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Deep multi-omic profiling reveals molecular signatures that underpin preschool wheeze and asthma

Deep multi-omic profiling reveals molecular signatures that underpin preschool wheeze and asthma
Deep multi-omic profiling reveals molecular signatures that underpin preschool wheeze and asthma

BACKGROUND: Wheezing in childhood is prevalent, with over half of all children experiencing at least one episode by age six. The pathophysiology of wheeze, especially why some children develop asthma while others do not, remains unclear.

OBJECTIVE: This study addresses the knowledge gap by investigating the transition from preschool wheeze to asthma using multi-omic profiling.

METHODS: Unsupervised, group-agnostic integrative multi-omic factor analysis was performed using host/bacterial (meta-)transcriptomic and bacterial shotgun metagenomic datasets from bronchial brush samples paired with metabolomic/lipidomic data from bronchoalveolar lavage samples acquired from children 1-17 years old.

RESULTS: Two multi-omic factors were identified: one characterising preschool-aged recurrent wheeze and another capturing an inferred trajectory from health to wheeze and school-aged asthma. Recurrent wheeze was driven by Type 1-immune signatures, coupled with upregulation of immune-related and neutrophil-associated lipids and metabolites. Comparatively, progression towards asthma from ages 1-18 was dominated by changes related to airway epithelial cell gene expression, Type 2-immune responses, and constituents of the airway microbiome, such as increased Haemophilus influenzae.

CONCLUSION: These factors highlighted distinctions between an inflammation-related phenotype in preschool wheeze, and the predominance of airway epithelial-related changes linked with the inferred trajectory toward asthma. These findings provide insights into the differential mechanisms driving the progression from wheeze to asthma and may inform targeted therapeutic strategies.

Wheeze, asthma, disease trajectory, gene expression, lipidomics, metabolomics, metagenomics, multiomics
0091-6749
Macowan, Matthew
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Pattaroni, Céline
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Bonner, Katie
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Chatzis, Roxanne
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Daunt, Carmel
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Gore, Mindy
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Custovic, Adnan
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Shields, Michael D
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Power, Ultan F
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Grigg, Jonathan
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Roberts, Graham
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Ghazal, Peter
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Schwarze, Jürgen
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Turner, Steve
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Bush, Andrew
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Saglani, Sejal
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Lloyd, Clare M
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Marsland, Benjamin J
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Macowan, Matthew
467ad6da-91a4-4721-a036-70303ef73452
Pattaroni, Céline
25092aed-88a8-4c20-9913-11a0e223373e
Bonner, Katie
a07914de-8fea-4482-8f6c-21cc37292259
Chatzis, Roxanne
aba5a5f5-6cef-4220-9478-7df6c53c4805
Daunt, Carmel
35ada135-9ec4-492c-a851-a9ba4d9db0e8
Gore, Mindy
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Custovic, Adnan
17d8d092-73b8-44fb-bf48-5cea7b29e3fc
Shields, Michael D
5cc8438d-407a-4f01-bb25-e245c83ca4e4
Power, Ultan F
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Grigg, Jonathan
587e2313-7a36-4d61-8010-45447565cfcd
Roberts, Graham
ea00db4e-84e7-4b39-8273-9b71dbd7e2f3
Ghazal, Peter
9abf47a0-13df-439c-b434-7f6248e39135
Schwarze, Jürgen
ae3e1b31-9050-454b-bca3-f29ceb7ac950
Turner, Steve
db854915-7aa0-4c38-b2f7-9ec23b1d2828
Bush, Andrew
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Saglani, Sejal
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Lloyd, Clare M
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Marsland, Benjamin J
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Macowan, Matthew, Pattaroni, Céline, Bonner, Katie, Chatzis, Roxanne, Daunt, Carmel, Gore, Mindy, Custovic, Adnan, Shields, Michael D, Power, Ultan F, Grigg, Jonathan, Roberts, Graham, Ghazal, Peter, Schwarze, Jürgen, Turner, Steve, Bush, Andrew, Saglani, Sejal, Lloyd, Clare M and Marsland, Benjamin J (2024) Deep multi-omic profiling reveals molecular signatures that underpin preschool wheeze and asthma. The Journal of Allergy and Clinical Immunology. (doi:10.1016/j.jaci.2024.08.017).

Record type: Article

Abstract

BACKGROUND: Wheezing in childhood is prevalent, with over half of all children experiencing at least one episode by age six. The pathophysiology of wheeze, especially why some children develop asthma while others do not, remains unclear.

OBJECTIVE: This study addresses the knowledge gap by investigating the transition from preschool wheeze to asthma using multi-omic profiling.

METHODS: Unsupervised, group-agnostic integrative multi-omic factor analysis was performed using host/bacterial (meta-)transcriptomic and bacterial shotgun metagenomic datasets from bronchial brush samples paired with metabolomic/lipidomic data from bronchoalveolar lavage samples acquired from children 1-17 years old.

RESULTS: Two multi-omic factors were identified: one characterising preschool-aged recurrent wheeze and another capturing an inferred trajectory from health to wheeze and school-aged asthma. Recurrent wheeze was driven by Type 1-immune signatures, coupled with upregulation of immune-related and neutrophil-associated lipids and metabolites. Comparatively, progression towards asthma from ages 1-18 was dominated by changes related to airway epithelial cell gene expression, Type 2-immune responses, and constituents of the airway microbiome, such as increased Haemophilus influenzae.

CONCLUSION: These factors highlighted distinctions between an inflammation-related phenotype in preschool wheeze, and the predominance of airway epithelial-related changes linked with the inferred trajectory toward asthma. These findings provide insights into the differential mechanisms driving the progression from wheeze to asthma and may inform targeted therapeutic strategies.

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More information

Accepted/In Press date: 23 August 2024
e-pub ahead of print date: 28 August 2024
Additional Information: Copyright © 2024. Published by Elsevier Inc.
Keywords: Wheeze, asthma, disease trajectory, gene expression, lipidomics, metabolomics, metagenomics, multiomics

Identifiers

Local EPrints ID: 494127
URI: http://eprints.soton.ac.uk/id/eprint/494127
ISSN: 0091-6749
PURE UUID: 40d5dcaa-9fc5-4818-93f8-b1a9ae053e04
ORCID for Graham Roberts: ORCID iD orcid.org/0000-0003-2252-1248

Catalogue record

Date deposited: 24 Sep 2024 16:46
Last modified: 01 Oct 2024 01:41

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Contributors

Author: Matthew Macowan
Author: Céline Pattaroni
Author: Katie Bonner
Author: Roxanne Chatzis
Author: Carmel Daunt
Author: Mindy Gore
Author: Adnan Custovic
Author: Michael D Shields
Author: Ultan F Power
Author: Jonathan Grigg
Author: Graham Roberts ORCID iD
Author: Peter Ghazal
Author: Jürgen Schwarze
Author: Steve Turner
Author: Andrew Bush
Author: Sejal Saglani
Author: Clare M Lloyd
Author: Benjamin J Marsland

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