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Coxiella burnetii, the agent of Q fever, replicates within trophoblasts and induces a unique transcriptional response

Authors :
Christian Capo
Florence Bretelle
J. L. Mege
Yannick Le Priol
Catherine Lepolard
Eric Ghigo
Emmanuel Lemichez
Amira Ben Amara
Suzana P. Salcedo
Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE)
Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR48
Institut des sciences biologiques (INSB-CNRS)-Institut des sciences biologiques (INSB-CNRS)-Centre National de la Recherche Scientifique (CNRS)
Laboratoire d'immunologie
Assistance Publique - Hôpitaux de Marseille (APHM)-Hôpital Sainte-Marguerite [CHU - APHM] (Hôpitaux Sud )
Centre d'Immunologie de Marseille - Luminy (CIML)
Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
Toxines bactériennes dans la relation hôtes-pathogènes
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)-IFR50-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Côte d'Azur (UCA)
INSB-INSB-Centre National de la Recherche Scientifique (CNRS)
Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)
Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR50-Université Côte d'Azur (UCA)-Université Nice Sophia Antipolis (... - 2019) (UNS)
COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)
Haon, Marie Laure
Source :
PLoS ONE, PLoS ONE, 2010, 5 (12), pp.e15315. ⟨10.1371/journal.pone.0015315⟩, PLoS ONE, Public Library of Science, 2010, 5 (12), pp.e15315. ⟨10.1371/journal.pone.0015315⟩, PLoS ONE, Vol 5, Iss 12, p e15315 (2010)
Publication Year :
2010
Publisher :
HAL CCSD, 2010.

Abstract

International audience; Q fever is a zoonosis caused by Coxiella burnetii, an obligate intracellular bacterium typically found in myeloid cells. The infection is a source of severe obstetrical complications in humans and cattle and can undergo chronic evolution in a minority of pregnant women. Because C. burnetii is found in the placentas of aborted fetuses, we investigated the possibility that it could infect trophoblasts. Here, we show that C. burnetii infected and replicated in BeWo trophoblasts within phagolysosomes. Using pangenomic microarrays, we found that C. burnetii induced a specific transcriptomic program. This program was associated with the modulation of inflammatory responses that were shared with inflammatory agonists, such as TNF, and more specific responses involving genes related to pregnancy development, including EGR-1 and NDGR1. In addition, C. burnetii stimulated gene networks organized around the IL-6 and IL-13 pathways, which both modulate STAT3. Taken together, these results revealed that trophoblasts represent a protective niche for C. burnetii. The activation program induced by C. burnetii in trophoblasts may allow bacterial replication but seems unable to interfere with the development of normal pregnancy. Such pathophysiologocal processes should require the activation of immune placental cells associated with trophoblasts.

Subjects

Subjects :
Proteomics
Bacterial Diseases
MESH: Inflammation
MESH: Interleukin-13
Transcription, Genetic
Microarrays
MESH: Trophoblasts
Placenta
lcsh:Medicine
Apoptosis
Mice
Pregnancy
Phagosomes
MESH: Early Growth Response Protein 1
Gram Negative
MESH: Animals
lcsh:Science
reproductive and urinary physiology
Phagosome
Oligonucleotide Array Sequence Analysis
0303 health sciences
Multidisciplinary
Spectrometric Identification of Proteins
Interleukin-13
biology
Obstetrics and Gynecology
MESH: STAT3 Transcription Factor
3. Good health
Bacterial Pathogens
Trophoblasts
medicine.anatomical_structure
Infectious Diseases
Phenotype
Coxiella burnetii
Interleukin 13
embryonic structures
Medicine
Cytokines
[SDV.IMM]Life Sciences [q-bio]/Immunology
Tumor necrosis factor alpha
medicine.symptom
Q Fever
Research Article
Q-Fever
STAT3 Transcription Factor
MESH: Q Fever
[SDV.IMM] Life Sciences [q-bio]/Immunology
Inflammation
Q fever
MESH: Phenotype
Microbiology
03 medical and health sciences
MESH: Gene Expression Profiling
Immune system
MESH: Phagosomes
medicine
Animals
Biology
Microbial Pathogens
MESH: Mice
030304 developmental biology
Early Growth Response Protein 1
Regulatory Networks
030306 microbiology
Interleukin-6
Gene Expression Profiling
Macrophages
MESH: Transcription, Genetic
lcsh:R
Immunity
Trophoblast
Computational Biology
Immune Defense
biology.organism_classification
medicine.disease
bacterial infections and mycoses
Virology
MESH: Interleukin-6
[SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology
Signaling Networks
MESH: Coxiella burnetii
Pregnancy Complications
MESH: Oligonucleotide Array Sequence Analysis
bacteria
lcsh:Q
[SDV.MP.BAC] Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology

Details

Language :
English
ISSN :
19326203
Database :
OpenAIRE
Journal :
PLoS ONE, PLoS ONE, 2010, 5 (12), pp.e15315. ⟨10.1371/journal.pone.0015315⟩, PLoS ONE, Public Library of Science, 2010, 5 (12), pp.e15315. ⟨10.1371/journal.pone.0015315⟩, PLoS ONE, Vol 5, Iss 12, p e15315 (2010)
Accession number :
edsair.doi.dedup.....caa1e8d8b84e6aa8752a2dd81f953424