IgG subclasses determine pathways of anaphylaxis in mice
Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and IgG2b bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1 binds only FcγRIII and FcγRIIB. Although thes...
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| Published in | Journal of allergy and clinical immunology Vol. 139; no. 1; pp. 269 - 280.e7 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.01.2017
Elsevier Limited Elsevier |
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| Online Access | Get full text |
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| Abstract | Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and IgG2b bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1 binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis. Objective We sought to determine which pathways control the induction of IgG1 -, IgG2a -, and IgG2b -dependent passive systemic anaphylaxis. Methods Mice were sensitized with IgG1 , IgG2a , or IgG2b anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis. Results Activating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1 - and IgG2b -induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis. Conclusion We propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass–dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. |
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| AbstractList | Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG
and IgG
bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG
binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis.
We sought to determine which pathways control the induction of IgG
-, IgG
-, and IgG
-dependent passive systemic anaphylaxis.
Mice were sensitized with IgG
, IgG
, or IgG
anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis.
Activating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG
- and IgG
-induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis.
We propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass-dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. BACKGROUND:Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and IgG2b bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1 binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis.OBJECTIVE:We sought to determine which pathways control the induction of IgG1-, IgG2a-, and IgG2b-dependent passive systemic anaphylaxis.METHODS:Mice were sensitized with IgG1, IgG2a, or IgG2b anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis.RESULTS:Activating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1- and IgG2b-induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis.CONCLUSION:We propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass-dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (Fc gamma Rs). Mouse IgG2a and IgG2b bind activating Fc gamma RI, Fc gamma RIII, and Fc gamma RIV and inhibitory Fc gamma RIIB; mouse IgG1 binds only Fc gamma RIII and Fc gamma RIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis. Objective We sought to determine which pathways control the induction of IgG1-, IgG2a-, and IgG2b-dependent passive systemic anaphylaxis. Methods Mice were sensitized with IgG1, IgG2a, or IgG2b anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for Fc gamma Rs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. Fc gamma R expression was evaluated on these cells before and after anaphylaxis. Results Activating Fc gamma RIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1- and IgG2b-induced anaphylaxis correlated with the ability of inhibitory Fc gamma RIIB to negatively regulate these models of anaphylaxis. Conclusion We propose that the differential expression of inhibitory Fc gamma RIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass-dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and IgG2b bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1 binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis. Objective We sought to determine which pathways control the induction of IgG1 -, IgG2a -, and IgG2b -dependent passive systemic anaphylaxis. Methods Mice were sensitized with IgG1 , IgG2a , or IgG2b anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis. Results Activating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1 - and IgG2b -induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis. Conclusion We propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass–dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. BACKGROUNDAnimal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and IgG2b bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1 binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis.OBJECTIVEWe sought to determine which pathways control the induction of IgG1-, IgG2a-, and IgG2b-dependent passive systemic anaphylaxis.METHODSMice were sensitized with IgG1, IgG2a, or IgG2b anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis.RESULTSActivating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1- and IgG2b-induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis.CONCLUSIONWe propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass-dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and IgG2b bind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1 binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis. We sought to determine which pathways control the induction of IgG1-, IgG2a-, and IgG2b-dependent passive systemic anaphylaxis. Mice were sensitized with IgG1, IgG2a, or IgG2b anti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis. Activating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1- and IgG2b-induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis. We propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass–dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactions in vivo. Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2aand IgG2bbind activating FcγRI, FcγRIII, and FcγRIV and inhibitory FcγRIIB; mouse IgG1binds only FcγRIII and FcγRIIB. Although these interactions are of strikingly different affinities, these 3 IgG subclasses have been shown to enable induction of systemic anaphylaxis. Objective We sought to determine which pathways control the induction of IgG1-, IgG2a-, and IgG2b-dependent passive systemic anaphylaxis. Methods Mice were sensitized with IgG1, IgG2a, or IgG2banti-trinitrophenyl mAbs and challenged with trinitrophenyl-BSA intravenously to induce systemic anaphylaxis that was monitored by using rectal temperature. Anaphylaxis was evaluated in mice deficient for FcγRs injected with mediator antagonists or in which basophils, monocytes/macrophages, or neutrophils had been depleted. FcγR expression was evaluated on these cells before and after anaphylaxis. Results Activating FcγRIII is the receptor primarily responsible for all 3 models of anaphylaxis, and subsequent downregulation of this receptor was observed. These models differentially relied on histamine release and the contribution of mast cells, basophils, macrophages, and neutrophils. Strikingly, basophil contribution and histamine predominance in mice with IgG1- and IgG2b-induced anaphylaxis correlated with the ability of inhibitory FcγRIIB to negatively regulate these models of anaphylaxis. Conclusion We propose that the differential expression of inhibitory FcγRIIB on myeloid cells and its differential binding of IgG subclasses controls the contributions of mast cells, basophils, neutrophils, and macrophages to IgG subclass-dependent anaphylaxis. Collectively, our results unravel novel complexities in the involvement and regulation of cell populations in IgG-dependent reactionsin vivo. |
| Author | Gillis, Caitlin M., BSci Beutier, Héloïse, PharmD Iannascoli, Bruno, BTS Bruhns, Pierre, PhD Van Rooijen, Nico, PhD England, Patrick, PhD Jönsson, Friederike, PhD Galli, Stephen J., MD Mancardi, David A., PhD Reber, Laurent L., PhD Godon, Ophélie, MSc Sibilano, Riccardo, PhD Cragg, Mark S., PhD |
| AuthorAffiliation | 3 Université Pierre et Marie Curie, Paris, France 8 Department of Molecular Cell Biology, VU Medical Center, Amsterdam, The Netherlands 1 Institut Pasteur, Department of Immunology, Unit of Antibodies in Therapy and Pathology, Paris, France 5 Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA 7 Antibody and Vaccine Group, Cancer Sciences Unit, University of Southampton Faculty of Medicine, Southampton General Hospital, Southampton, UK 2 INSERM, U1222, Paris, France 6 Sean N. Parker Center for Allergy and Asthma Research, Stanford University School of Medicine, Stanford, CA, USA 4 Institut Pasteur, Plate-Forme de Biophysique Moléculaire, Centre d'Innovation et Recherche Technologique (CiTech), CNRS-UMR3528, Paris, France |
| AuthorAffiliation_xml | – name: 3 Université Pierre et Marie Curie, Paris, France – name: 4 Institut Pasteur, Plate-Forme de Biophysique Moléculaire, Centre d'Innovation et Recherche Technologique (CiTech), CNRS-UMR3528, Paris, France – name: 6 Sean N. Parker Center for Allergy and Asthma Research, Stanford University School of Medicine, Stanford, CA, USA – name: 2 INSERM, U1222, Paris, France – name: 8 Department of Molecular Cell Biology, VU Medical Center, Amsterdam, The Netherlands – name: 5 Department of Pathology, Stanford University School of Medicine, Stanford, CA, USA – name: 1 Institut Pasteur, Department of Immunology, Unit of Antibodies in Therapy and Pathology, Paris, France – name: 7 Antibody and Vaccine Group, Cancer Sciences Unit, University of Southampton Faculty of Medicine, Southampton General Hospital, Southampton, UK |
| Author_xml | – sequence: 1 fullname: Beutier, Héloïse, PharmD – sequence: 2 fullname: Gillis, Caitlin M., BSci – sequence: 3 fullname: Iannascoli, Bruno, BTS – sequence: 4 fullname: Godon, Ophélie, MSc – sequence: 5 fullname: England, Patrick, PhD – sequence: 6 fullname: Sibilano, Riccardo, PhD – sequence: 7 fullname: Reber, Laurent L., PhD – sequence: 8 fullname: Galli, Stephen J., MD – sequence: 9 fullname: Cragg, Mark S., PhD – sequence: 10 fullname: Van Rooijen, Nico, PhD – sequence: 11 fullname: Mancardi, David A., PhD – sequence: 12 fullname: Bruhns, Pierre, PhD – sequence: 13 fullname: Jönsson, Friederike, PhD |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27246523$$D View this record in MEDLINE/PubMed https://pasteur.hal.science/pasteur-01388338$$DView record in HAL |
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| Copyright | American Academy of Allergy, Asthma & Immunology 2016 American Academy of Allergy, Asthma & Immunology Copyright © 2016 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. Copyright Elsevier Limited Jan 01, 2017 Copyright |
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| IngestDate | Tue Sep 17 21:16:42 EDT 2024 Tue Oct 15 15:32:58 EDT 2024 Fri Oct 25 21:11:31 EDT 2024 Thu Oct 24 22:46:25 EDT 2024 Thu Oct 10 18:04:28 EDT 2024 Fri Dec 06 01:05:23 EST 2024 Wed Oct 16 00:57:53 EDT 2024 Fri Feb 23 02:34:42 EST 2024 Tue Oct 15 22:55:41 EDT 2024 |
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| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 1 |
| Keywords | Fluorescein isothiocyanate Mast cell protease 1 Association rate histamine RU Gfi1 IgG Neonatal IgG receptor platelet-activating factor basophil neutrophil mMCP-1 Growth factor independence 1 FITC Anaphylaxis TNP FcRn C57Bl/6 wild-type Dissociation equilibrium constant Trinitrophenyl TRIM21 WT PSA Tripartite motif-containing protein 21 mouse model Affinity constant macrophage Resonance units K off IgG Fc receptor K A K D PAF K on Passive systemic anaphylaxis monocyte Dissociation rate FcγR KA KD Koff Kon |
| Language | English |
| License | Copyright © 2016 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. Copyright: http://hal.archives-ouvertes.fr/licences/copyright |
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| PublicationCentury | 2000 |
| PublicationDate | 2017-01-01 |
| PublicationDateYYYYMMDD | 2017-01-01 |
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| PublicationPlace | United States |
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| PublicationTitle | Journal of allergy and clinical immunology |
| PublicationTitleAlternate | J Allergy Clin Immunol |
| PublicationYear | 2017 |
| Publisher | Elsevier Inc Elsevier Limited Elsevier |
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| Snippet | Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs).... Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG2a and... Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse IgG and... BACKGROUNDAnimal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs). Mouse... Background Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (Fc gamma... BACKGROUND:Animal models have demonstrated that allergen-specific IgG confers sensitivity to systemic anaphylaxis that relies on IgG Fc receptors (FcγRs).... |
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| SubjectTerms | Allergies Allergy and Immunology Anaphylaxis Anaphylaxis - immunology Animals Antibodies, Monoclonal - immunology basophil Colleges & universities Female Haptens - immunology histamine Histamine - immunology Human subjects IgG IgG Fc receptor Immunoglobulin E - immunology Immunoglobulin G - immunology Immunoglobulins Immunology Life Sciences macrophage Mice, Inbred C57BL Mice, Transgenic monocyte mouse model Myeloid Cells - immunology neutrophil Neutrophils platelet-activating factor Protein Subunits - immunology Receptors, IgG - genetics Receptors, IgG - immunology Rodents Serum Albumin, Bovine - immunology |
| Title | IgG subclasses determine pathways of anaphylaxis in mice |
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