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Helminth parasites and immune regulation

Gazzinelli-Guimaraes, Pedro H., Nutman, Thomas B.·2018·F1000Research
DOI 10.12688/f1000research.15596.1PMC PMC6206608
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Abstract

Helminth parasites are complex metazoans that belong to different taxonomic families but that collectively share the capacity to downregulate the host immune response directed toward themselves (parasite-specific immunoregulation). During long-standing chronic infection, these helminths appear able to suppress immune responses to bystander pathogens/antigens and atopic, autoimmune, and metabolic disorders. Helminth-induced immunoregulation occurs through the induction of regulatory T cells or Th2-type cells (or both). However, secreted or excreted parasite metabolites, proteins, or extracellular vesicles (or a combination of these) may also directly induce signaling pathways in host cells. Therefore, the focus of this review will be to highlight recent advances in understanding the immune responses to helminth infection, emphasizing the strategies/molecules and some of the mechanisms used by helminth parasites to modulate the immune response of their hosts.

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Figure 1. Acuteness and chronicity of helminth infection drive distinct immune profiles. Early in infection, normally during the larval migration through the lungs or intestinal mucosa, prior to adult worm development and establishment, epithelial cells secrete a group of alarmins—thymic stromal lymphopoietin (TSLP) and interleukin-33 (IL-33), including IL-25-producing tuft cells—that promote the activation and differentiation of type 2 innate lymphoid cells (ILC2) and polyfunctional CD4 T helper 2 (Th2) cells, leading to the secretion of a myriad of cytokines, including IL-4, IL-5, and IL-13. These type 2-associated cytokines result in goblet cell hyperplasia, mucus hyper-secretion, peripheral and tissue eosinophilia, and differentiation of M2 macrophages and also induce high antigen-specific IgG1 and IgE levels. Helminth early/acute responses generally associate with an allergy-like response. The persistent exposure to helminth parasites and helminth-derived excretory/secretory (ES) antigens over the course of the infection lead to a modified type 2 response resulting in a significant modulation of T helper 1 (Th1) response—IL-2 and interferon-gamma (IFN-γ)—and also induce the expansion of natural regulatory T (nTreg) cells expressing CTLA-4, PD-1, GITR, and regulatory dendritic cells (regDCs) and monocytes, which are all sources of IL-10. This same response drives B-cell class-switching to IgG4. Chronic infection with helminth also alters the composition of intestinal bacterial communities leading to more microbial-derived short chain fatty acids (SCFAs) that also activate and promote the expansion of Treg cells. Collectively, this new regulatory environment is the signature for the establishment of an asymptomatic chronic long-standing infection, characterized by a muted/anergic parasite-specific lymphoproliferative response but also a suppressed immunity to bystander pathogens, allergens, vaccines, or non-related inflammatory, autoimmune—inflammatory bowel diseases (IBDs) and type 1 diabetes (T1DM)—or metabolic diseases. DC, dendritic cell; EOS, eosinophil; EV, extracellular vesicle; TGF-β, transforming growth factor beta.
Figure 1. Acuteness and chronicity of helminth infection drive distinct immune profiles. Early in infection, normally during the larval migration through the lungs or intestinal mucosa, prior to adult worm development and establishment, epithelial cells secrete a group of alarmins—thymic stromal lymphopoietin (TSLP) and interleukin-33 (IL-33), including IL-25-producing tuft cells—that promote the activation and differentiation of type 2 innate lymphoid cells (ILC2) and polyfunctional CD4 T helper 2 (Th2) cells, leading to the secretion of a myriad of cytokines, including IL-4, IL-5, and IL-13. These type 2-associated cytokines result in goblet cell hyperplasia, mucus hyper-secretion, peripheral and tissue eosinophilia, and differentiation of M2 macrophages and also induce high antigen-specific IgG1 and IgE levels. Helminth early/acute responses generally associate with an allergy-like response. The persistent exposure to helminth parasites and helminth-derived excretory/secretory (ES) antigens over the course of the infection lead to a modified type 2 response resulting in a significant modulation of T helper 1 (Th1) response—IL-2 and interferon-gamma (IFN-γ)—and also induce the expansion of natural regulatory T (nTreg) cells expressing CTLA-4, PD-1, GITR, and regulatory dendritic cells (regDCs) and monocytes, which are all sources of IL-10. This same response drives B-cell class-switching to IgG4. Chronic infection with helminth also alters the composition of intestinal bacterial communities leading to more microbial-derived short chain fatty acids (SCFAs) that also activate and promote the expansion of Treg cells. Collectively, this new regulatory environment is the signature for the establishment of an asymptomatic chronic long-standing infection, characterized by a muted/anergic parasite-specific lymphoproliferative response but also a suppressed immunity to bystander pathogens, allergens, vaccines, or non-related inflammatory, autoimmune—inflammatory bowel diseases (IBDs) and type 1 diabetes (T1DM)—or metabolic diseases. DC, dendritic cell; EOS, eosinophil; EV, extracellular vesicle; TGF-β, transforming growth factor beta.CC BY · PubMed Central

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Metadata

Authors
Gazzinelli-Guimaraes, P. H., & Nutman, T. B.
ORCID
Gazzinelli-Guimaraes, Pedro H.
Venue
F1000Research
Publisher
F1000 Research Ltd
Published
2018-10-23
Volume
7
Pages
1685
ISSN
2046-1402
DOI
10.12688/f1000research.15596.1
PMC
PMC6206608
Cited by
145
References
7
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (unspecified)
Funders
Division of Intramural Research of the National Institutes of Health

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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