Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro

Ellen Goeteyn; Steven L. Taylor; Alison Dicker; Laura Bollé; Merel Wauters; Marie Joossens; Eva Van Braeckel; Jodie L. Simpson; Lucy Burr; James D. Chalmers; Geraint B. Rogers; Aurélie Crabbé

doi:10.1186/s12931-024-02983-z

Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro

Ellen Goeteyn, Steven L. Taylor, Alison Dicker, Laura Bollé, Merel Wauters, Marie Joossens, Eva Van Braeckel, Jodie L. Simpson, Lucy Burr, James D. Chalmers, Geraint B. Rogers, Aurélie Crabbé (Lead / Corresponding author)

Research output: Contribution to journal › Article › peer-review

37 Downloads (Pure)

Abstract

Background

Chronic airway disease (CAD) is characterized by chronic airway inflammation and colonization of the lungs by pro-inflammatory pathogens. However, while various other bacterial species are present in the lower airways, it is not fully understood how they influence inflammation. We aimed to identify novel anti-inflammatory species present in lower airway samples of patients with CAD.

Methods

Paired sputum microbiome and inflammatory marker data of adults with CAD across three separate cohorts (Australian asthma and bronchiectasis, Scottish bronchiectasis) was analyzed using Linear discriminant analysis Effect Size (LEfSE) and Spearman correlation analysis to identify species associated with a low inflammatory profile in patients.

Results

We identified the genus Aggregatibacter as more abundant in patients with lower levels of airway inflammatory markers in two CAD cohorts (Australian asthma and bronchiectasis). In addition, the relative abundance of Aggregatibacter was inversely correlated with sputum IL-8 (Australian bronchiectasis) and IL-1β levels (Australian asthma and bronchiectasis). Subsequent in vitro testing, using a physiologically relevant three-dimensional lung epithelial cell model, revealed that Aggregatibacter spp. (i.e. A. actinomycetemcomitans, A. aphrophilus) and their cell-free supernatant exerted anti-inflammatory activity without influencing host cell viability.

Conclusions

These findings suggest that Aggregatibacter spp. might act to reduce airway inflammation in CAD patients.

Original language	English
Article number	368
Number of pages	14
Journal	Respiratory Research
Volume	25
DOIs	https://doi.org/10.1186/s12931-024-02983-z
Publication status	Published - 12 Oct 2024

ASJC Scopus subject areas

Pulmonary and Respiratory Medicine

Access to Document

10.1186/s12931-024-02983-zLicence: CC BY-NC-ND

Final Published VersionFinal published version, 2.97 MBLicence: CC BY-NC-ND

Cite this

Goeteyn, E., Taylor, S. L., Dicker, A., Bollé, L., Wauters, M., Joossens, M., Van Braeckel, E., Simpson, J. L., Burr, L., Chalmers, J. D., Rogers, G. B., & Crabbé, A. (2024). Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro. Respiratory Research, 25, Article 368. https://doi.org/10.1186/s12931-024-02983-z

@article{fa3a0371caae4008bef68c21bb367fb3,

title = "Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro",

abstract = "Background Chronic airway disease (CAD) is characterized by chronic airway inflammation and colonization of the lungs by pro-inflammatory pathogens. However, while various other bacterial species are present in the lower airways, it is not fully understood how they influence inflammation. We aimed to identify novel anti-inflammatory species present in lower airway samples of patients with CAD. Methods Paired sputum microbiome and inflammatory marker data of adults with CAD across three separate cohorts (Australian asthma and bronchiectasis, Scottish bronchiectasis) was analyzed using Linear discriminant analysis Effect Size (LEfSE) and Spearman correlation analysis to identify species associated with a low inflammatory profile in patients. Results We identified the genus Aggregatibacter as more abundant in patients with lower levels of airway inflammatory markers in two CAD cohorts (Australian asthma and bronchiectasis). In addition, the relative abundance of Aggregatibacter was inversely correlated with sputum IL-8 (Australian bronchiectasis) and IL-1β levels (Australian asthma and bronchiectasis). Subsequent in vitro testing, using a physiologically relevant three-dimensional lung epithelial cell model, revealed that Aggregatibacter spp. (i.e. A. actinomycetemcomitans, A. aphrophilus) and their cell-free supernatant exerted anti-inflammatory activity without influencing host cell viability. Conclusions These findings suggest that Aggregatibacter spp. might act to reduce airway inflammation in CAD patients.",

author = "Ellen Goeteyn and Taylor, {Steven L.} and Alison Dicker and Laura Boll{\'e} and Merel Wauters and Marie Joossens and {Van Braeckel}, Eva and Simpson, {Jodie L.} and Lucy Burr and Chalmers, {James D.} and Rogers, {Geraint B.} and Aur{\'e}lie Crabb{\'e}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = oct,

day = "12",

doi = "10.1186/s12931-024-02983-z",

language = "English",

volume = "25",

journal = "Respiratory Research",

issn = "1465-9921",

publisher = "BioMed Central",

}

Goeteyn, E, Taylor, SL, Dicker, A, Bollé, L, Wauters, M, Joossens, M, Van Braeckel, E, Simpson, JL, Burr, L, Chalmers, JD, Rogers, GB & Crabbé, A 2024, 'Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro', Respiratory Research, vol. 25, 368. https://doi.org/10.1186/s12931-024-02983-z

TY - JOUR

T1 - Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro

AU - Goeteyn, Ellen

AU - Taylor, Steven L.

AU - Dicker, Alison

AU - Bollé, Laura

AU - Wauters, Merel

AU - Joossens, Marie

AU - Van Braeckel, Eva

AU - Simpson, Jodie L.

AU - Burr, Lucy

AU - Chalmers, James D.

AU - Rogers, Geraint B.

AU - Crabbé, Aurélie

PY - 2024/10/12

Y1 - 2024/10/12

N2 - Background Chronic airway disease (CAD) is characterized by chronic airway inflammation and colonization of the lungs by pro-inflammatory pathogens. However, while various other bacterial species are present in the lower airways, it is not fully understood how they influence inflammation. We aimed to identify novel anti-inflammatory species present in lower airway samples of patients with CAD. Methods Paired sputum microbiome and inflammatory marker data of adults with CAD across three separate cohorts (Australian asthma and bronchiectasis, Scottish bronchiectasis) was analyzed using Linear discriminant analysis Effect Size (LEfSE) and Spearman correlation analysis to identify species associated with a low inflammatory profile in patients. Results We identified the genus Aggregatibacter as more abundant in patients with lower levels of airway inflammatory markers in two CAD cohorts (Australian asthma and bronchiectasis). In addition, the relative abundance of Aggregatibacter was inversely correlated with sputum IL-8 (Australian bronchiectasis) and IL-1β levels (Australian asthma and bronchiectasis). Subsequent in vitro testing, using a physiologically relevant three-dimensional lung epithelial cell model, revealed that Aggregatibacter spp. (i.e. A. actinomycetemcomitans, A. aphrophilus) and their cell-free supernatant exerted anti-inflammatory activity without influencing host cell viability. Conclusions These findings suggest that Aggregatibacter spp. might act to reduce airway inflammation in CAD patients.

AB - Background Chronic airway disease (CAD) is characterized by chronic airway inflammation and colonization of the lungs by pro-inflammatory pathogens. However, while various other bacterial species are present in the lower airways, it is not fully understood how they influence inflammation. We aimed to identify novel anti-inflammatory species present in lower airway samples of patients with CAD. Methods Paired sputum microbiome and inflammatory marker data of adults with CAD across three separate cohorts (Australian asthma and bronchiectasis, Scottish bronchiectasis) was analyzed using Linear discriminant analysis Effect Size (LEfSE) and Spearman correlation analysis to identify species associated with a low inflammatory profile in patients. Results We identified the genus Aggregatibacter as more abundant in patients with lower levels of airway inflammatory markers in two CAD cohorts (Australian asthma and bronchiectasis). In addition, the relative abundance of Aggregatibacter was inversely correlated with sputum IL-8 (Australian bronchiectasis) and IL-1β levels (Australian asthma and bronchiectasis). Subsequent in vitro testing, using a physiologically relevant three-dimensional lung epithelial cell model, revealed that Aggregatibacter spp. (i.e. A. actinomycetemcomitans, A. aphrophilus) and their cell-free supernatant exerted anti-inflammatory activity without influencing host cell viability. Conclusions These findings suggest that Aggregatibacter spp. might act to reduce airway inflammation in CAD patients.

UR - http://www.scopus.com/inward/record.url?scp=85206122858&partnerID=8YFLogxK

U2 - 10.1186/s12931-024-02983-z

DO - 10.1186/s12931-024-02983-z

M3 - Article

C2 - 39395980

AN - SCOPUS:85206122858

SN - 1465-9921

VL - 25

JO - Respiratory Research

JF - Respiratory Research

M1 - 368

ER -

Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro

Abstract

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Human COPD lung microbiome

Project: PRJEB71587

Human respiratory disease lung microbiome

Cite this

Aggregatibacter is inversely associated with inflammatory mediators in sputa of patients with chronic airway diseases and reduces inflammation in vitro

Abstract

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Datasets

Human COPD lung microbiome

Project: PRJEB71587

Human respiratory disease lung microbiome

Cite this