Cited by 121Chronic Obstructive Pulmonary Disease (COPD) ResearchTelomeres, Telomerase, and SenescenceInflammatory mediators and NSAID effects

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The Cyclooxygenase-2–Prostaglandin E2 Pathway Maintains Senescence of Chronic Obstructive Pulmonary Disease Fibroblasts

Dagouassat, Maylis, Gagliolo, Jean-Marie, Chrusciel, Sandra, Bourin, Marie-Claude, Duprez, Corinne, Caramelle, Philippe, Boyer, Laurent, Hue, Sophie, Stern, Jean-Baptiste, Validire, Pierre, Longrois, Dan, Norel, Xavier, Dubois-Randé, Jean-Luc, Le Gouvello, Sabine, Adnot, Serge, Boczkowski, Jorge·2013·American Journal of Respiratory and Critical Care Medicine

DOI 10.1164/rccm.201208-1361oc

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Abstract

Rationale: Chronic obstructive pulmonary disease (COPD) is associated with lung fibroblast senescence, a process characterized by the irreversible loss of replicative capacity associated with the secretion of inflammatory mediators. However, the mechanisms of this phenomenon remain poorly defined. Objectives: The aim of this study was to analyze the role of prostaglandin E2 (PGE2), a prostaglandin known to be increased in COPD lung fibroblasts, in inducing senescence and related inflammation in vitro in lung fibroblasts and in vivo in mice. Methods: Fibroblasts were isolated from patients with COPD and from smoker and nonsmoker control subjects. Senescence markers and inflammatory mediators were investigated in fibroblasts and in mice. Measurements and Main Results: Lung fibroblasts from patients with COPD exhibited higher expression of PGE2 receptors EP2 and EP4 as compared with nonsmoker and smoker control subjects. Compared with both nonsmoker and smoker control subjects, during long-term culture, COPD fibroblasts displayed increased senescent markers (increased senescence associated-β galactosidase activity, p16, and p53 expression and lower proliferative capacity), and an increased PGE2, IL-6, IL-8, growth-regulated oncogene (GRO), CX3CL1, and matrix metalloproteinase-2 protein and cyclooxygenase-2 and mPGES-1 mRNA expression. Using in vitro pharmacologic approaches and in vivo experiments in wild-type and p53−/− mice we demonstrated that PGE2 produced by senescent COPD fibroblasts is responsible for the increased senescence and related inflammation. PGE2 acts either in a paracrine or autocrine fashion by a pathway involving EP2 and EP4 prostaglandin receptors, cyclooxygenase-2–dependent reactive oxygen species production and signaling, and consecutive p53 activation. Conclusions: PGE2 is a critical component of an amplifying and self-perpetuating circle inducing senescence and inflammation in COPD fibroblasts. Modulating the described PGE2 signaling pathway could provide a new basis to dampen senescence and senescence-associated inflammation in COPD.

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Authors: Dagouassat, M., Gagliolo, J.-M., Chrusciel, S., Bourin, M.-C., Duprez, C., Caramelle, P., Boyer, L., Hue, S., Stern, J.-B., Validire, P., Longrois, D., Norel, X., Dubois-Randé, J.-L., Le Gouvello, S., Adnot, S., & Boczkowski, J.
Affiliations: Inserm (FR)
Service d’Immunologie Biologique
Faculté de Médecine, Université Paris-Est, UMR U955, Créteil, France
Département Thoracique and
Institute Mutualiste Montsouris (FR)
Corresponding author: Boczkowski, Jorge
ORCID: Dagouassat, Maylis
Boyer, Laurent
Stern, Jean-Baptiste
Validire, Pierre
Longrois, Dan
Norel, Xavier
Adnot, Serge
Boczkowski, Jorge
Venue: American Journal of Respiratory and Critical Care Medicine
Publisher: Oxford University Press (OUP)
Published: 2013-04-01
Volume: 187
Issue: 7
Pages: 703-714
ISSN: 1073-449X (ISSN-L)
1535-4970
DOI: 10.1164/rccm.201208-1361oc
OpenAlex: W2034209637
Cited by: 120
References: 52
Citations by year: 2026: 7 · 2025: 12 · 2024: 7 · 2023: 11 · 2022: 9 · 2021: 11 · 2020: 8 · 2019: 5 · 2018: 10 · 2017: 3 · 2016: 8 · 2015: 14 · 2014: 13 · 2013: 2
FWCI: 10.03
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: American Journal of Respiratory and Critical Care Medicine (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
Health Sciences › Medicine › Pharmacology (medical) › Inflammatory mediators and NSAID effects
Keywords: chronic obstructive pulmonary disease, fibroblast senescence, cyclooxygenase-2, prostaglandin E2, EP2 receptor, EP4 receptor, senescence-associated inflammation, p53 activation, reactive oxygen species, MMP-2, interleukin-6, interleukin-8, smoking, senescence-associated β-galactosidase, p16
MeSH terms: Adult, Aged, Aged, 80 and over, Aging, Animals, Cells, Cultured, Female, Fibroblasts, Humans, Lung, Male, Mice, Inbred C57BL, Middle Aged, Dinoprostone, Case-Control Studies, Genes, p53, Reactive Oxygen Species, Statistics, Nonparametric, Autocrine Communication, Paracrine Communication, Pulmonary Disease, Chronic Obstructive, Mice, Cyclooxygenase 2, Receptors, Prostaglandin E, EP2 Subtype, Receptors, Prostaglandin E, EP4 Subtype

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The Cyclooxygenase-2–Prostaglandin E2 Pathway Maintains Senescence of Chronic Obstructive Pulmonary Disease Fibroblasts

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