Differences in innate immune function between allergic and nonallergic children: New insights into immune ontogeny
Microbial products are of central interest in the modulation of allergic propensity. We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)–mediated responses over their first 5 years of life. Mononuclear cells isolated from 35 allergic and 35 nonallerg...
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| Published in | Journal of allergy and clinical immunology Vol. 127; no. 2; pp. 470 - 478.e1 |
|---|---|
| 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.2010.09.020 |
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| Abstract | Microbial products are of central interest in the modulation of allergic propensity.
We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)–mediated responses over their first 5 years of life.
Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology.
Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T
H1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (
P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (
P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T
H1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T
H2 responses (
P < .01).
Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. |
|---|---|
| AbstractList | BACKGROUND: Microbial products are of central interest in the modulation of allergic propensity. OBJECTIVE: We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)–mediated responses over their first 5 years of life. METHODS: Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology. RESULTS: Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive TH1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of TH1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific TH2 responses (P < .01). CONCLUSION: Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. Microbial products are of central interest in the modulation of allergic propensity. We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)–mediated responses over their first 5 years of life. Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology. Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T H1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth ( P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects ( P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T H1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T H2 responses ( P < .01). Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. Microbial products are of central interest in the modulation of allergic propensity.BACKGROUNDMicrobial products are of central interest in the modulation of allergic propensity.We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)-mediated responses over their first 5 years of life.OBJECTIVEWe sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)-mediated responses over their first 5 years of life.Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology.METHODSMononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology.Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T(H)1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T(H)1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T(H)2 responses (P < .01).RESULTSNonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T(H)1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T(H)1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T(H)2 responses (P < .01).Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity.CONCLUSIONOur findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. Background: Microbial products are of central interest in the modulation of allergic propensity. Objective: We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)-mediated responses over their first 5 years of life. Methods: Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology. Results: Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1 beta, IL-6, TNF-alpha, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T(H)1 (IFN-gamma) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (P andlt; .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (P andlt; .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T(H)1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T(H)2 responses (P andlt; .01). Conclusion: Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. Background Microbial products are of central interest in the modulation of allergic propensity. Objective We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)–mediated responses over their first 5 years of life. Methods Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology. Results Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive TH 1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth ( P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects ( P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of TH 1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific TH 2 responses ( P < .01). Conclusion Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. Microbial products are of central interest in the modulation of allergic propensity. We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)-mediated responses over their first 5 years of life. Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology. Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1β, IL-6, TNF-α, and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T(H)1 (IFN-γ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T(H)1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T(H)2 responses (P < .01). Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity. Background: Microbial products are of central interest in the modulation of allergic propensity. Objective: We sought to explore whether allergic children show differences in microbial Toll-like receptor (TLR)-mediated responses over their first 5 years of life. Methods: Mononuclear cells isolated from 35 allergic and 35 nonallergic children at birth and 1, 2.5, and 5 years of age were stimulated with TLR2-TLR9 ligands to study innate immune function and with allergens or mitogen to assess adaptive T-cell responses. Cytokine production was measured by using Luminex multiplexing technology. Results: Nonallergic children show progressive and significant age-related increases in innate cytokine responses (IL-1 beta , IL-6, TNF- alpha , and IL-10) to virtually all TLR ligands. This innate maturation corresponds with a parallel increase in adaptive T sub(H1 (IFN- gamma ) responses to allergens and mitogens. In contrast, allergic children show exaggerated innate responses at birth (P < .01) but a relative decrease with age thereafter, so that by age 5 years, TLR responses are attenuated compared with those seen in nonallergic subjects (P < .05). This early hyperresponsiveness in allergic subjects fails to translate to a corresponding maturation of T) sub(H)1 function, which remains attenuated relative to that seen in nonallergic subjects but is associated with a characteristic age-dependent increase in allergen-specific T sub(H2 responses (P < .01). Conclusion: Our findings suggest significant differences in the developmental trajectory of innate immune function in children with allergic disease that might contribute to the recognized differences in postnatal adaptive T-cell immunity.) |
| Author | Richman, Tara Hodder, Megan Thornton, Catherine A. McCarthy, Suzi D’Vaz, Nina van den Biggelaar, Anita H.J. Prescott, Susan L. Tulic, Meri K. Forsberg, Anna |
| Author_xml | – sequence: 1 givenname: Meri K. surname: Tulic fullname: Tulic, Meri K. email: mtulic@meddent.uwa.edu.au organization: Childhood Allergy and Immunology Research, School of Paediatrics and Child Health, University of Western Australia, Perth, Australia – sequence: 2 givenname: Megan surname: Hodder fullname: Hodder, Megan organization: Childhood Allergy and Immunology Research, School of Paediatrics and Child Health, University of Western Australia, Perth, Australia – sequence: 3 givenname: Anna surname: Forsberg fullname: Forsberg, Anna organization: Department of Clinical and Experimental Medicine, Division of Inflammation Medicine, Linköping University, Linkoping, Sweden – sequence: 4 givenname: Suzi surname: McCarthy fullname: McCarthy, Suzi organization: Childhood Allergy and Immunology Research, School of Paediatrics and Child Health, University of Western Australia, Perth, Australia – sequence: 5 givenname: Tara surname: Richman fullname: Richman, Tara organization: Childhood Allergy and Immunology Research, School of Paediatrics and Child Health, University of Western Australia, Perth, Australia – sequence: 6 givenname: Nina surname: D’Vaz fullname: D’Vaz, Nina organization: Childhood Allergy and Immunology Research, School of Paediatrics and Child Health, University of Western Australia, Perth, Australia – sequence: 7 givenname: Anita H.J. surname: van den Biggelaar fullname: van den Biggelaar, Anita H.J. organization: Division of Cell Biology, Telethon Institute for Child Health Research, Centre for Child Health Research, UWA, Perth, Australia – sequence: 8 givenname: Catherine A. surname: Thornton fullname: Thornton, Catherine A. organization: Institute of Life Science, School of Medicine, Swansea University, Swansea, United Kingdom – sequence: 9 givenname: Susan L. surname: Prescott fullname: Prescott, Susan L. organization: Childhood Allergy and Immunology Research, School of Paediatrics and Child Health, University of Western Australia, Perth, Australia |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23889751$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/21093030$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:liu:diva-66292$$DView record from Swedish Publication Index |
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| ContentType | Journal Article |
| Copyright | 2010 American Academy of Allergy, Asthma & Immunology American Academy of Allergy, Asthma & Immunology 2015 INIST-CNRS Copyright © 2010 American Academy of Allergy, Asthma & Immunology. Published by Mosby, Inc. All rights reserved. Copyright Elsevier Limited Feb 2011 |
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| Keywords | innate immunity APC children SPT TLR allergic disease ontogeny mDC NK Toll-like receptor pDC myeloid dendritic cell Skin prick test Plasmacytoid dendritic cell Natural killer Antigen-presenting cell Human Immunopathology Allergy Natural immunity Toll like receptor Immunology Development Child Comparative study |
| Language | English |
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| Snippet | Microbial products are of central interest in the modulation of allergic propensity.
We sought to explore whether allergic children show differences in... Background Microbial products are of central interest in the modulation of allergic propensity. Objective We sought to explore whether allergic children show... BACKGROUND: Microbial products are of central interest in the modulation of allergic propensity. OBJECTIVE: We sought to explore whether allergic children show... Microbial products are of central interest in the modulation of allergic propensity.BACKGROUNDMicrobial products are of central interest in the modulation of... Background: Microbial products are of central interest in the modulation of allergic propensity. Objective: We sought to explore whether allergic children show... |
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| SubjectTerms | Adaptive Immunity Age Factors allergens allergic disease Allergies Allergy and Immunology Antigen-Presenting Cells - immunology Asthma Biological and medical sciences Case-Control Studies Child, Preschool children Disease Eczema Female Food Food allergies Fundamental and applied biological sciences. Psychology Fundamental immunology Hospitals Humans Hypersensitivity - immunology immunity Immunity, Innate Immunopathology Infant Infant, Newborn Infections innate immunity interferon-gamma interleukin-10 interleukin-1beta interleukin-6 Ligands Male Medical sciences ontogeny Sarcoidosis. Granulomatous diseases of unproved etiology. Connective tissue diseases. Elastic tissue diseases. Vasculitis T-lymphocytes T-Lymphocytes - immunology TECHNOLOGY TEKNIKVETENSKAP Toll-like receptor Toll-like receptors Toll-Like Receptors - physiology tumor necrosis factor-alpha |
| Title | Differences in innate immune function between allergic and nonallergic children: New insights into immune ontogeny |
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