Long-term tolerance after allergen immunotherapy is accompanied by selective persistence of blocking antibodies
Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen–specific IgG antibodies capable of blocking allergen...
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| Published in | Journal of allergy and clinical immunology Vol. 127; no. 2; pp. 509 - 516.e5 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York, NY
Mosby, Inc
01.02.2011
Elsevier Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0091-6749 1097-6825 1097-6825 |
| DOI | 10.1016/j.jaci.2010.12.1080 |
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| Abstract | Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen–specific IgG antibodies capable of blocking allergen-IgE interactions.
We sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy.
We conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE–grass pollen allergen complexes to B cells.
Clinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen–specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged.
Grass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance. |
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| AbstractList | BACKGROUND: Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen–specific IgG antibodies capable of blocking allergen-IgE interactions. OBJECTIVES: We sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy. METHODS: We conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE–grass pollen allergen complexes to B cells. RESULTS: Clinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen–specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged. CONCLUSION: Grass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance. Background Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen–specific IgG antibodies capable of blocking allergen-IgE interactions. Objectives We sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy. Methods We conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE–grass pollen allergen complexes to B cells. Results Clinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen–specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged. Conclusion Grass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance. Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen–specific IgG antibodies capable of blocking allergen-IgE interactions. We sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy. We conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE–grass pollen allergen complexes to B cells. Clinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen–specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged. Grass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance. Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen-specific IgG antibodies capable of blocking allergen-IgE interactions.BACKGROUNDGrass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen-specific IgG antibodies capable of blocking allergen-IgE interactions.We sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy.OBJECTIVESWe sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy.We conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE-grass pollen allergen complexes to B cells.METHODSWe conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE-grass pollen allergen complexes to B cells.Clinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen-specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged.RESULTSClinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen-specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged.Grass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance.CONCLUSIONGrass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance. Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment discontinuation. Active treatment is associated with generation of inhibitory grass pollen-specific IgG antibodies capable of blocking allergen-IgE interactions. We sought to investigate the involvement of IgG-associated inhibitory antibodies with long-term clinical tolerance after discontinuation of grass pollen immunotherapy. We conducted a 4-year study in which patients who had moderate-to-severe allergic rhinitis underwent a randomized, double-blind, placebo-controlled discontinuation of subcutaneous grass pollen immunotherapy. All subjects received grass pollen immunotherapy injections for 2 years (n = 13), followed by a further 2 years of either active (n = 7) or placebo (n = 6) injections. Clinical outcomes included seasonal symptoms and use of rescue medication. Serum specimens were collected at baseline and after 2 and 4 years for quantification of allergen-specific IgG antibodies. Sera were also tested for IgG-dependent inhibitory bioactivity against IgE-allergen binding in cellular assays by using flow cytometry and confocal microscopy to detect binding of IgE-grass pollen allergen complexes to B cells. Clinical improvement was maintained after 2 years of discontinuation. Although immunotherapy-induced grass pollen-specific IgG1 and IgG4 levels decreased to near-preimmunotherapy levels during discontinuation, inhibitory bioactivity of allergen-specific IgG antibodies was maintained unchanged. Grass pollen immunotherapy induces a subpopulation of allergen-specific IgG antibodies with potent inhibitory activity against IgE that persists after treatment discontinuation and that could account for long-term clinical tolerance. |
| Author | Shamji, Mohamed H. James, Louisa K. Walker, Samantha M. Francis, James N. Till, Stephen J. Durham, Stephen R. Jacobson, Mikila R. Wachholz, Petra A. Wilson, Duncan R. Kimber, Ian |
| Author_xml | – sequence: 1 givenname: Louisa K. surname: James fullname: James, Louisa K. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 2 givenname: Mohamed H. surname: Shamji fullname: Shamji, Mohamed H. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 3 givenname: Samantha M. surname: Walker fullname: Walker, Samantha M. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 4 givenname: Duncan R. surname: Wilson fullname: Wilson, Duncan R. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 5 givenname: Petra A. surname: Wachholz fullname: Wachholz, Petra A. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 6 givenname: James N. surname: Francis fullname: Francis, James N. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 7 givenname: Mikila R. surname: Jacobson fullname: Jacobson, Mikila R. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 8 givenname: Ian surname: Kimber fullname: Kimber, Ian organization: Faculty of Life Sciences, University of Manchester, Manchester, United Kingdom – sequence: 9 givenname: Stephen J. surname: Till fullname: Till, Stephen J. organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom – sequence: 10 givenname: Stephen R. surname: Durham fullname: Durham, Stephen R. email: s.durham@imperial.ac.uk organization: Allergy and Clinical Immunology, National Heart and Lung Institute, Imperial College London, part of the Medical Research Council and Asthma UK Centre for Allergic Mechanisms of Asthma, London, United Kingdom |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23889756$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/21281875$$D View this record in MEDLINE/PubMed |
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| CODEN | JACIBY |
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| Keywords | Immunotherapy IgE FAB IgG4 IQR facilitated antigen presentation CD23 Facilitated allergen binding Interquartile range Immunopathology Antigen presentation Immunoglobulins Desensitization FcεRII receptor Tolerance Blocking antibody Long term Persistence Immunology Treatment |
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| References | Shamji, Wilcock, Wachholz, Dearman, Kimber, Wurtzen (bib16) 2006; 317 Wurtzen, Lund, Lund, Arvidsson, Rak, Ipsen (bib26) 2008; 38 Rossi, Monasterolo, Coco, Silvestro, Operti (bib23) 2007; 15 Passalacqua, Durham (bib7) 2007; 119 Satoguina, Adjobimey, Arndts, Hoch, Oldenburg, Layland (bib12) 2008; 38 Aalberse, van der Gaag, van Leeuwen (bib33) 1983; 130 Smith, Garman, Wrammert, Zheng, Capra, Ahmed (bib38) 2009; 4 McHugh, Lavelle, Kemeny, Patel, Ewan (bib21) 1990; 86 Durham, Walker, Varga, Jacobson, O'Brien, Noble (bib8) 1999; 341 Walker, Pajno, Lima, Wilson, Durham (bib15) 2001; 107 Klunker, Saggar, Seyfert-Margolis, Asare, Casale, Durham (bib18) 2007; 120 Lambin, Bouzoumou, Murrieta, Debbia, Rouger, Leynadier (bib24) 1993; 165 van Neerven, Wikborg, Lund, Jacobsen, Brinch-Nielsen, Arnved (bib11) 1999; 163 Wilson, Sims, Orr, Robb, Lipworth (bib5) 2003; 55 Cady, Powell, Harbeck, Giclas, Murphy, Katial (bib27) 2010; 130 Walker, Khan-Wasti, Fletcher, Cullinan, Harris, Sheikh (bib2) 2007; 120 Svenson, Jacobi, Bødtger, Poulsen, Rieneck, Bendtzen (bib36) 2003; 39 van der Neut Kolfschoten, Schuurman, Losen, Bleeker, Martínez-Martínez, Vermeulen (bib31) 2007; 317 Bauchau, Durham (bib1) 2004; 24 Francis, James, Paraskevopoulos, Wong, Calderon, Durham (bib9) 2008; 121 Aalberse, Schuurman (bib32) 2002; 105 Djurup, Sondergaard, Magnusson, Weeke (bib30) 1984; 39 Strait, Morris, Finkelman (bib25) 2006; 116 Calderon, Alves, Jacobson, Hurwitz, Sheikh, Durham (bib6) 2007 Muller, Akdis, Fricker, Akdis, Blesken, Bettens (bib28) 1998; 101 Radulovic, Jacobson, Durham, Nouri-Aria (bib14) 2008; 121 Meiler, Klunker, Zimmermann, Akdis, Akdis (bib13) 2008; 63 Tiller, Meffre, Yurasov, Tsuiji, Nussenzweig, Wardemann (bib37) 2008; 329 Gehlar, Schlaak, Becker, Bufe (bib22) 1999; 29 Bousquet, Khaltaev, Cruz, Denburg, Fokkens, Togias (bib3) 2008; 63 Nouri-Aria, Wachholz, Francis, Jacobson, Walker, Wilcock (bib17) 2004; 172 Des Roches, Paradis, Knani, Hejjaoui, Dhivert, Chanez (bib20) 1996; 51 Ewan, Deighton, Wilson, Lachmann (bib29) 1993; 23 Michils, Baldassarre, Ledent, Mairesse, Gossart, Duchateau (bib35) 2000; 55 Gleich, Zimmermann, Henderson, Yunginger (bib34) 1982; 70 White, Smith, Baker, Davis, Frew (bib4) 1998; 28 Wachholz, Soni, Till, Durham (bib19) 2003; 112 Garcia, Sanz, Gato, Fernandez, Oehling (bib10) 1993; 3 |
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I. Prolonged immunization results in an IgG4-restricted response publication-title: J Immunol – volume: 15 start-page: 957 year: 2007 end-page: 964 ident: bib23 article-title: Evaluation of serum IgG4 antibodies specific to grass pollen allergen components in the follow up of allergic patients undergoing subcutaneous and sublingual immunotherapy publication-title: Vaccine – volume: 105 start-page: 9 year: 2002 end-page: 19 ident: bib32 article-title: IgG4 breaking the rules publication-title: Immunology – volume: 39 start-page: 603 year: 2003 end-page: 612 ident: bib36 article-title: Vaccination for birch pollen allergy. 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| Snippet | Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after treatment... Background Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after... BACKGROUND: Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after... Background: Grass pollen immunotherapy for allergic rhinitis is a disease-modifying treatment that results in long-term clinical tolerance lasting years after... |
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| SubjectTerms | Adult allergens Allergies Allergy and Immunology antibodies Antibodies, Blocking - blood Antigens Biological activity Biological and medical sciences blood serum CD23 confocal microscopy Desensitization, Immunologic Double-Blind Method drug therapy facilitated antigen presentation Female flow cytometry Fundamental and applied biological sciences. Psychology Fundamental immunology grasses Humans IgE IgG4 Immune Tolerance immunoglobulin E Immunoglobulin E - immunology immunoglobulin G Immunoglobulin G - blood Immunopathology Immunotherapy Male Medical sciences patients placebos Poaceae - immunology pollen rhinitis Rhinitis, Allergic, Seasonal - immunology Rhinitis, Allergic, Seasonal - therapy Sarcoidosis. Granulomatous diseases of unproved etiology. Connective tissue diseases. Elastic tissue diseases. Vasculitis Seasons Time Factors |
| Title | Long-term tolerance after allergen immunotherapy is accompanied by selective persistence of blocking antibodies |
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