Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice

Abstract Several species of the Gram-negative genus Bordetella are the cause of respiratory infections in mammals and birds, including whooping cough (pertussis) in humans. Very recently, a novel atypical species, Bordetella pseudohinzii, was isolated from laboratory mice. These mice presented no ob...

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Main Authors: Alexander Perniss, Nadine Schmidt, Corinne Gurtner, Kristina Dietert, Oliver Schwengers, Markus Weigel, Julia Hempe, Christa Ewers, Uwe Pfeil, Ulrich Gärtner, Achim D. Gruber, Torsten Hain, Wolfgang Kummer
Format: Article
Language:English
Published: Nature Publishing Group 2018-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-018-23830-4
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spelling doaj-a4e38a4616c9419092e411bc2705df3d2020-12-08T05:12:06ZengNature Publishing GroupScientific Reports2045-23222018-04-018111510.1038/s41598-018-23830-4Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in miceAlexander Perniss0Nadine Schmidt1Corinne Gurtner2Kristina Dietert3Oliver Schwengers4Markus Weigel5Julia Hempe6Christa Ewers7Uwe Pfeil8Ulrich Gärtner9Achim D. Gruber10Torsten Hain11Wolfgang Kummer12Institute of Anatomy and Cell Biology, German Center for Lung Research (DZL), Excellence Cluster Cardio-Pulmonary System (ECCPS), Justus-Liebig-University GiessenInstitute of Hygiene and Infectious Diseases of Animals, Justus-Liebig-University GiessenInstitute of Veterinary Pathology, Freie Universität BerlinInstitute of Veterinary Pathology, Freie Universität BerlinInstitute for Medical Microbiology, Justus-Liebig-University GiessenInstitute for Medical Microbiology, Justus-Liebig-University GiessenCentral Experimental Animal Facility, Justus-Liebig-University GiessenInstitute of Hygiene and Infectious Diseases of Animals, Justus-Liebig-University GiessenInstitute of Anatomy and Cell Biology, German Center for Lung Research (DZL), Excellence Cluster Cardio-Pulmonary System (ECCPS), Justus-Liebig-University GiessenInstitute of Anatomy and Cell Biology, German Center for Lung Research (DZL), Excellence Cluster Cardio-Pulmonary System (ECCPS), Justus-Liebig-University GiessenInstitute of Veterinary Pathology, Freie Universität BerlinInstitute for Medical Microbiology, Justus-Liebig-University GiessenInstitute of Anatomy and Cell Biology, German Center for Lung Research (DZL), Excellence Cluster Cardio-Pulmonary System (ECCPS), Justus-Liebig-University GiessenAbstract Several species of the Gram-negative genus Bordetella are the cause of respiratory infections in mammals and birds, including whooping cough (pertussis) in humans. Very recently, a novel atypical species, Bordetella pseudohinzii, was isolated from laboratory mice. These mice presented no obvious clinical symptoms but elevated numbers of neutrophils in bronchoalveolar lavage fluid and inflammatory signs in histopathology. We noted that this species can occur at high prevalence in a mouse facility despite regular pathogen testing according to the FELASA-recommendations. Affected C57BL/6 J mice had, in addition to the reported pulmonary alterations, tracheal inflammation with reduced numbers of ciliated cells, slower ciliary beat frequency, and largely (>50%) compromised cilia-driven particle transport speed on the mucosal surface, a primary innate defence mechanism. In an in vitro-model, Bordetella pseudohinzii attached to respiratory kinocilia, impaired ciliary function within 4 h and caused epithelial damage within 24 h. Regular testing for this ciliotropic Bordetella species and excluding it from colonies that provide mice for lung research shall be recommended. On the other hand, controlled colonization and infection with Bordetella pseudohinzii may serve as an experimental model to investigate mechanisms of mucociliary clearance and microbial strategies to escape from this primary innate defence response.https://doi.org/10.1038/s41598-018-23830-4
collection DOAJ
language English
format Article
sources DOAJ
author Alexander Perniss
Nadine Schmidt
Corinne Gurtner
Kristina Dietert
Oliver Schwengers
Markus Weigel
Julia Hempe
Christa Ewers
Uwe Pfeil
Ulrich Gärtner
Achim D. Gruber
Torsten Hain
Wolfgang Kummer
spellingShingle Alexander Perniss
Nadine Schmidt
Corinne Gurtner
Kristina Dietert
Oliver Schwengers
Markus Weigel
Julia Hempe
Christa Ewers
Uwe Pfeil
Ulrich Gärtner
Achim D. Gruber
Torsten Hain
Wolfgang Kummer
Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
Scientific Reports
author_facet Alexander Perniss
Nadine Schmidt
Corinne Gurtner
Kristina Dietert
Oliver Schwengers
Markus Weigel
Julia Hempe
Christa Ewers
Uwe Pfeil
Ulrich Gärtner
Achim D. Gruber
Torsten Hain
Wolfgang Kummer
author_sort Alexander Perniss
title Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
title_short Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
title_full Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
title_fullStr Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
title_full_unstemmed Bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
title_sort bordetella pseudohinzii targets cilia and impairs tracheal cilia-driven transport in naturally acquired infection in mice
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2018-04-01
description Abstract Several species of the Gram-negative genus Bordetella are the cause of respiratory infections in mammals and birds, including whooping cough (pertussis) in humans. Very recently, a novel atypical species, Bordetella pseudohinzii, was isolated from laboratory mice. These mice presented no obvious clinical symptoms but elevated numbers of neutrophils in bronchoalveolar lavage fluid and inflammatory signs in histopathology. We noted that this species can occur at high prevalence in a mouse facility despite regular pathogen testing according to the FELASA-recommendations. Affected C57BL/6 J mice had, in addition to the reported pulmonary alterations, tracheal inflammation with reduced numbers of ciliated cells, slower ciliary beat frequency, and largely (>50%) compromised cilia-driven particle transport speed on the mucosal surface, a primary innate defence mechanism. In an in vitro-model, Bordetella pseudohinzii attached to respiratory kinocilia, impaired ciliary function within 4 h and caused epithelial damage within 24 h. Regular testing for this ciliotropic Bordetella species and excluding it from colonies that provide mice for lung research shall be recommended. On the other hand, controlled colonization and infection with Bordetella pseudohinzii may serve as an experimental model to investigate mechanisms of mucociliary clearance and microbial strategies to escape from this primary innate defence response.
url https://doi.org/10.1038/s41598-018-23830-4
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