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Clinical & Experimental Allergy

Gastrointestinal nematode infection interferes with experimental allergic airway inflammation but not atopic dermatitis

Authors

  • S. Hartmann,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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    • 1Contributed equally.

  • C. Schnoeller,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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    • 1Contributed equally.

  • A. Dahten,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • A. Avagyan,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • S. Rausch,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • M. Lendner,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • C. Bocian,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • S. Pillai,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • C. Loddenkemper,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • R. Lucius,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • M. Worm,

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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  • E. Hamelmann

    1. * Department of Molecular Parasitology, Humboldt-University Berlin, Berlin, Germany, Center for Respiratory Infections, National Heart and Lung Institute, St. Mary's Campus, Imperial College London, UK, Department of Dermatology and Allergy, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, § Department of Paediatrics, Allergy-Center-Charité, Charité Universitätsmedizin Berlin, Berlin, Germany, Pathology/RCIS, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany University Children's Hospital, Ruhr-University Bochum, Bochum, Germany
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Correspondence:
Dr Susanne Hartmann, Department of Molecular Parasitology, Humboldt-University Berlin, Philippstr. 13, 10115 Berlin, Germany.
E-mail: susanne.hartmann@hu-berlin.de

Summary

Background Some helminth infections are negatively associated with the prevalence of allergic disorders, arguing for a modulation of allergic reactions by the parasites, depending on the worm species, intensity and phase of infection and the type of disease.

Objective The aim of this study was to analyse the influence of a chronic infection with the gastrointestinal nematode Heligmosomoides polygyrus, in a murine model of allergic airway disease and of atopic dermatitis (AD), respectively.

Methods Mice were infected with H. polygyrus and systemically sensitized with the model allergen ovalbumin. Subsequently, the animals were challenged with the allergen either via the airways for induction of airway disease, or via skin patches for induction of dermatitis.

Results Mice concomitantly infected with H. polygyrus showed diminished eosinophil and lymphocyte recruitment into the lungs and decreased allergen-specific IgE levels when compared with sensitized and airway challenged controls. In addition, animals showed a trend towards reduced airway hyper-reactivity. In contrast, no significant differences in the severity of eczematous skin lesions were observed between infected and control animals in the AD model. Although H. polygyrus infection reduced CD8+ and CD4+ T-cell infiltration into the skin and production of allergen-specific IgE, mast cell recruitment was significantly increased in worm-infected mice in the dermatitis model. The worm infection was associated with significantly elevated numbers of Foxp3+ regulatory T cells (Treg) in peribronchial lymph nodes in H. polygyrus-infected sensitized and airway challenged mice. In contrast, Treg cells were basically absent in eczematous skin and their number was not increased in skin-draining lymph nodes of mice with experimental dermatitis.

Conclusion Infection with the gastrointestinal nematode used in our study leads to significant inhibition of mucosa-associated but not cutaneous allergic reactions, pointing to a site specificity of the immunomodulation exerted by helminths. This finding might be an important aspect for future considerations of helminths for treatment of allergic diseases.

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