Basophil-derived IL-4 promotes epicutaneous antigen sensitization concomitant with the development of food allergy
Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced aller...
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| Veröffentlicht in: | Journal of allergy and clinical immunology Jg. 141; H. 1; S. 223 - 234.e5 |
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| Hauptverfasser: | , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
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United States
Elsevier Inc
01.01.2018
Elsevier Limited |
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| ISSN: | 0091-6749, 1097-6825, 1097-6825 |
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| Abstract | Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood.
We sought to test the role of basophil-intrinsic IL-4 production in TH2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut.
Mice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for TH2 polarization and the pathogenesis of IgE-mediated food allergy was assessed in vitro by using coculture experiments with naive T cells and in vivo by using Il4 3′UTR mice that selectively lack IL-4 production in basophils.
Epicutaneous food antigen sensitization is associated with infiltration of IL-4–competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4–competent basophils together with dendritic cells and naive T cells was sufficient to promote TH2 polarization in an IL-4–dependent manner in vitro, whereas absence of basophil-intrinsic IL-4 production in vivo was associated with reduced food-induced allergic responses.
TSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP–basophil–IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites.
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| AbstractList | Background Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood. Objective We sought to test the role of basophil-intrinsic IL-4 production in TH2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut. Methods Mice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for TH2 polarization and the pathogenesis of IgE-mediated food allergy was assessedin vitroby using coculture experiments with naive T cells andin vivoby usingIl4 3′UTRmice that selectively lack IL-4 production in basophils. Results Epicutaneous food antigen sensitization is associated with infiltration of IL-4-competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4-competent basophils together with dendritic cells and naive T cells was sufficient to promote TH2 polarization in an IL-4-dependent mannerin vitro, whereas absence of basophil-intrinsic IL-4 productionin vivowas associated with reduced food-induced allergic responses. Conclusion TSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP-basophil-IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites. Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood. We sought to test the role of basophil-intrinsic IL-4 production in T 2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut. Mice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for T 2 polarization and the pathogenesis of IgE-mediated food allergy was assessed in vitro by using coculture experiments with naive T cells and in vivo by using Il4 3'UTR mice that selectively lack IL-4 production in basophils. Epicutaneous food antigen sensitization is associated with infiltration of IL-4-competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4-competent basophils together with dendritic cells and naive T cells was sufficient to promote T 2 polarization in an IL-4-dependent manner in vitro, whereas absence of basophil-intrinsic IL-4 production in vivo was associated with reduced food-induced allergic responses. TSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP-basophil-IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites. Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood.BACKGROUNDExaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood.We sought to test the role of basophil-intrinsic IL-4 production in TH2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut.OBJECTIVEWe sought to test the role of basophil-intrinsic IL-4 production in TH2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut.Mice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for TH2 polarization and the pathogenesis of IgE-mediated food allergy was assessed in vitro by using coculture experiments with naive T cells and in vivo by using Il4 3'UTR mice that selectively lack IL-4 production in basophils.METHODSMice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for TH2 polarization and the pathogenesis of IgE-mediated food allergy was assessed in vitro by using coculture experiments with naive T cells and in vivo by using Il4 3'UTR mice that selectively lack IL-4 production in basophils.Epicutaneous food antigen sensitization is associated with infiltration of IL-4-competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4-competent basophils together with dendritic cells and naive T cells was sufficient to promote TH2 polarization in an IL-4-dependent manner in vitro, whereas absence of basophil-intrinsic IL-4 production in vivo was associated with reduced food-induced allergic responses.RESULTSEpicutaneous food antigen sensitization is associated with infiltration of IL-4-competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4-competent basophils together with dendritic cells and naive T cells was sufficient to promote TH2 polarization in an IL-4-dependent manner in vitro, whereas absence of basophil-intrinsic IL-4 production in vivo was associated with reduced food-induced allergic responses.TSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP-basophil-IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites.CONCLUSIONTSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP-basophil-IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites. Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood. We sought to test the role of basophil-intrinsic IL-4 production in TH2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut. Mice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for TH2 polarization and the pathogenesis of IgE-mediated food allergy was assessed in vitro by using coculture experiments with naive T cells and in vivo by using Il4 3′UTR mice that selectively lack IL-4 production in basophils. Epicutaneous food antigen sensitization is associated with infiltration of IL-4–competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4–competent basophils together with dendritic cells and naive T cells was sufficient to promote TH2 polarization in an IL-4–dependent manner in vitro, whereas absence of basophil-intrinsic IL-4 production in vivo was associated with reduced food-induced allergic responses. TSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP–basophil–IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites. [Display omitted] Background Exaggerated thymic stromal lymphopoietin (TSLP) production and infiltration of basophils are associated with the pathogenesis of atopic dermatitis (AD), a recognized risk factor for the development of food allergies. Although TSLP and basophils have been implicated in promotion of food-induced allergic disorders in response to epicutaneous sensitization, the mechanisms by which TSLP-elicited basophils guide the progression of allergic inflammation in the skin to distant mucosal sites, such as the gastrointestinal tract, are poorly understood. Objective We sought to test the role of basophil-intrinsic IL-4 production in TH 2 sensitization to food antigens in the skin and effector food-induced allergic responses in the gut. Methods Mice were epicutaneously sensitized with ovalbumin on an AD-like skin lesion, followed by intragastric antigen challenge to induce IgE-mediated food allergy. The requirement for basophil-derived IL-4 production for TH 2 polarization and the pathogenesis of IgE-mediated food allergy was assessed in vitro by using coculture experiments with naive T cells and in vivo by using Il4 3′UTR mice that selectively lack IL-4 production in basophils. Results Epicutaneous food antigen sensitization is associated with infiltration of IL-4–competent innate immune cells to the skin, with basophils and eosinophils representing the predominant populations. In contrast to basophils, absence of eosinophils did not alter disease outcome. Coculture of IL-4–competent basophils together with dendritic cells and naive T cells was sufficient to promote TH 2 polarization in an IL-4–dependent manner in vitro , whereas absence of basophil-intrinsic IL-4 production in vivo was associated with reduced food-induced allergic responses. Conclusion TSLP-elicited basophils promote epicutaneous sensitization to food antigens and subsequent IgE-mediated food allergy through IL-4. Strategies to target the TSLP–basophil–IL-4 axis in patients with AD might lead to innovative therapies that can prevent the progression of allergies to distant mucosal sites. |
| Author | Mueller, Christoph Hussain, Maryam Pena Rodriguez, Maria Noti, Mario Artis, David Borcard, Loïc Walsh, Kevin P. Kim, Brian S. Kubo, Masato |
| Author_xml | – sequence: 1 givenname: Maryam surname: Hussain fullname: Hussain, Maryam organization: Institute of Pathology, Division of Experimental Pathology, University of Bern, Bern, Switzerland – sequence: 2 givenname: Loïc surname: Borcard fullname: Borcard, Loïc organization: Institute of Pathology, Division of Experimental Pathology, University of Bern, Bern, Switzerland – sequence: 3 givenname: Kevin P. surname: Walsh fullname: Walsh, Kevin P. organization: Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pa – sequence: 4 givenname: Maria surname: Pena Rodriguez fullname: Pena Rodriguez, Maria organization: Institute of Pathology, Division of Experimental Pathology, University of Bern, Bern, Switzerland – sequence: 5 givenname: Christoph orcidid: 0000-0002-3921-8678 surname: Mueller fullname: Mueller, Christoph organization: Institute of Pathology, Division of Experimental Pathology, University of Bern, Bern, Switzerland – sequence: 6 givenname: Brian S. surname: Kim fullname: Kim, Brian S. organization: Division of Dermatology, Department of Medicine, Washington University School of Medicine, St Louis, Mo – sequence: 7 givenname: Masato surname: Kubo fullname: Kubo, Masato organization: Division of Molecular Pathology, Research Institute for Biomedical Science, Laboratory for Cytokine Regulation, RIKEN Center for Integrative Medical Sciences (IMS), RIKEN Yokohama Institute, Tokyo University of Science, Yamazaki, Noda, Japan – sequence: 8 givenname: David surname: Artis fullname: Artis, David organization: Jill Roberts Institute for Research in Inflammatory Bowel Disease, Joan and Sanford I. Weill Department of Medicine, Department of Microbiology and Immunology, Weill Cornell Medical College, Cornell University, New York, NY – sequence: 9 givenname: Mario orcidid: 0000-0001-9386-1245 surname: Noti fullname: Noti, Mario email: mario.noti@pathology.unibe.ch organization: Institute of Pathology, Division of Experimental Pathology, University of Bern, Bern, Switzerland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28390860$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2017 American Academy of Allergy, Asthma & Immunology American Academy of Allergy, Asthma & Immunology Copyright © 2017 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. Copyright Elsevier Science Ltd. Jan 1, 2018 |
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| ISSN | 0091-6749 1097-6825 |
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| Issue | 1 |
| Keywords | eGFP AD TSLP OX40L IgE IL-4 atopic dermatitis TH2 polarization IgE-mediated food allergy basophils mast cells ILC2 epicutaneous sensitization thymic stromal lymphopoietin OVA WT DC Dendritic cell Ovalbumin T H2 polarization Wild-type Group 2 innate lymphoid cell OX40 ligand Enhanced green fluorescent protein T(H)2 polarization |
| Language | English |
| License | Copyright © 2017 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. |
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| PublicationTitle | Journal of allergy and clinical immunology |
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| SubjectTerms | Allergens - immunology Allergy and Immunology Animals Antigens Asthma Atopic dermatitis basophils Basophils - immunology Basophils - metabolism Biomarkers Cell Communication - immunology Dendritic cells Dendritic Cells - immunology Dendritic Cells - metabolism Dermatitis Disease Models, Animal Eczema epicutaneous sensitization Food - adverse effects Food allergies Food Hypersensitivity - immunology Food Hypersensitivity - metabolism Gastrointestinal tract IgE IgE-mediated food allergy IL-4 Immunity, Innate Immunization Immunoglobulin E Immunoglobulin E - immunology Immunophenotyping Inflammation Interleukin 4 Interleukin-4 - metabolism Leukocytes (basophilic) Leukocytes (eosinophilic) Lymphocytes T mast cells Medical innovations Mice Mice, Transgenic Mucosa Ovalbumin Pathogenesis Polarization Skin diseases T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism Th2 Cells - immunology Th2 Cells - metabolism TH2 polarization Thymic stromal lymphopoietin Thymus |
| Title | Basophil-derived IL-4 promotes epicutaneous antigen sensitization concomitant with the development of food allergy |
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