Ascaris suum infection modulates inflammation: Implication of CD4+ CD25high Foxp3+ T cells and IL‐10

Titz, Tiago de Oliveira; Araújo, Claudia Andréa Alves de; Enobe, C. S.; Rigato, Paula Ordonhez; Oshiro, Telma Miyuki; Macedo-Soares, Maria Fernanda

doi:10.1111/pim.12453

Cited by 10 publications

(8 citation statements)

References 60 publications

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“…69,70 In both studies, mice were injected with 1 lg LPS with or without PCF supplementation into an air pouch and the researchers observed that helminth PCF prevented LPS-induced leukocyte influx and suppressed pro-inflammatory cytokine (IL-1b, TNF-a and IL-6) secretion. 69,70 In both studies, mice were injected with 1 lg LPS with or without PCF supplementation into an air pouch and the researchers observed that helminth PCF prevented LPS-induced leukocyte influx and suppressed pro-inflammatory cytokine (IL-1b, TNF-a and IL-6) secretion.…”

Section: Discussionmentioning

confidence: 99%

“…Contrasting the probable induction of Th2 immune responses in humans, two mouse studies strongly support the potential of helminth PCF to induce robust Treg cell responses as well as increased IL-10 levels during LPS-induced inflammatory conditions. 69,70 In both studies, mice were injected with 1 lg LPS with or without PCF supplementation into an air pouch and the researchers observed that helminth PCF prevented LPS-induced leukocyte influx and suppressed pro-inflammatory cytokine (IL-1b, TNF-a and IL-6) secretion. Furthermore, helminth PCF supplementation has also been shown to induce Treg cells during non-LPS-induced inflammatory conditions.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, helminth PCF supplementation has also been shown to induce Treg cells during non-LPS-induced inflammatory conditions. 15,16 Although we did not focus on the chemical composition of the helminth PCF, it seems that both protein 69,70 and glycan 68,71 structures in PCF could be responsible for their immunoregulatory potential. Notably, the metabolite succinate has been shown to be secreted by the helminth Nippostrongylus brasiliensis.…”

Section: Discussionmentioning

confidence: 99%

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Body fluid from the parasitic worm Ascaris suum inhibits broad‐acting pro‐inflammatory programs in dendritic cells

et al. 2019

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Dendritic cells (DCs) are essential for generating T-cell-based immune responses through sensing of potential inflammatory and metabolic cues in the local environment. However, there is still limited insight into the processes defining the resultant DC phenotype, including the type of early transcriptional changes in pro-inflammatory cues towards regulatory or type 2 immune-based cues induced by a variety of exogenous and endogenous molecules. Here we compared the ability of a selected number of molecules to modulate the pro-inflammatory phenotype of lipopolysaccharide (LPS) and interferon-c (IFN-c)-stimulated human monocytederived DCs towards an anti-inflammatory or regulatory phenotype, including Ascaris suum body fluid [helminth pseudocoelomic fluid (PCF)], the metabolites succinate and butyrate, and the type 2 cytokines thymic stromal lymphopoietin and interleukin-25. Our data show that helminth PCF and butyrate treatment suppress the T helper type 1 (Th1)inducing pro-inflammatory DC phenotype through induction of different transcriptional programs in DCs. RNA sequencing indicated that helminth PCF treatment strongly inhibited the Th1 and Th17 polarizing ability of LPS + IFN-c-matured DCs by down-regulating myeloid differentiation primary response gene 88 (MyD88)-dependent and MyD88-independent pathways in Toll-like receptor 4 signaling. By contrast, butyrate treatment had a strong Th1-inhibiting action, and transcripts encoding important gut barrier defending factors such as IL18, IL1B and CXCL8 were up-regulated. Collectively, our results further understanding of how compounds from parasites and gut microbiota-derived butyrate may exert immunomodulatory effects on the host immune system.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Body fluid from the parasitic worm Ascaris suum inhibits broad‐acting pro‐inflammatory programs in dendritic cells

et al. 2019

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“…The mechanisms of the immune down‐regulatory effects of A. suum infection have been recently explored in a LPS‐induced inflammatory response in mice, finding that infection suppressed secretion of pro‐inflammatory cytokines (IL‐1β, TNF‐α and IL‐6) and induces high levels of IL‐10 and TGF‐β, as well as CD4 + CD25high, Foxp3 + T cells in the mesenteric lymph nodes. This has also investigated in pigs using transcriptomic analysis, showing that chronic A. suum infection induces suppression of inflammatory pathways in the intestinal mucosa, down‐regulating genes encoding cytokines, as well as antigen‐processing and co‐stimulatory molecules.…”

Section: Immunological and Clinical Influences Of Ascariasis On Asthmamentioning

confidence: 99%

Ascariasis as a model to study the helminth/allergy relationships

Caraballo

Acevedo

Zakzuk

2018

Parasite Immunology

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Summary Ascariasis is the most frequent soil transmitted helminthiasis and, as well as other helminth infections, is expected to influence the clinical presentation of allergic diseases such as asthma. Indeed, several clinical and experimental works have shown an important impact either increasing or suppressing symptoms, and the same effects have been detected on the underlying immune responses. In this review we analyze the work on this field performed in Colombia, a Latin American tropical country, including aspects such as the molecular genetics of the IgE response to Ascaris; the allergenic activity of Ascaris IgE‐binding molecular components and the immunological and clinical influences of ascariasis on asthma. The analysis allows us to conclude that the impact of ascariasis on the inception and evolution of allergic diseases such as asthma deserves more investigation, but advances have been made during the last years. The concurrent parasite‐induced immunostimulatory and immunosuppressive effects during this helminthiasis do modify the natural history of asthma and some aspects of the practice of allergology in the tropics. Theoretically it can also influence the epidemiological trends of allergic diseases either by its absence or presence in different regions and countries.

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“…The mechanisms of the immune downregulatory effects of A. suum infection have been recently explored in LPS (Lipopolysaccharide)-induced inflammatory responses in mice [25], finding that infection suppressed secretion of pro-inflammatory cytokines (IL-1β, TNF-α, and IL-6) and induced high levels of IL-10 and TGF-β as well as CD4+CD25highFoxp3+ T cells in the mesenteric lymph nodes. This has also been investigated in pigs using transcriptomic analysis, showing that chronic A. suum infection induces suppression of inflammatory pathways in the intestinal mucosa, downregulating genes encoding cytokines and antigen-processing and co-stimulatory molecules.…”

Section: Helminth-driven Immunomodulationmentioning

confidence: 99%

The tropics, helminth infections and hygiene hypotheses

Caraballo

2018

Expert Review of Clinical Immunology

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The Tropics is very appropriate to test the hypotheses raised to explain the increasing trends of allergy and other inflammatory diseases worldwide. The absence of parasite infection as a possible cause of the increase of allergic diseases was proposed by J. Gerrard a long time ago; however, the idea that helminth infections, which induce a strong Th2 could reduce allergy symptoms seems counterintuitive; but the fact is that they have a dual effect: they increase the Th2 responses but also exert immunosuppression and both effects influence the symptoms of allergy. Basic experimentation has provided valuable information about the mechanisms of allergic inflammation and more recently, about its control by helminth induced immunomodulation, discovering helminth molecules with anti-inflammatory properties that are meant to replace the live helminth therapeutic approaches. The immunosuppressive power of helminths makes them excellent candidates to be considered in the hygiene hypotheses. Future comprehensive studies evaluating simultaneously the role of microbial infections, helminth infections, microbiota, pollution and biodiversity will help to elucidate the causes of the increasing trends of allergic disorders. Doing this in the tropics, where all these variables are still present could be difficult but no doubt that will be more informative. ARTICLE HISTORY

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Ascaris suum infection modulates inflammation: Implication of CD4⁺ CD25^high Foxp3⁺ T cells and IL‐10

Cited by 10 publications

References 60 publications

Body fluid from the parasitic worm Ascaris suum inhibits broad‐acting pro‐inflammatory programs in dendritic cells

Body fluid from the parasitic worm Ascaris suum inhibits broad‐acting pro‐inflammatory programs in dendritic cells

Ascariasis as a model to study the helminth/allergy relationships

The tropics, helminth infections and hygiene hypotheses

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