL-10 production in regulatory B cells. J Allergy Clin Immunol. 2013;131:1674–82.CrossRefPubMed Jin G, Hamaguchi Y, Matsushita T, Hasegawa M, Le Huu D, Ishiura N, et al. B-cell linker protein expression contributes to controlling allergic and autoimmune diseases by mediating IL-10 production in regulatory B cells. J Allergy Clin Immunol. 2013;131:1674–82.CrossRefPubMed
22.
go back to reference Fink K, Zellweger R, Weber J, Manjarrez-Orduno N, Holdener M, Senn BM, et al. Long-term maternal imprinting of the specific B cell repertoire by maternal antibodies. Eur J Immunol. 2008;38:90–101.CrossRefPubMed Fink K, Zellweger R, Weber J, Manjarrez-Orduno N, Holdener M, Senn BM, et al. Long-term maternal imprinting of the specific B cell repertoire by maternal antibodies. Eur J Immunol. 2008;38:90–101.CrossRefPubMed
24.
go back to reference Flicker S, Marth K, Kofler H, Valenta R. Placental transfer of allergen-specific IgG but not IgE from a specific immunotherapy-treated mother. J Allergy Clin Immunol. 2009;124:1358–60.CrossRefPubMed Flicker S, Marth K, Kofler H, Valenta R. Placental transfer of allergen-specific IgG but not IgE from a specific immunotherapy-treated mother. J Allergy Clin Immunol. 2009;124:1358–60.CrossRefPubMed
25.
go back to reference Glovsky MM, Ghekiere L, Rejzek E. Effect of maternal immunotherapy on immediate skin test reactivity, specific rye I IgG and IgE antibody, and total IgE of the children. Ann Allergy. 1991;67:21–4.PubMed Glovsky MM, Ghekiere L, Rejzek E. Effect of maternal immunotherapy on immediate skin test reactivity, specific rye I IgG and IgE antibody, and total IgE of the children. Ann Allergy. 1991;67:21–4.PubMed
Metadata
Title
Preconception allergen sensitization can induce B10 cells in offspring: a potential main role for maternal IgG
Authors
Marília Garcia de Oliveira
Luana de Mendonça Oliveira
Aline Aparecida de Lima Lira
Fábio da Ressureição Sgnotto
Alberto José da Silva Duarte
Maria Notomi Sato
Jefferson Russo Victor
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Allergy, Asthma & Clinical Immunology / Issue 1/2017
Electronic ISSN: 1710-1492
DOI
https://doi.org/10.1186/s13223-017-0195-8

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