Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection

Smits, Hermelijn H.; Hammad, Hamida; Nimwegen, Menno van; Soullié, Thomas; Willart, Monique; Lievers, Ellen; Kadouch, Jonathan; Kool, Mirjam; Oosterhoud, Janneke Kos-van; Deelder, André M.; Lambrecht, Bart N.; Yazdanbakhsh, Maria

doi:10.1016/j.jaci.2007.06.009

Cited by 152 publications

(185 citation statements)

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“…The degree to which helminths may influence allergy, however, is clearly variable between different parasite species [18], and is probably dependent upon the duration and intensity of infection [2,19], each factors that need to be taken into account in assessing this interaction.…”

Section: Introductionmentioning

confidence: 99%

Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminthHeligmosomoides polygyrus

McSorley

O'Gorman

Blair³

et al. 2012

Eur J Immunol

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Allergic asthma is less prevalent in countries with parasitic helminth infections, and mice infected with parasites such as Heligmosomoides polygyrus are protected from allergic airway inflammation. To establish whether suppression of allergy could be mediated by soluble products of this helminth, we tested H. polygyrus excretory-secretory (HES) material for its ability to impair allergic inflammation. When HES was added to sensitising doses of ovalbumin, the subsequent allergic airway response was suppressed, with ablated cell infiltration, a lower ratio of effector (CD4 + CD25 + Foxp3 − ) to regulatory (CD4 + Foxp3 + ) T (Treg) cells, and reduced Th1, Th2 and Th17 cytokine production. HES exposure reduced IL-5 responses and eosinophilia, abolished IgE production and inhibited the type 2 innate molecules arginase-1 and RELM-α (resistin-like molecule-α). Although HES contains a TGF-β-like activity, similar effects in modulating allergy were not observed when administering mammalian TGF-β alone. HES also protected previously sensitised mice, suppressing recruitment of eosinophils to the airways when given at challenge, but no change in Th or Treg cell populations was apparent. Because heat-treatment of HES did not impair suppression at sensitisation, but compromised its ability to suppress at challenge, we propose that HES contains distinct heat-stable and heat-labile immunomodulatory molecules, which modulate pro-allergic adaptive and innate cell populations.Keywords: Allergy r Eosinophils r IgE r Infection r Macrophages IntroductionAllergic asthma has dramatically increased in prevalence in developing countries, exceeding 5% of the Western European and North American populations [1]. This contrasts with much lower asthma incidence in tropical countries that have significant levels of parasite infections, and these observations have stimulated research into the effects of parasitic organisms on human allergy [2][3][4]. From these studies, it has emerged that allergic diseases are least common in parts of the world with high helminth endemicity, and that within endemic populations the prevalence of atopy is significantly lower in individuals with chronic worm infections [5][6][7][8][9][10].Correspondence: Dr. Rick M. Maizels e-mail: rick.maizels@ed.ac.ukWhile a causal link between human helminth infections and reduced allergy has yet to be proven [2], chemotherapeutic clearance of intestinal helminths can result in accentuated atopic responsiveness [11][12][13] and helminth infection blocks overt allergy in a number of animal models [14][15][16][17]. The degree to which helminths may influence allergy, however, is clearly variable between different parasite species [18], and is probably dependent upon the duration and intensity of infection [2,19], each factors that need to be taken into account in assessing this interaction.The concept that helminths may act in a beneficial way for therapy of immunological disorders is one that has been gaining * These author contributed equally to this work. Eur. J. Immunol. 20...

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Section: Introductionmentioning

confidence: 99%

Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminthHeligmosomoides polygyrus

McSorley

O'Gorman

Blair³

et al. 2012

Eur J Immunol

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“…18 In addition to epidemiological observations, experimental studies have also provided support for the hygiene hypothesis. [19][20][21][22][23][24][25][26][27][28][29][30] For example, BCG infection prevented the development of asthma-like reactions in a murine asthma model. 19,20 Some studies showed that systemic or mucosal administration of killed bacteria, introduction of bacterial CpG, and intramuscular infection with adenovirus also inhibit allergic reactions.…”

Section: Introductionmentioning

confidence: 99%

“…[35][36][37][38] Moreover, recent studies demonstrated an inhibitory effect of parasitic infections on allergy/asthma. [27][28][29][30] However, this hypothesis currently faces numerous challenges, [39][40][41][42][43][44][45] because some epidemiological studies have been performed on populations with different genetic backgrounds, culture, economic development stage, health care system and geographical location, and they have shown either no relationship between infection and allergy, especially asthma, or an increased risk of allergic asthma in association with infection. [40][41][42][43][44][45][46] In experimental models, some infections, such as acute infections, exacerbated already established allergy/ asthma or enhanced allergic reactions when the allergen and infectious agents were co-administered.…”

Section: Introductionmentioning

confidence: 99%

Role of dendritic cells: a step forward for the hygiene hypothesis

Yang

Gao

2010

Cell Mol Immunol

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The hygiene hypothesis was proposed more than two decades ago, but its mechanism remains unclear. This review focuses on recent advances in the field, especially on the role played by dendritic cells (DCs) and their modulating effects on various infections and allergic diseases, including allergic asthma. DCs isolated from mice long after the resolution of an infection were reported to have a significant modulating effect on allergen-specific Th2 responses in both in vitro and in vivo systems. These DCs showed DC1-like and/or tolerogenic DC capacity, which allowed for the inhibition of allergic responses by immune deviation (enhancing Th1 response) and immune regulation (through regulatory T-cell and Th2 hyporesponsiveness) mechanisms. These findings represented a significant advance in the elucidation of the mechanisms underlying the hygiene hypothesis. Further investigation on the mechanisms by which DCs are 'educated' by infectious agents and the influence of the type, time, and extent of infections on this 'education' process will help us understand immune regulation in disease settings and in the rational design of preventive/therapeutic approaches to allergy/asthma and infections.

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“…However, intensity and chronicity of infection are important factors that are associated with the amelioration of allergic inflammation, whereas acute infections may procure aggravation of allergic responses (4). Downmodulation of allergic inflammation has been explained as a survival strategy of worms, which is initiated to modulate inflammatory host responses directed against them.…”

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confidence: 99%

A Helminth Immunomodulator Reduces Allergic and Inflammatory Responses by Induction of IL-10-Producing Macrophages

Schnoeller

Rausch

Pillai

et al. 2008

The Journal of Immunology

228

196

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The coincidence between infections with parasitic worms and the reduced prevalence of allergic disease in humans and in animal models has prompted the search for helminth molecules with antiallergic and antiinflammatory potential. We report herein that filarial cystatin, a secreted protease inhibitor of filarial nematodes, suppresses Th2-related inflammation and the ensuing asthmatic disease in a murine model of OVA-induced allergic airway responsiveness. Treatment with recombinant filarial cystatin inhibited eosinophil recruitment, reduced levels of OVA-specific and total IgE, down-regulated IL-4 production, and suppressed allergic airway hyperreactivity when applied during or after sensitization and before challenge with the allergen. Depletion of macrophages by clodronate-containing liposomes prevented the curative effects and restored the levels of infiltrating cells, IgE, and allergic airway reactivity. Blocking of IL-10 by application of anti-IL-10 receptor Abs restored the reduced number of infiltrating cells and the levels of OVA-specific IgE. In contrast, depletion of regulatory T cells by anti-CD25 Abs had only limited effects. Cystatin also modulated macrophage-mediated inflammation in a murine model of dextran sulfate sodium-induced colitis, leading to reduction of inflammatory infiltrations and epithelial damage. Our data demonstrate that treatment with a single helminth protein can exert the antiallergic effects of helminth infections.

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Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection

Cited by 152 publications

References 37 publications

Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminthHeligmosomoides polygyrus

Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminthHeligmosomoides polygyrus

Role of dendritic cells: a step forward for the hygiene hypothesis

A Helminth Immunomodulator Reduces Allergic and Inflammatory Responses by Induction of IL-10-Producing Macrophages

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