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

Straubinger, Kathrin; PAUL, S.; Costa, Olivia Prazeres da; Ritter, Manuel; Buch, Thorsten; Busch, Dirk H.; Layland, Laura E.; Costa, Clarissa U. Prazeres da

doi:10.1016/j.jaci.2014.05.034

Cited by 57 publications

(64 citation statements)

References 42 publications

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“…Similarly, sensitization with OVA (CFA), and re-exposure to OVA during pregnancy limited the development of OVA-specific IgE and pulmonary eosinophilia in offspring of exposed mothers 50 . Contrary to this protective effect, our observations of increased asthma development in offspring of HDM-exposed mothers are consistent with reports showing increased asthma development in offspring following maternal OVA (alum) sensitization and challenge 29–32 , maternal Aspergillus fumigatus -exposure 33 , and in Schistosoma mansoni -infected mothers impregnated during the Th2 phase of the anti-helminthic response 21 . Blockade of IL-4 during pregnancy completely abrogated the increased sensitivity of offspring of following maternal OVA (alum) sensitization and challenge 30 , again suggesting maternal cytokines can influence offspring asthma.…”

Section: Discussionsupporting

confidence: 92%

“…However, maternal exposures have been reported to influence, both positively and negatively, the development of asthma in other animal models. For example, if Schistosoma mansoni -infected mothers were impregnated during the systemic Th1 phase of the infection, offspring were found to be protected from development of asthma 21 . Anti-IFNγ abrogated this protective effect of maternal Schistosoma mansoni infection, suggesting that maternal cytokines can influence asthma development in offspring 21 .…”

Section: Discussionmentioning

confidence: 99%

“…For example, if Schistosoma mansoni -infected mothers were impregnated during the systemic Th1 phase of the infection, offspring were found to be protected from development of asthma 21 . Anti-IFNγ abrogated this protective effect of maternal Schistosoma mansoni infection, suggesting that maternal cytokines can influence asthma development in offspring 21 . Feeding female mice OVA prior to pregnancy to induce tolerance protects from the development of OVA-induced allergic airway disease in an FcRn and IFNγ-dependent manner 49 .…”

Section: Discussionmentioning

confidence: 99%

“…This critical developmental window appears to extend into the prenatal period as well, as in utero exposures to these factors also influence asthma risk 13, 15–18 , as do alterations in maternal diet 19, 20 . Similarly, infection with the helminthic parasite Schistosoma mansoni increases development of asthma in offspring if pregnancy was initiated during the “Th2 phase” of the anti-parasitic immune response 21 . Consistent with the existence of such a “prenatal window”, maternal asthma is a risk factor for the development of asthma, whereas paternal asthma does not confer as great a risk 22–26 suggesting that maternal exposures/factors can contribute to asthma development.…”

Section: Introductionmentioning

confidence: 99%

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Maternal house dust mite exposure during pregnancy enhances severity of house dust mite–induced asthma in murine offspring

Richgels

Yamani

Chougnet

et al. 2017

Journal of Allergy and Clinical Immunology

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Background Atopic status of the mother and maternal exposure to environmental factors is associated with increased asthma risk. Moreover, animal models demonstrate that exposure to allergens in strongly sensitized mothers influences offspring asthma development, suggesting that in utero exposures can influence offspring asthma. However, it is unclear whether maternal exposure to common human allergens like house dust mite (HDM), in the absence of additional adjuvants, influences offspring asthma development. Objective To determine if maternal HDM exposure influences asthma development in offspring. Methods Pregnant female mice were exposed to PBS or HDM during pregnancy. Using offspring of PBS or HDM-exposed mothers, the magnitude of HDM or Aspergillus fumigatus (AF) extract-induced airway hyperresponsiveness (AHR), airway inflammation, immunoglobulin production, Th2-associated cytokine synthesis and pulmonary dendritic cell activity was assessed. Results Compared to offspring of PBS-exposed mothers, offspring of HDM-exposed mothers demonstrate increased AHR, airway inflammation, Th2 cytokine production, immunoglobulin levels and a modest decrease in the phagocytic capacity of pulmonary macrophage populations following HDM exposure. Increased sensitivity to AF-induced airway disease was not observed. Offspring of HDM-exposed B cell deficient mothers also demonstrated increased HDM-induced AHR, suggesting transfer of maternal immunoglobulins is not required. Conclusions Our data demonstrate that maternal exposure to HDM during pregnancy increases asthma sensitivity in offspring in an HDM-specific manner, suggesting that vertical transmission of maternal immune responses may be involved. These findings have important implications for regulation of asthma risk, and suggest that exposure to HDM in the developed world may have under-appreciated influences on the overall prevalence of allergic asthma.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Maternal house dust mite exposure during pregnancy enhances severity of house dust mite–induced asthma in murine offspring

Richgels

Yamani

Chougnet

et al. 2017

Journal of Allergy and Clinical Immunology

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“…39 Recent mouse model studies have demonstrated that prenatal helminth (ie, schistosome) infection can prevent the induction of the allergic asthma phenotype only if pregnancy occurred during the T H 1 phases of the infection (eg, chronic) and in a maternal IFN-g-dependent manner, but not if pregnancy occurred during the acute T H 2 phase of infection. 40 …”

Section: Importance Of Early Lifementioning

confidence: 99%

Revisiting the hygiene hypothesis for allergy and asthma

Liu

2015

Journal of Allergy and Clinical Immunology

137

109

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The hygiene hypothesis, which describes the protective influence of microbial exposures in early life on the development of allergy and asthma, has continued its swell of academic interest, investigation, and evolution. This article is focused on studies published in the past 3 years that have furthered the substance and shape of hygiene theory, primarily as it relates to allergic airways and asthma. Recent investigations have furthered an overarching "microbiome hypothesis" to home features, medical practices, and cleanliness behaviors that are suspects in the hygiene effect. Relatively crude markers of the protective microbial environment have been supplanted by culture-independent microbiome science, distinguishing the characteristics of potentially protective microbiomes from pathologic features. Understanding how the microbiome is shaped and affects healthful versus harmful outcomes in the human host is relatively nascent. Good clues are emerging that give mechanistic substance to the theory and could help guide microbe-based therapeutics to fill the allergy and asthma management gap in prevention and disease modification.

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Chronic schistosomiasis during pregnancy epigenetically reprograms T‐cell differentiation in offspring of infected mothers

et al. 2017

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Schistosomiasis is a nontransplacental helminth infection. Chronic infection during pregnancy suppresses allergic airway responses in offspring.We addressed the question whether in utero exposure to chronic schistosome infection (Reg phase) in mice affects B-cell and T-cell development. Therefore, we focused our analyses on T-cell differentiation capacity induced by epigenetic changes in promoter regions of signature cytokines in offspring. Here, we show that naïve T cells from offspring of schistosome infected female mice had a strong capacity to differentiate into T H 1 cells, whereas T H 2 differentiation was impaired. In accordance, reduced levels of histone acetylation of the IL-4 promoter regions were observed in naïve T cells. To conclude, our mouse model revealed distinct epigenetic changes within the naïve T-cell compartment affecting T H 2 and T H 1 cell differentiation in offspring of mothers with chronic helminth infection. These findings could eventually help understand how helminths alter T-cell driven immune responses induced by allergens, bacterial or viral infections, as well as vaccines.Keywords: Epigenetic histone modification r In utero programming r Maternal helminth infection r Schistosomiasis r T-cell differentiation Additional supporting information may be found in the online version of this article at the publisher's web-site Over the last century and in strong contrast to developing countries, a continuous rise in allergic diseases, such as asthma, is observed in industrialized countries [1]. It is currently discussed whether helminthic parasites contribute to the low prevalence of allergic diseases in parasite endemic areas [2] due to their well-known ability to suppress bystander immune responses * These authors contributed equally to this work.

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

Cited by 57 publications

References 42 publications

Maternal house dust mite exposure during pregnancy enhances severity of house dust mite–induced asthma in murine offspring

Maternal house dust mite exposure during pregnancy enhances severity of house dust mite–induced asthma in murine offspring

Revisiting the hygiene hypothesis for allergy and asthma

Chronic schistosomiasis during pregnancy epigenetically reprograms T‐cell differentiation in offspring of infected mothers

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