Stratification of asthma by lipidomic profiling of induced sputum supernatant.

Asthma epithelial lining fluid extracellular vesicles granulocytic inflammation induced sputum lipidomics molecular phenotyping pulmonary surfactant

Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
Jul 2023
Historique:
received: 09 08 2022
revised: 07 02 2023
accepted: 14 02 2023
medline: 10 7 2023
pubmed: 15 3 2023
entrez: 14 3 2023
Statut: ppublish

Résumé

Asthma is a chronic respiratory disease with significant heterogeneity in its clinical presentation and pathobiology. There is need for improved understanding of respiratory lipid metabolism in asthma patients and its relation to observable clinical features. We performed a comprehensive, prospective, cross-sectional analysis of the lipid composition of induced sputum supernatant obtained from asthma patients with a range of disease severities, as well as from healthy controls. Induced sputum supernatant was collected from 211 adults with asthma and 41 healthy individuals enrolled onto the U-BIOPRED (Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes) study. Sputum lipidomes were characterized by semiquantitative shotgun mass spectrometry and clustered using topologic data analysis to identify lipid phenotypes. Shotgun lipidomics of induced sputum supernatant revealed a spectrum of 9 molecular phenotypes, highlighting not just significant differences between the sputum lipidomes of asthma patients and healthy controls, but also within the asthma patient population. Matching clinical, pathobiologic, proteomic, and transcriptomic data helped inform the underlying disease processes. Sputum lipid phenotypes with higher levels of nonendogenous, cell-derived lipids were associated with significantly worse asthma severity, worse lung function, and elevated granulocyte counts. We propose a novel mechanism of increased lipid loading in the epithelial lining fluid of asthma patients resulting from the secretion of extracellular vesicles by granulocytic inflammatory cells, which could reduce the ability of pulmonary surfactant to lower surface tension in asthmatic small airways, as well as compromise its role as an immune regulator.

Sections du résumé

BACKGROUND BACKGROUND
Asthma is a chronic respiratory disease with significant heterogeneity in its clinical presentation and pathobiology. There is need for improved understanding of respiratory lipid metabolism in asthma patients and its relation to observable clinical features.
OBJECTIVE OBJECTIVE
We performed a comprehensive, prospective, cross-sectional analysis of the lipid composition of induced sputum supernatant obtained from asthma patients with a range of disease severities, as well as from healthy controls.
METHODS METHODS
Induced sputum supernatant was collected from 211 adults with asthma and 41 healthy individuals enrolled onto the U-BIOPRED (Unbiased Biomarkers for the Prediction of Respiratory Disease Outcomes) study. Sputum lipidomes were characterized by semiquantitative shotgun mass spectrometry and clustered using topologic data analysis to identify lipid phenotypes.
RESULTS RESULTS
Shotgun lipidomics of induced sputum supernatant revealed a spectrum of 9 molecular phenotypes, highlighting not just significant differences between the sputum lipidomes of asthma patients and healthy controls, but also within the asthma patient population. Matching clinical, pathobiologic, proteomic, and transcriptomic data helped inform the underlying disease processes. Sputum lipid phenotypes with higher levels of nonendogenous, cell-derived lipids were associated with significantly worse asthma severity, worse lung function, and elevated granulocyte counts.
CONCLUSION CONCLUSIONS
We propose a novel mechanism of increased lipid loading in the epithelial lining fluid of asthma patients resulting from the secretion of extracellular vesicles by granulocytic inflammatory cells, which could reduce the ability of pulmonary surfactant to lower surface tension in asthmatic small airways, as well as compromise its role as an immune regulator.

Identifiants

pubmed: 36918039
pii: S0091-6749(23)00293-2
doi: 10.1016/j.jaci.2023.02.032
pii:
doi:

Substances chimiques

Lipids 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

117-125

Informations de copyright

Copyright © 2023 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Joost Brandsma (J)

Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, United Kingdom; National Institute for Health Research Southampton Biomedical Research Centre, Southampton, United Kingdom. Electronic address: JBrandsma@aceso-sepsis.org.

James P R Schofield (JPR)

National Institute for Health Research Southampton Biomedical Research Centre, Southampton, United Kingdom; Centre for Proteomic Research, Biological Sciences, University of Southampton, Southampton, United Kingdom.

Xian Yang (X)

Data Science Institute, Imperial College, London, United Kingdom.

Fabio Strazzeri (F)

Mathematical Sciences, University of Southampton, Southampton, United Kingdom.

Clair Barber (C)

National Institute for Health Research Southampton Biomedical Research Centre, Southampton, United Kingdom.

Victoria M Goss (VM)

Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, United Kingdom; National Institute for Health Research Southampton Biomedical Research Centre, Southampton, United Kingdom.

Grielof Koster (G)

Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, United Kingdom; National Institute for Health Research Southampton Biomedical Research Centre, Southampton, United Kingdom.

Per S Bakke (PS)

Department of Clinical Science, University of Bergen, Bergen, Norway.

Massimo Caruso (M)

Department of Biomedical and Biotechnological Sciences, University of Catania, Catania, Italy.

Pascal Chanez (P)

Department of Respiratory Diseases, Aix-Marseille University, Marseille, France.

Sven-Erik Dahlén (SE)

Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden.

Stephen J Fowler (SJ)

Division of Infection, Immunity and Respiratory Medicine, School of Biological Sciences, University of Manchester, Manchester, United Kingdom; Manchester Academic Health Centre and NIHR Manchester Biomedical Research Centre, Manchester University Hospitals NHS Foundation Trust, Manchester, United Kingdom.

Ildikó Horváth (I)

Department of Pulmonology, Semmelweis University, Budapest, Hungary.

Norbert Krug (N)

Fraunhofer Institute for Toxicology and Experimental Medicine, Hannover, Germany.

Paolo Montuschi (P)

Department of Pharmacology, Faculty of Medicine, Catholic University of the Sacred Heart, Rome, Italy; National Heart and Lung Institute, Imperial College, London, United Kingdom.

Marek Sanak (M)

Department of Medicine, Jagiellonian University, Krakow, Poland.

Thomas Sandström (T)

Department of Public Health and Clinical Medicine, Umeå University, Umeå, Sweden.

Dominick E Shaw (DE)

National Institute for Health Research Biomedical Research Unit, University of Nottingham, Nottingham, United Kingdom.

Kian Fan Chung (KF)

National Heart and Lung Institute, Imperial College, London, United Kingdom.

Florian Singer (F)

Division of Paediatric Respiratory Medicine and Allergology, Department of Paediatrics, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland; Department of Paediatrics and Adolescent Medicine, Division of Paediatric Pulmonology and Allergology, Medical University of Graz, Graz, Austria.

Louise J Fleming (LJ)

National Heart and Lung Institute, Imperial College, London, United Kingdom.

Ian M Adcock (IM)

National Heart and Lung Institute, Imperial College, London, United Kingdom.

Ioannis Pandis (I)

Data Science Institute, Imperial College, London, United Kingdom.

Aruna T Bansal (AT)

Acclarogen Ltd, St John's Innovation Centre, Cambridge, United Kingdom.

Julie Corfield (J)

Areteva Ltd, Nottingham, United Kingdom.

Ana R Sousa (AR)

Respiratory Therapy Unit, GlaxoSmithKline, London, United Kingdom.

Peter J Sterk (PJ)

Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, the Netherlands.

Rubén J Sánchez-García (RJ)

Mathematical Sciences, University of Southampton, Southampton, United Kingdom.

Paul J Skipp (PJ)

Centre for Proteomic Research, Biological Sciences, University of Southampton, Southampton, United Kingdom.

Anthony D Postle (AD)

Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, United Kingdom.

Ratko Djukanović (R)

Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, United Kingdom; National Institute for Health Research Southampton Biomedical Research Centre, Southampton, United Kingdom.

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