Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.

The Gram negative bacterium Vibrio cholerae is the causative agent of the secretory diarrheal disease cholera, which has traditionally been classified as a noninflammatory disease. However, several recent reports suggest that a V. cholerae infection induces an inflammatory response in the gastrointe...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Andrea Seper, Ava Hosseinzadeh, Gregor Gorkiewicz, Sabine Lichtenegger, Sandro Roier, Deborah R Leitner, Marc Röhm, Andreas Grutsch, Joachim Reidl, Constantin F Urban, Stefan Schild
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/953e54e00cba46ac81a0e83b8f35756e
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:953e54e00cba46ac81a0e83b8f35756e
record_format	dspace
spelling	oai:doaj.org-article:953e54e00cba46ac81a0e83b8f35756e2021-11-18T06:07:40ZVibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.1553-73661553-737410.1371/journal.ppat.1003614https://doaj.org/article/953e54e00cba46ac81a0e83b8f35756e2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24039581/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374The Gram negative bacterium Vibrio cholerae is the causative agent of the secretory diarrheal disease cholera, which has traditionally been classified as a noninflammatory disease. However, several recent reports suggest that a V. cholerae infection induces an inflammatory response in the gastrointestinal tract indicated by recruitment of innate immune cells and increase of inflammatory cytokines. In this study, we describe a colonization defect of a double extracellular nuclease V. cholerae mutant in immunocompetent mice, which is not evident in neutropenic mice. Intrigued by this observation, we investigated the impact of neutrophils, as a central part of the innate immune system, on the pathogen V. cholerae in more detail. Our results demonstrate that V. cholerae induces formation of neutrophil extracellular traps (NETs) upon contact with neutrophils, while V. cholerae in return induces the two extracellular nucleases upon presence of NETs. We show that the V. cholerae wild type rapidly degrades the DNA component of the NETs by the combined activity of the two extracellular nucleases Dns and Xds. In contrast, NETs exhibit prolonged stability in presence of the double nuclease mutant. Finally, we demonstrate that Dns and Xds mediate evasion of V. cholerae from NETs and lower the susceptibility for extracellular killing in the presence of NETs. This report provides a first comprehensive characterization of the interplay between neutrophils and V. cholerae along with new evidence that the innate immune response impacts the colonization of V. cholerae in vivo. A limitation of this study is an inability for technical and physiological reasons to visualize intact NETs in the intestinal lumen of infected mice, but we can hypothesize that extracellular nuclease production by V. cholerae may enhance survival fitness of the pathogen through NET degradation.Andrea SeperAva HosseinzadehGregor GorkiewiczSabine LichteneggerSandro RoierDeborah R LeitnerMarc RöhmAndreas GrutschJoachim ReidlConstantin F UrbanStefan SchildPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 9, p e1003614 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Andrea Seper Ava Hosseinzadeh Gregor Gorkiewicz Sabine Lichtenegger Sandro Roier Deborah R Leitner Marc Röhm Andreas Grutsch Joachim Reidl Constantin F Urban Stefan Schild Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
description	The Gram negative bacterium Vibrio cholerae is the causative agent of the secretory diarrheal disease cholera, which has traditionally been classified as a noninflammatory disease. However, several recent reports suggest that a V. cholerae infection induces an inflammatory response in the gastrointestinal tract indicated by recruitment of innate immune cells and increase of inflammatory cytokines. In this study, we describe a colonization defect of a double extracellular nuclease V. cholerae mutant in immunocompetent mice, which is not evident in neutropenic mice. Intrigued by this observation, we investigated the impact of neutrophils, as a central part of the innate immune system, on the pathogen V. cholerae in more detail. Our results demonstrate that V. cholerae induces formation of neutrophil extracellular traps (NETs) upon contact with neutrophils, while V. cholerae in return induces the two extracellular nucleases upon presence of NETs. We show that the V. cholerae wild type rapidly degrades the DNA component of the NETs by the combined activity of the two extracellular nucleases Dns and Xds. In contrast, NETs exhibit prolonged stability in presence of the double nuclease mutant. Finally, we demonstrate that Dns and Xds mediate evasion of V. cholerae from NETs and lower the susceptibility for extracellular killing in the presence of NETs. This report provides a first comprehensive characterization of the interplay between neutrophils and V. cholerae along with new evidence that the innate immune response impacts the colonization of V. cholerae in vivo. A limitation of this study is an inability for technical and physiological reasons to visualize intact NETs in the intestinal lumen of infected mice, but we can hypothesize that extracellular nuclease production by V. cholerae may enhance survival fitness of the pathogen through NET degradation.
format	article
author	Andrea Seper Ava Hosseinzadeh Gregor Gorkiewicz Sabine Lichtenegger Sandro Roier Deborah R Leitner Marc Röhm Andreas Grutsch Joachim Reidl Constantin F Urban Stefan Schild
author_facet	Andrea Seper Ava Hosseinzadeh Gregor Gorkiewicz Sabine Lichtenegger Sandro Roier Deborah R Leitner Marc Röhm Andreas Grutsch Joachim Reidl Constantin F Urban Stefan Schild
author_sort	Andrea Seper
title	Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
title_short	Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
title_full	Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
title_fullStr	Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
title_full_unstemmed	Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
title_sort	vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/953e54e00cba46ac81a0e83b8f35756e
work_keys_str_mv	AT andreaseper vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT avahosseinzadeh vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT gregorgorkiewicz vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT sabinelichtenegger vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT sandroroier vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT deborahrleitner vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT marcrohm vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT andreasgrutsch vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT joachimreidl vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT constantinfurban vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases AT stefanschild vibriocholeraeevadesneutrophilextracellulartrapsbytheactivityoftwoextracellularnucleases
_version_	1718424554188046336

Vibrio cholerae evades neutrophil extracellular traps by the activity of two extracellular nucleases.

Ejemplares similares