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Pseudomonas aeruginosa eradicates Staphylococcus aureus by manipulating the host immunity

Authors :
Pierre-Régis Burgel
Isabelle Sermet-Gaudelus
Louise Jeammet
Gérard Lambeau
Lhousseine Touqui
Dominique Leduc
Michel Chignard
Laurent Guillemot
Clémence Martin
Philippe Morand
Dorota Sands
Yongzheng Wu
Erwan Pernet
Défense innée et inflammation
Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM)
Cellule Pasteur UPMC
Institut Pasteur [Paris] (IP)-Sorbonne Université (SU)
Université Paris Descartes - Paris 5 (UPD5)
Service de pneumologie [CHU Cochin]
Hôpital Cochin [AP-HP]
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)
Institut de pharmacologie moléculaire et cellulaire (IPMC)
Université Nice Sophia Antipolis (1965 - 2019) (UNS)
COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Centre National de la Recherche Scientifique (CNRS)-Université Côte d'Azur (UCA)
Service de Pneumologie et d'Allergologie Pédiatriques
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-CHU Necker - Enfants Malades [AP-HP]
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)
Régulation du transport anionique transépithélial : de la recherche fondamentale aux pathologies épithéliales (UMR_S 806)
Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
National Research Institute of Mother and Child [Warsaw, Poland]
Service de Bactériologie [CHU Cochin, AP-HP]
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Hôpital Cochin [AP-HP]
This study was supported by France ‘Vaincre la Mucoviscidose’ and ‘DIM Malinf-Region Ile de France’ foundation.
We thank Dr R. Ramphal (University of Florida, Gainesville, FL, USA), Dr T. Msadek (Institut Pasteur, Paris), Dr E. Pearlman (Case Western Reserve University, Cleveland, OH, USA), Dr J.C. Olson (West Virginia University, Morgantown, WV, USA), Dr P. Peris (University of València, Spain), Dr M. Gelb (University of Washington, Seattle, WA, USA) for providing PA and SA strains as well as substrate for sPLA2 activity assay and RO032007A compound
Dr C. Schmitt (Hôpital Trousseau, Paris) for providing expectorations of children patients
V. Balloy and M. Nahori (Institut Pasteur, Paris) for technical assistance with intratracheal and intravenous instillation and C. Payre for helpful advices in sPLA2 analyses.
Wu, Yongzheng
Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM)
Institut Pasteur [Paris]-Sorbonne Université (SU)
Centre National de la Recherche Scientifique (CNRS)-Université Nice Sophia Antipolis (... - 2019) (UNS)
COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Université Côte d'Azur (UCA)
Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris Descartes - Paris 5 (UPD5)
Source :
Nature Communications, Nature Communications, 2014, 5 (1), pp.5105. ⟨10.1038/ncomms6105⟩, Nature Communications, Nature Publishing Group, 2014, 5 (1), pp.5105. ⟨10.1038/ncomms6105⟩
Publication Year :
2014
Publisher :
Springer Science and Business Media LLC, 2014.

Abstract

International audience; Young cystic fibrosis (CF) patients' airways are mainly colonized by Staphylococcus aureus, while Pseudomonas aeruginosa predominates in adults. However, the mechanisms behind this infection switch are unclear. Here, we show that levels of type-IIA-secreted phospholipase A2 (sPLA2-IIA, a host enzyme with bactericidal activity) increase in expectorations of CF patients in an age-dependent manner. These levels are sufficient to kill S. aureus, with marginal effects on P. aeruginosa strains. P. aeruginosa laboratory strains and isolates from CF patients induce sPLA2-IIA expression in bronchial epithelial cells from CF patients (these cells are a major source of the enzyme). In an animal model of lung infection, P. aeruginosa induces sPLA2-IIA production that favours S. aureus killing. We suggest that sPLA2-IIA induction by P. aeruginosa contributes to S. aureus eradication in CF airways. Our results indicate that a bacterium can eradicate another bacterium by manipulating the host immunity.

Subjects

Subjects :
Cystic Fibrosis
MESH: ADP Ribose Transferases
General Physics and Astronomy
MESH: Staphylococcus aureus / physiology
medicine.disease_cause
[SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity
Cystic fibrosis
Mice
[SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases
MESH: Child
MESH: Respiratory Mucosa
MESH: Animals
Child
ADP Ribose Transferases
MESH: Sputum / enzymology
0303 health sciences
Multidisciplinary
MESH: Bronchi
respiratory system
3. Good health
MESH: Young Adult
Staphylococcus aureus
Child, Preschool
Pseudomonas aeruginosa
Disease Progression
[SDV.MHEP.MI] Life Sciences [q-bio]/Human health and pathology/Infectious diseases
MESH: Disease Progression
Adult
Host immunity
Adolescent
Bacterial Toxins
Guinea Pigs
Bronchi
Respiratory Mucosa
MESH: Epithelial Cells / enzymology
Biology
Group II Phospholipases A2
General Biochemistry, Genetics and Molecular Biology
MESH: Guinea Pigs
Microbiology
Young Adult
03 medical and health sciences
MESH: Pseudomonas aeruginosa / physiology
medicine
Animals
Humans
MESH: Mice
[SDV.IMM.II] Life Sciences [q-bio]/Immunology/Innate immunity
030304 developmental biology
MESH: Adolescent
Respiratory tract diseases
MESH: Humans
MESH: Group II Phospholipases A2 / metabolism
030306 microbiology
MESH: Child, Preschool
Sputum
Epithelial Cells
MESH: Adult
General Chemistry
medicine.disease
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
respiratory tract diseases
MESH: Bacterial Toxins
Immunology
MESH: Cystic Fibrosis / enzymology
Bacterial infection
[SDV.MP.BAC] Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
MESH: Cystic Fibrosis / microbiology

Details

ISSN :
20411723
Volume :
5
Database :
OpenAIRE
Journal :
Nature Communications
Accession number :
edsair.doi.dedup.....1f06fb088795a54d7501c15fac13411f
Full Text :
https://doi.org/10.1038/ncomms6105