Microbiome-induced antigen-presenting cell recruitment coordinates skin and lung allergic inflammation
Allergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature. We sought to determine the immunologic rules that govern skin inflammation in early life. Neonatal and adult mice were...
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| Veröffentlicht in: | Journal of allergy and clinical immunology Jg. 147; H. 3; S. 1049 - 1062.e7 |
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01.03.2021
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| Abstract | Allergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature.
We sought to determine the immunologic rules that govern skin inflammation in early life.
Neonatal and adult mice were epicutaneously sensitized with allergen followed by airway allergen challenge. Epicutaneous application of labeled allergen allowed for determination of antigen uptake and processing by antigen-presenting cells. RNAseq and microbiome analysis was performed on skin from neonatal and adult specific pathogen-free and germ-free mice.
A mixed TH2/TH17 inflammatory response in the skin and the lungs of adult mice was observed following sensitization and challenge. Comparatively, neonatal mice did not develop overt skin inflammation, but exhibited systemic release of IL-17a and a TH2-dominated lung response. Mechanical skin barrier disruption was not sufficient to drive allergic skin inflammation, although it did promote systemic immune priming. Skin of neonatal mice and adult germ-free mice was seeded with low numbers of antigen-presenting cells and impaired chemokine and alarmin production. Enhanced chemokine and alarmin production, and seeding of the skin with antigen-presenting cells capable of instructing recruited cells to elicit their effector function, was, at least in part, dependent on formation of the microbiome, and consequently contributed to the development of overt skin disease.
These data shed light on the principles that underlie allergic inflammation in different tissues and highlight a window of opportunity that might exist for early-life prevention of allergic diseases.
[Display omitted] |
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| AbstractList | Allergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature.
We sought to determine the immunologic rules that govern skin inflammation in early life.
Neonatal and adult mice were epicutaneously sensitized with allergen followed by airway allergen challenge. Epicutaneous application of labeled allergen allowed for determination of antigen uptake and processing by antigen-presenting cells. RNAseq and microbiome analysis was performed on skin from neonatal and adult specific pathogen-free and germ-free mice.
A mixed T
2/T
17 inflammatory response in the skin and the lungs of adult mice was observed following sensitization and challenge. Comparatively, neonatal mice did not develop overt skin inflammation, but exhibited systemic release of IL-17a and a T
2-dominated lung response. Mechanical skin barrier disruption was not sufficient to drive allergic skin inflammation, although it did promote systemic immune priming. Skin of neonatal mice and adult germ-free mice was seeded with low numbers of antigen-presenting cells and impaired chemokine and alarmin production. Enhanced chemokine and alarmin production, and seeding of the skin with antigen-presenting cells capable of instructing recruited cells to elicit their effector function, was, at least in part, dependent on formation of the microbiome, and consequently contributed to the development of overt skin disease.
These data shed light on the principles that underlie allergic inflammation in different tissues and highlight a window of opportunity that might exist for early-life prevention of allergic diseases. Allergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature. We sought to determine the immunologic rules that govern skin inflammation in early life. Neonatal and adult mice were epicutaneously sensitized with allergen followed by airway allergen challenge. Epicutaneous application of labeled allergen allowed for determination of antigen uptake and processing by antigen-presenting cells. RNAseq and microbiome analysis was performed on skin from neonatal and adult specific pathogen-free and germ-free mice. A mixed TH2/TH17 inflammatory response in the skin and the lungs of adult mice was observed following sensitization and challenge. Comparatively, neonatal mice did not develop overt skin inflammation, but exhibited systemic release of IL-17a and a TH2-dominated lung response. Mechanical skin barrier disruption was not sufficient to drive allergic skin inflammation, although it did promote systemic immune priming. Skin of neonatal mice and adult germ-free mice was seeded with low numbers of antigen-presenting cells and impaired chemokine and alarmin production. Enhanced chemokine and alarmin production, and seeding of the skin with antigen-presenting cells capable of instructing recruited cells to elicit their effector function, was, at least in part, dependent on formation of the microbiome, and consequently contributed to the development of overt skin disease. These data shed light on the principles that underlie allergic inflammation in different tissues and highlight a window of opportunity that might exist for early-life prevention of allergic diseases. [Display omitted] Allergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature.BACKGROUNDAllergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature.We sought to determine the immunologic rules that govern skin inflammation in early life.OBJECTIVEWe sought to determine the immunologic rules that govern skin inflammation in early life.Neonatal and adult mice were epicutaneously sensitized with allergen followed by airway allergen challenge. Epicutaneous application of labeled allergen allowed for determination of antigen uptake and processing by antigen-presenting cells. RNAseq and microbiome analysis was performed on skin from neonatal and adult specific pathogen-free and germ-free mice.METHODSNeonatal and adult mice were epicutaneously sensitized with allergen followed by airway allergen challenge. Epicutaneous application of labeled allergen allowed for determination of antigen uptake and processing by antigen-presenting cells. RNAseq and microbiome analysis was performed on skin from neonatal and adult specific pathogen-free and germ-free mice.A mixed TH2/TH17 inflammatory response in the skin and the lungs of adult mice was observed following sensitization and challenge. Comparatively, neonatal mice did not develop overt skin inflammation, but exhibited systemic release of IL-17a and a TH2-dominated lung response. Mechanical skin barrier disruption was not sufficient to drive allergic skin inflammation, although it did promote systemic immune priming. Skin of neonatal mice and adult germ-free mice was seeded with low numbers of antigen-presenting cells and impaired chemokine and alarmin production. Enhanced chemokine and alarmin production, and seeding of the skin with antigen-presenting cells capable of instructing recruited cells to elicit their effector function, was, at least in part, dependent on formation of the microbiome, and consequently contributed to the development of overt skin disease.RESULTSA mixed TH2/TH17 inflammatory response in the skin and the lungs of adult mice was observed following sensitization and challenge. Comparatively, neonatal mice did not develop overt skin inflammation, but exhibited systemic release of IL-17a and a TH2-dominated lung response. Mechanical skin barrier disruption was not sufficient to drive allergic skin inflammation, although it did promote systemic immune priming. Skin of neonatal mice and adult germ-free mice was seeded with low numbers of antigen-presenting cells and impaired chemokine and alarmin production. Enhanced chemokine and alarmin production, and seeding of the skin with antigen-presenting cells capable of instructing recruited cells to elicit their effector function, was, at least in part, dependent on formation of the microbiome, and consequently contributed to the development of overt skin disease.These data shed light on the principles that underlie allergic inflammation in different tissues and highlight a window of opportunity that might exist for early-life prevention of allergic diseases.CONCLUSIONSThese data shed light on the principles that underlie allergic inflammation in different tissues and highlight a window of opportunity that might exist for early-life prevention of allergic diseases. BackgroundAllergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient or long-term in nature.ObjectiveWe sought to determine the immunologic rules that govern skin inflammation in early life.MethodsNeonatal and adult mice were epicutaneously sensitized with allergen followed by airway allergen challenge. Epicutaneous application of labeled allergen allowed for determination of antigen uptake and processing by antigen-presenting cells. RNAseq and microbiome analysis was performed on skin from neonatal and adult specific pathogen-free and germ-free mice.ResultsA mixed TH2/TH17 inflammatory response in the skin and the lungs of adult mice was observed following sensitization and challenge. Comparatively, neonatal mice did not develop overt skin inflammation, but exhibited systemic release of IL-17a and a TH2-dominated lung response. Mechanical skin barrier disruption was not sufficient to drive allergic skin inflammation, although it did promote systemic immune priming. Skin of neonatal mice and adult germ-free mice was seeded with low numbers of antigen-presenting cells and impaired chemokine and alarmin production. Enhanced chemokine and alarmin production, and seeding of the skin with antigen-presenting cells capable of instructing recruited cells to elicit their effector function, was, at least in part, dependent on formation of the microbiome, and consequently contributed to the development of overt skin disease.ConclusionsThese data shed light on the principles that underlie allergic inflammation in different tissues and highlight a window of opportunity that might exist for early-life prevention of allergic diseases. |
| Author | Ubags, Niki D. Pattaroni, Céline Trompette, Aurélien Rapin, Alexis Wong, Nicholas C. Nibbering, Britt Nicod, Laurent P. Marsland, Benjamin J. Pernot, Julie Harris, Nicola L. |
| Author_xml | – sequence: 1 givenname: Niki D. surname: Ubags fullname: Ubags, Niki D. email: Niki.ubags@chuv.ch organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland – sequence: 2 givenname: Aurélien surname: Trompette fullname: Trompette, Aurélien organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland – sequence: 3 givenname: Julie surname: Pernot fullname: Pernot, Julie organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland – sequence: 4 givenname: Britt surname: Nibbering fullname: Nibbering, Britt organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland – sequence: 5 givenname: Nicholas C. surname: Wong fullname: Wong, Nicholas C. organization: Monash Bioinformatics Platform, Monash University, Clayton, Australia – sequence: 6 givenname: Céline surname: Pattaroni fullname: Pattaroni, Céline organization: Department of Immunology and Pathology, Central Clinical School, Monash University, Melbourne, Australia – sequence: 7 givenname: Alexis surname: Rapin fullname: Rapin, Alexis organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland – sequence: 8 givenname: Laurent P. surname: Nicod fullname: Nicod, Laurent P. organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland – sequence: 9 givenname: Nicola L. surname: Harris fullname: Harris, Nicola L. organization: Department of Immunology and Pathology, Central Clinical School, Monash University, Melbourne, Australia – sequence: 10 givenname: Benjamin J. surname: Marsland fullname: Marsland, Benjamin J. email: Benjamin.marsland@monash.edu organization: Faculty of Biology and Medicine, University of Lausanne, Service de Pneumologie, CHUV – Epalinges, Epalinges, Switzerland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32679208$$D View this record in MEDLINE/PubMed |
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| Keywords | airway inflammation immune maturation TEWL AD cDC Epicutaneous sensitization early life Treg GO SPF allergy LTA-SA APC LC OVA GF |
| Language | English |
| License | Copyright © 2020 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. |
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| Snippet | Allergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is transient... BackgroundAllergic skin inflammation often presents in early childhood; however, little is known about the events leading to its initiation and whether it is... |
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| StartPage | 1049 |
| SubjectTerms | airway inflammation Allergens Allergic diseases Allergies allergy Animal models Antigen-presenting cells Antigens Chemokines Children Disease early life Effector cells Epicutaneous sensitization Flow cytometry Gene expression Germfree Helper cells Hypersensitivity immune maturation Inflammation Laboratories Lymphocytes Lymphocytes T Microbiomes Neonates Skin diseases Software Specific pathogen free |
| Title | Microbiome-induced antigen-presenting cell recruitment coordinates skin and lung allergic inflammation |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S0091674920309611 https://dx.doi.org/10.1016/j.jaci.2020.06.030 https://www.ncbi.nlm.nih.gov/pubmed/32679208 https://www.proquest.com/docview/2496206994 https://www.proquest.com/docview/2424996059 |
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