Prenatal exposure to a farm environment modifies atopic sensitization at birth

Ege, Markus; Herzum, Ileana; Büchele, Gisela; Krauss‐Etschmann, Susanne; Lauener, Roger; Roponen, Marjut; Hyvärinen, Anne; Vuitton, Dominique A.; Riedler, Josef; Brunekreef, Bert; Dalphin, Jean‐Charles; Braun‐Fahrländer, Charlotte; Pekkanen, Juha; Renz, Harald; Mutius, Erika von

doi:10.1016/j.jaci.2008.06.011

Cited by 162 publications

(113 citation statements)

References 26 publications

(29 reference statements)

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“…However, a role of IL-10 in transplacental immune regulation has not been reported so far. Previous studies exploring the effect of maternal influence on development of atopy in offspring have mainly focused on Th1 and Th2 cytokines such as IFN-g and IL-4 (5,6,8,9). Our finding that serum IL-10 levels were significantly correlated between mother and fetus was surprising, but perhaps related to a previous report showing that maternal IL-10 levels were significantly associated with the offspring's IL-10 level at 1 y of age (28).…”

Section: Discussioncontrasting

confidence: 40%

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Fetal–Maternal Alignment of Regulatory T Cells Correlates with IL-10 and Bcl-2 Upregulation in Pregnancy

Santner-Nanan

Straubinger

Hsu

et al. 2013

The Journal of Immunology

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Transplacental immune regulation refers to the concept that during pregnancy, significant cross-talk occurs between the maternal and fetal immune system with potential long-term effects for both the mother and child. In this study, we made the surprising observation that there is a strong correlation of peripheral blood regulatory T (Treg) cells between the mother and the fetus. In contrast, there is no significant Treg cell correlation between paternal fetal dyads (pairs), suggesting that the specific context of pregnancy, rather than the genetic parental similarity to the fetus, is responsible for this correlation. Gene microarray analysis of Treg cells identified a typical IL-10–dependent signature in maternal and fetal Treg cells. In addition, a direct correlation of serum IL-10 protein levels between maternal fetal dyads was observed. Furthermore, we show that maternal serum IL-10 levels correlate with serum estradiol and estriol, implicating hormonal involvement in this alignment. Interestingly, we show that Treg cells possess higher expression of IL-10 receptor α and that Treg cell IL-10 receptor α expression directly correlates with their Bcl-2 expression. Indeed, in vitro data in both humans and mice demonstrate that IL-10 upregulates Bcl-2 specifically in Treg cells but not non-Treg cells. Our results provide evidence for transplacental regulation of cellular immunity and suggest that IL-10 may influence Treg cell homeostasis through its effect on Treg cell Bcl-2 expression. These novel findings have important implications on immune tolerance in pregnancy and beyond in areas of autoimmunity, allergy, and transplantation.

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Section: Discussioncontrasting

confidence: 40%

“…In humans, cord blood cytokine levels have been linked to subsequent development of atopy (5). Maternal exposure to farm environment during pregnancy also reduces atopic sensitization of the offspring (6); this appears to be in part mediated through an increase of fetal Treg cells (7).…”

mentioning

confidence: 99%

Fetal–Maternal Alignment of Regulatory T Cells Correlates with IL-10 and Bcl-2 Upregulation in Pregnancy

Santner-Nanan

Straubinger

Hsu

et al. 2013

The Journal of Immunology

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“…The nature and extent of innate and acquired immune responses to respiratory pathogens and allergens are influenced genetically and developmentally and by exposure to specific pathogens and toxicants. There is increasing evidence that pulmonary immune responses are initiated early in development, in utero, and during infancy (6)(7)(8)(9)(10). Mechanisms by which early exposures of the lung to pathogens instruct the acquisition of innate and acquired immunity are of considerable interest.…”

Section: Introductionmentioning

confidence: 99%

Airway epithelial SPDEF integrates goblet cell differentiation and pulmonary Th2 inflammation

Rajavelu¹,

Chen²,

Xu³

et al. 2015

J. Clin. Invest.

133

118

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“…In animal models, maternal Th1 type cytokines during gestation were shown to contribute to the reduction of experimental allergic airway disease in the newborn (20). Similarly, in humans, maternal exposure to Th1 type cytokines during gestation alleviates atopic sensitization of the offspring (21,22). Intriguingly, maternal cytokine levels (e.g., tumor necrosis factor alpha [TNF-␣], monocyte chemoattractant protein 1 [MCP-1], and interleukin-10 [IL-10]) during gestation correlate with the newborn's cytokine levels at up to 1 year of age (23), reinforcing the synchronized polarization of the maternal and fetal immune systems.…”

mentioning

confidence: 99%

Protective Role of Passively Transferred Maternal Cytokines against Bordetella pertussis Infection in Newborn Piglets

et al. 2017

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Maternal vaccination represents a potential strategy to protect both the mother and the offspring against life-threatening infections. This protective role has mainly been associated with antibodies, but the role of cell-mediated immunity, in particular passively transferred cytokines, is not well understood. Here, using a pertussis model, we have demonstrated that immunization of pregnant sows with heat-inactivated bacteria leads to induction of a wide range of cytokines (e.g., tumor necrosis factor alpha [TNF-␣], gamma interferon [IFN-␥], interleukin-6 [IL-6], IL-8, and IL-12/IL-23p40) in addition to pertussis-specific antibodies. These cytokines can be detected in the sera and colostrum/milk of vaccinated sows and subsequently were detected at significant levels in the serum and bronchoalveolar lavage fluid of piglets born to vaccinated sows together with pertussis-specific antibodies. In contrast, active vaccination of newborn piglets with heat-inactivated bacteria induced high levels of specific IgG and IgA but no cytokines. Although the levels of antibodies in vaccinated piglets were comparable to those of passively transferred antibodies, no protection against Bordetella pertussis infection was observed. Thus, our results demonstrate that a combination of passively transferred cytokines and antibodies is crucial for disease protection. The presence of passively transferred cytokines/antibodies influences the cytokine secretion ability of splenocytes in the neonate, which provides novel evidence that maternal immunization can influence the newborn's cytokine milieu and may impact immune cell differentiation (e.g., Th1/Th2 phenotype). Therefore, these maternally derived cytokines may play an essential role both as mediators of early defense against infections and possibly as modulators of the immune repertoire of the offspring.

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Prenatal exposure to a farm environment modifies atopic sensitization at birth

Cited by 162 publications

References 26 publications

Fetal–Maternal Alignment of Regulatory T Cells Correlates with IL-10 and Bcl-2 Upregulation in Pregnancy

Fetal–Maternal Alignment of Regulatory T Cells Correlates with IL-10 and Bcl-2 Upregulation in Pregnancy

Airway epithelial SPDEF integrates goblet cell differentiation and pulmonary Th2 inflammation

Protective Role of Passively Transferred Maternal Cytokines against Bordetella pertussis Infection in Newborn Piglets

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