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Regulation of immunity and allergy by helminth parasites

Maizels, Rick M.·2020·Allergy
DOI 10.1111/all.13944
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Abstract

There is increasing interest in helminth parasite modulation of the immune system, both from the fundamental perspective of the “arms race” between host and parasite, and equally importantly, to understand if parasites offer new pathways to abate and control untoward immune responses in humans. This article reviews the epidemiological and experimental evidence for parasite down‐regulation of host immunity and immunopathology, in allergy and other immune disorders, and recent progress towards defining the mechanisms and molecular mediators which parasites exploit in order to modulate their host. Among these are novel products that interfere with epithelial cell alarmins, dendritic cell activation, macrophage function and T‐cell responsiveness through the promotion of an immunoregulatory environment. These modulatory effects assist parasites to establish and survive, while dampening immune reactivity to allergens, autoantigens and microbiome determinants.

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FIGURE 1 Early and late acting influences on the immune system which may underpin the Hygiene Hypothesis. Maternal infection status can influence the development of allergy in offspring, with further early-life effects resulting from neonatal infections that may either promote tolerance or sensitize the newborn host. Changes in diet at weaning and the use of antibiotics in infancy can alter the microbiome, with potential lifelong consequences. In later life, the mature immune system may also be modulated by infectious agents, particularly those such as helminths which exert immunosuppressive effects and activate the immune regulatory network. Thus, prevention of allergy may require intervention in the maternal and early-life environment, while therapy can exploit helminth products to dampen established allergic diseases
FIGURE 1 Early and late acting influences on the immune system which may underpin the Hygiene Hypothesis. Maternal infection status can influence the development of allergy in offspring, with further early-life effects resulting from neonatal infections that may either promote tolerance or sensitize the newborn host. Changes in diet at weaning and the use of antibiotics in infancy can alter the microbiome, with potential lifelong consequences. In later life, the mature immune system may also be modulated by infectious agents, particularly those such as helminths which exert immunosuppressive effects and activate the immune regulatory network. Thus, prevention of allergy may require intervention in the maternal and early-life environment, while therapy can exploit helminth products to dampen established allergic diseasesCC-BY · From the PDF
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FIGURE 2 Pathways of allergic inflammation and helminth immune modulation. Helminths may penetrate and damage epithelial tissue, releasing parasite PAMPs (pathogen-associated molecular patterns) and host DAMPs (damage-associated molecular patterns). Type 2 inflammation (coloured red) is initiated in response to DAMPs/PAMPs, together with antigen presentation by dendritic cells (DCs), to generate type 2 innate lymphoid cells (ILC2) and helper T cells (Th2). Type 2 lymphocytes induce allergic mediators including eosinophils and IgE from B cells. In the presence of an immunomodulatory helminth, a regulatory network is invoked (coloured green) and DCs may instead induce regulatory T cells (Tregs) that produce suppressive cytokines (IL-10 and TGF-beta). These act on B cells to switch to IgG4 production, on macrophages to assume an anti-inflammatory (M2) phenotype, and on effector Th2 cells to block activation and develop a state of tolerance. These pathways inhibit both helminth-specific and bystander (eg allergen-specific) reactivity, thereby creating a profound anti-inflammatory effect
FIGURE 2 Pathways of allergic inflammation and helminth immune modulation. Helminths may penetrate and damage epithelial tissue, releasing parasite PAMPs (pathogen-associated molecular patterns) and host DAMPs (damage-associated molecular patterns). Type 2 inflammation (coloured red) is initiated in response to DAMPs/PAMPs, together with antigen presentation by dendritic cells (DCs), to generate type 2 innate lymphoid cells (ILC2) and helper T cells (Th2). Type 2 lymphocytes induce allergic mediators including eosinophils and IgE from B cells. In the presence of an immunomodulatory helminth, a regulatory network is invoked (coloured green) and DCs may instead induce regulatory T cells (Tregs) that produce suppressive cytokines (IL-10 and TGF-beta). These act on B cells to switch to IgG4 production, on macrophages to assume an anti-inflammatory (M2) phenotype, and on effector Th2 cells to block activation and develop a state of tolerance. These pathways inhibit both helminth-specific and bystander (eg allergen-specific) reactivity, thereby creating a profound anti-inflammatory effectCC-BY · From the PDF
FIGURE 3 Illustration of pathways of immune interference by the model helminth parasite H polygyrus mediated by the excretorysecretory products (HES) and 2 newly defined components. One, Hp-ARI, targets innate immunity by neutralizing IL-33, thereby forestalling activation of ILC2, eosinophils and M2 macrophages. 103 A second, TGM, activates the TGFβ pathway to induce regulatory T cells 155 ; these suppress the adaptive Th2 arm of immunity, further inhibiting M2 macrophage induction and the differentiation of epithelial effector populations such as the goblet cells. In these ways, the parasite prevents both outcomes of the Th2 response, namely allergic inflammation and helminth expulsion
FIGURE 3 Illustration of pathways of immune interference by the model helminth parasite H polygyrus mediated by the excretorysecretory products (HES) and 2 newly defined components. One, Hp-ARI, targets innate immunity by neutralizing IL-33, thereby forestalling activation of ILC2, eosinophils and M2 macrophages. 103 A second, TGM, activates the TGFβ pathway to induce regulatory T cells 155 ; these suppress the adaptive Th2 arm of immunity, further inhibiting M2 macrophage induction and the differentiation of epithelial effector populations such as the goblet cells. In these ways, the parasite prevents both outcomes of the Th2 response, namely allergic inflammation and helminth expulsionCC-BY · From the PDF
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Metadata

Authors
Maizels, R. M.
Venue
Allergy
Publisher
Wiley
Published
2019-07-18
Volume
75
Issue
3
Pages
524-534
ISSN
  • 0105-4538
  • 1398-9995
DOI
10.1111/all.13944
Cited by
162
References
11
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
Wellcome Trust (106122)

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Maizels, R. M. (2020). Regulation of immunity and allergy by helminth parasites. Allergy. https://doi.org/10.1111/all.13944