Evidence of early increased sialylation of airway mucins and defective mucociliary clearance in CFTR-deficient piglets.


Journal

Journal of cystic fibrosis : official journal of the European Cystic Fibrosis Society
ISSN: 1873-5010
Titre abrégé: J Cyst Fibros
Pays: Netherlands
ID NLM: 101128966

Informations de publication

Date de publication:
01 2021
Historique:
received: 30 01 2020
revised: 29 06 2020
accepted: 09 09 2020
pubmed: 27 9 2020
medline: 15 12 2021
entrez: 26 9 2020
Statut: ppublish

Résumé

Bacterial colonization in cystic fibrosis (CF) lungs has been directly associated to the loss of CFTR function, and/or secondarily linked to repetitive cycles of chronic inflammation/infection. We hypothesized that altered molecular properties of mucins could contribute to this process. Newborn CFTR We provide evidence of an increased sialylation of CF airway mucins and impaired mucociliary transport that occur before the onset of inflammation. Hypersialylation of mucins was reproduced on tracheal explants from non CF animals treated with GlyH101, an inhibitor of CFTR channel activity, indicating a causal relationship between the absence of CFTR expression and the sialylation of mucins. This increased sialylation was correlated to an increased adherence of P. aeruginosa to mucins. In vivo infection of newborn CF piglets by live luminescent P. aeruginosa demonstrated an impairment of mucociliary transport of this bacterium, with no evidence of pre-existing inflammation. Our results document for the first time in a well-defined CF animal model modifications that affect the O-glycan chains of mucins. These alterations precede infection and inflammation of airway tissues, and provide a favorable context for microbial development in CF lung that hallmarks this disease.

Sections du résumé

BACKGROUND
Bacterial colonization in cystic fibrosis (CF) lungs has been directly associated to the loss of CFTR function, and/or secondarily linked to repetitive cycles of chronic inflammation/infection. We hypothesized that altered molecular properties of mucins could contribute to this process.
METHODS
Newborn CFTR
RESULTS
We provide evidence of an increased sialylation of CF airway mucins and impaired mucociliary transport that occur before the onset of inflammation. Hypersialylation of mucins was reproduced on tracheal explants from non CF animals treated with GlyH101, an inhibitor of CFTR channel activity, indicating a causal relationship between the absence of CFTR expression and the sialylation of mucins. This increased sialylation was correlated to an increased adherence of P. aeruginosa to mucins. In vivo infection of newborn CF piglets by live luminescent P. aeruginosa demonstrated an impairment of mucociliary transport of this bacterium, with no evidence of pre-existing inflammation.
CONCLUSIONS
Our results document for the first time in a well-defined CF animal model modifications that affect the O-glycan chains of mucins. These alterations precede infection and inflammation of airway tissues, and provide a favorable context for microbial development in CF lung that hallmarks this disease.

Identifiants

pubmed: 32978064
pii: S1569-1993(20)30868-7
doi: 10.1016/j.jcf.2020.09.009
pii:
doi:

Substances chimiques

Mucins 0
Cystic Fibrosis Transmembrane Conductance Regulator 126880-72-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

173-182

Informations de copyright

Copyright © 2020. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare no conflict of interests.

Auteurs

Ignacio Caballero (I)

INRAE, Université de Tours, ISP, Nouzilly F-37380, France.

Bélinda Ringot-Destrez (B)

Univ.lille, CNRS, UMR8576-UGSF-Unité de Glycobiologie Structurale et Fonctionnelle, Lille F59000, France.

Mustapha Si-Tahar (M)

Université de Tours, Tours 37000, France; INSERM U1100, Centre d'étude des pathologies respiratoires (CEPR), Tours 37000, France.

Pascal Barbry (P)

Université Côte d'Azur, CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Sophia Antipolis F06560, France.

Antoine Guillon (A)

Université de Tours, Tours 37000, France; INSERM U1100, Centre d'étude des pathologies respiratoires (CEPR), Tours 37000, France; CHU Tours, service de Médecine Intensive-Réanimation, Tours, France.

Isabelle Lantier (I)

INRAE, Université de Tours, ISP, Nouzilly F-37380, France.

Mustapha Berri (M)

INRAE, Université de Tours, ISP, Nouzilly F-37380, France.

Claire Chevaleyre (C)

INRAE, Université de Tours, ISP, Nouzilly F-37380, France.

Isabelle Fleurot (I)

INRAE, Université de Tours, ISP, Nouzilly F-37380, France.

Céline Barc (C)

Plateforme d'Infectiologie expérimentale (UE-1277 PFIE), INRA, Nouzilly, France.

Reuben Ramphal (R)

Université de Tours, Tours 37000, France; INSERM U1100, Centre d'étude des pathologies respiratoires (CEPR), Tours 37000, France.

Nicolas Pons (N)

Université Côte d'Azur, CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Sophia Antipolis F06560, France.

Agnès Paquet (A)

Université Côte d'Azur, CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Sophia Antipolis F06560, France.

Kévin Lebrigand (K)

Université Côte d'Azur, CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Sophia Antipolis F06560, France.

Carole Baron (C)

Université Côte d'Azur, CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Sophia Antipolis F06560, France.

Andrea Bähr (A)

CIMM-Gene Center and Center for Innovative Medical Models, LMU Munich, Germany.

Nikolai Klymiuk (N)

CIMM-Gene Center and Center for Innovative Medical Models, LMU Munich, Germany.

Renaud Léonard (R)

Univ.lille, CNRS, UMR8576-UGSF-Unité de Glycobiologie Structurale et Fonctionnelle, Lille F59000, France.

Catherine Robbe-Masselot (C)

Univ.lille, CNRS, UMR8576-UGSF-Unité de Glycobiologie Structurale et Fonctionnelle, Lille F59000, France. Electronic address: catherine.robbe-masselot@univ-lille.fr.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH