Specific immunotherapy modifies allergen-specific CD4+ T-cell responses in an epitope-dependent manner
Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies. We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to...
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| Published in | Journal of allergy and clinical immunology Vol. 133; no. 3; pp. 872 - 879.e7 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York, NY
Elsevier Inc
01.03.2014
Elsevier Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2013.10.054 |
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| Abstract | Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies.
We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4+ T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy.
Timothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine–treated subjects was determined by using an ex vivo peptide–MHC class II tetramer approach.
CD4+ T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH2 or TH1/TR1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH2 cells and without a significant change in the frequency of TH1/TR1 cells.
Preferential allergen-specific TH2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy. |
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| AbstractList | Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies.
We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4(+) T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy.
Timothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine-treated subjects was determined by using an ex vivo peptide-MHC class II tetramer approach.
CD4(+) T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH2 or TH1/TR1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH2 cells and without a significant change in the frequency of TH1/TR1 cells.
Preferential allergen-specific TH2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy. Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies. We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4+ T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy. Timothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine–treated subjects was determined by using an ex vivo peptide–MHC class II tetramer approach. CD4+ T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH2 or TH1/TR1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH2 cells and without a significant change in the frequency of TH1/TR1 cells. Preferential allergen-specific TH2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy. Background: Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies. Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies.BACKGROUNDUnderstanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies.We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4(+) T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy.OBJECTIVEWe sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4(+) T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy.Timothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine-treated subjects was determined by using an ex vivo peptide-MHC class II tetramer approach.METHODSTimothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine-treated subjects was determined by using an ex vivo peptide-MHC class II tetramer approach.CD4(+) T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH2 or TH1/TR1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH2 cells and without a significant change in the frequency of TH1/TR1 cells.RESULTSCD4(+) T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH2 or TH1/TR1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH2 cells and without a significant change in the frequency of TH1/TR1 cells.Preferential allergen-specific TH2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy.CONCLUSIONSPreferential allergen-specific TH2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy. Background Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies. Objective We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4+ T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy. Methods Timothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine–treated subjects was determined by using an ex vivo peptide–MHC class II tetramer approach. Results CD4+ T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH 2 or TH 1/TR 1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH 2 cells and without a significant change in the frequency of TH 1/TR 1 cells. Conclusions Preferential allergen-specific TH 2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy. Background Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of new allergy vaccine strategies. Objective We sought to characterize allergen-specific T-cell responses linked with allergy or peripheral tolerance and to determine how CD4+T-cell responses to individual allergen-derived epitopes change over allergen-specific immunotherapy. Methods Timothy grass pollen (TGP) allergy was used as a model for studying grass pollen allergies. The breadth, magnitude, epitope hierarchy, and phenotype of the DR04:01-restricted TGP-specific T-cell responses in 10 subjects with grass pollen allergy, 5 nonatopic subjects, and 6 allergy vaccine-treated subjects was determined by using anex vivopeptide-MHC class II tetramer approach. Results CD4+T cells in allergic subjects are directed to a broad range of TGP epitopes characterized by defined immunodominance hierarchy patterns and with distinct functional profiles that depend on the epitope recognized. Epitopes that are restricted specifically to either TH2 or TH1/TR1 responses were identified. Allergen-specific immunotherapy was associated with preferential deletion of allergen-specific TH2 cells and without a significant change in the frequency of TH1/TR1 cells. Conclusions Preferential allergen-specific TH2 cell deletion after repeated high-dose antigen stimulation can be another independent mechanism to restore tolerance to allergen during immunotherapy. |
| Author | DeLong, Jonathan H. Kwok, William W. Wambre, Erik Durham, Stephen R. Till, Stephen J. Torres-Chinn, Nadia Möbs, Christian Robinson, David Pfützner, Wolfgang James, Eddie A. |
| AuthorAffiliation | 3 Department of Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College, London, United Kingdom 1 Benaroya Research Institute at Virginia Mason, Seattle, WA, USA 4 Allergy, Asthma and Lung Biology, King’s College London, United Kingdom 6 Department of Medicine, University of Washington, Seattle, WA 5 Allergy, Asthma and Lung Biology, King’s College London, United Kingdom 2 Department of Dermatology and Allergology, University Medical Center, Marburg, Germany |
| AuthorAffiliation_xml | – name: 4 Allergy, Asthma and Lung Biology, King’s College London, United Kingdom – name: 6 Department of Medicine, University of Washington, Seattle, WA – name: 1 Benaroya Research Institute at Virginia Mason, Seattle, WA, USA – name: 2 Department of Dermatology and Allergology, University Medical Center, Marburg, Germany – name: 3 Department of Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College, London, United Kingdom – name: 5 Allergy, Asthma and Lung Biology, King’s College London, United Kingdom |
| Author_xml | – sequence: 1 givenname: Erik surname: Wambre fullname: Wambre, Erik organization: Benaroya Research Institute at Virginia Mason, Seattle, Wash – sequence: 2 givenname: Jonathan H. surname: DeLong fullname: DeLong, Jonathan H. organization: Benaroya Research Institute at Virginia Mason, Seattle, Wash – sequence: 3 givenname: Eddie A. surname: James fullname: James, Eddie A. organization: Benaroya Research Institute at Virginia Mason, Seattle, Wash – sequence: 4 givenname: Nadia surname: Torres-Chinn fullname: Torres-Chinn, Nadia organization: Benaroya Research Institute at Virginia Mason, Seattle, Wash – sequence: 5 givenname: Wolfgang surname: Pfützner fullname: Pfützner, Wolfgang organization: Department of Dermatology and Allergology, University Medical Center, Marburg, Germany – sequence: 6 givenname: Christian surname: Möbs fullname: Möbs, Christian organization: Department of Dermatology and Allergology, University Medical Center, Marburg, Germany – sequence: 7 givenname: Stephen R. surname: Durham fullname: Durham, Stephen R. organization: Department of Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College, London, United Kingdom – sequence: 8 givenname: Stephen J. surname: Till fullname: Till, Stephen J. organization: Allergy, Asthma and Lung Biology, King’s College London, London, United Kingdom – sequence: 9 givenname: David surname: Robinson fullname: Robinson, David organization: Virginia Mason Medical Center, Seattle, Wash – sequence: 10 givenname: William W. surname: Kwok fullname: Kwok, William W. email: bkwok@benaroyaresearch.org organization: Benaroya Research Institute at Virginia Mason, Seattle, Wash |
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| Snippet | Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the design of... Background Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the... Background: Understanding the mechanisms by which the immune system induces and controls allergic inflammation at the T-cell epitope level is critical for the... |
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| SubjectTerms | Allergens - immunology Allergies allergy Allergy and Immunology Biological and medical sciences CD4 CD4-Positive T-Lymphocytes - immunology Cytokines Desensitization, Immunologic epitope Epitopes, T-Lymphocyte - immunology ex vivo Fundamental and applied biological sciences. Psychology Fundamental immunology Grasses Humans Immune Tolerance Immunopathology Immunophenotyping Immunotherapy Lymphocytes Medical sciences Peptides peptide–MHC class II tetramer peripheral tolerance Phleum - immunology pollen Sarcoidosis. Granulomatous diseases of unproved etiology. Connective tissue diseases. Elastic tissue diseases. Vasculitis Statistical analysis T cell receptors T cells Th1 Cells - immunology Th2 Cells - immunology Tumor Necrosis Factor Receptor Superfamily, Member 7 - analysis |
| Title | Specific immunotherapy modifies allergen-specific CD4+ T-cell responses in an epitope-dependent manner |
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