Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis

Several bacterial pathogens and viruses interfere with the cell cycle of their host cells to enhance virulence. This is especially apparent in bacteria that colonize the gut epithelium, where inhibition of the cell cycle of infected cells enhances the intestinal colonization. We found that intracell...

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Autores: Santos, António J. M., Durkin, Charlotte H., Helaine, Sophie, Boucrot, Emmanuel, Holden, David W.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2016
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/30905
Acceso en línea:http://hdl.handle.net/10230/30905
http://dx.doi.org/10.1128/IAI.00062-16
Access Level:acceso abierto
Palabra clave:Cellular Microbiology
Pathogen-Host Cell Molecular
Interactions
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spelling Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell CytokinesisSantos, António J. M.Durkin, Charlotte H.Helaine, SophieBoucrot, EmmanuelHolden, David W.Cellular MicrobiologyPathogen-Host Cell MolecularInteractionsSeveral bacterial pathogens and viruses interfere with the cell cycle of their host cells to enhance virulence. This is especially apparent in bacteria that colonize the gut epithelium, where inhibition of the cell cycle of infected cells enhances the intestinal colonization. We found that intracellular Salmonella enterica serovar Typhimurium induced the binucleation of a large proportion of epithelial cells by 14 h postinvasion and that the effect was dependent on an intact Salmonella pathogenicity island 2 (SPI-2) type 3 secretion system. The SPI-2 effectors SseF and SseG were required to induce binucleation. SseF and SseG are known to maintain microcolonies of Salmonella-containing vacuoles close to the microtubule organizing center of infected epithelial cells. During host cell division, these clustered microcolonies prevented the correct localization of members of the chromosomal passenger complex and mitotic kinesin-like protein 1 and consequently prevented cytokinesis. Tetraploidy, arising from a cytokinesis defect, is known to have a deleterious effect on subsequent cell divisions, resulting in either chromosomal instabilities or cell cycle arrest. In infected mice, proliferation of small intestinal epithelial cells was compromised in an SseF/SseG-dependent manner, suggesting that cytokinesis failure caused by S. Typhimurium delays epithelial cell turnover in the intestine.This work was funded by the Wellcome Trust, Medical Research Council (MRC), the Biotechnology and Biological Sciences Research Council (BBSRC), and the Ministry of Education and Science | Fundação para a Ciência e a Tecnologia (FCT) (SFRH/BD/33545/2008).American Society for Microbiology201720172016info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/30905http://dx.doi.org/10.1128/IAI.00062-16reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésInfection and Immunity. 2016; 84(7): 2149-2158© American Society for Microbiology. Copyright © 2016 Santos et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/309052026-06-12T07:21:37Z
dc.title.none.fl_str_mv Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
title Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
spellingShingle Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
Santos, António J. M.
Cellular Microbiology
Pathogen-Host Cell Molecular
Interactions
title_short Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
title_full Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
title_fullStr Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
title_full_unstemmed Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
title_sort Clustered Intracellular Salmonella enterica Serovar Typhimurium Blocks Host Cell Cytokinesis
dc.creator.none.fl_str_mv Santos, António J. M.
Durkin, Charlotte H.
Helaine, Sophie
Boucrot, Emmanuel
Holden, David W.
author Santos, António J. M.
author_facet Santos, António J. M.
Durkin, Charlotte H.
Helaine, Sophie
Boucrot, Emmanuel
Holden, David W.
author_role author
author2 Durkin, Charlotte H.
Helaine, Sophie
Boucrot, Emmanuel
Holden, David W.
author2_role author
author
author
author
dc.subject.none.fl_str_mv Cellular Microbiology
Pathogen-Host Cell Molecular
Interactions
topic Cellular Microbiology
Pathogen-Host Cell Molecular
Interactions
description Several bacterial pathogens and viruses interfere with the cell cycle of their host cells to enhance virulence. This is especially apparent in bacteria that colonize the gut epithelium, where inhibition of the cell cycle of infected cells enhances the intestinal colonization. We found that intracellular Salmonella enterica serovar Typhimurium induced the binucleation of a large proportion of epithelial cells by 14 h postinvasion and that the effect was dependent on an intact Salmonella pathogenicity island 2 (SPI-2) type 3 secretion system. The SPI-2 effectors SseF and SseG were required to induce binucleation. SseF and SseG are known to maintain microcolonies of Salmonella-containing vacuoles close to the microtubule organizing center of infected epithelial cells. During host cell division, these clustered microcolonies prevented the correct localization of members of the chromosomal passenger complex and mitotic kinesin-like protein 1 and consequently prevented cytokinesis. Tetraploidy, arising from a cytokinesis defect, is known to have a deleterious effect on subsequent cell divisions, resulting in either chromosomal instabilities or cell cycle arrest. In infected mice, proliferation of small intestinal epithelial cells was compromised in an SseF/SseG-dependent manner, suggesting that cytokinesis failure caused by S. Typhimurium delays epithelial cell turnover in the intestine.
publishDate 2016
dc.date.none.fl_str_mv 2016
2017
2017
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/30905
http://dx.doi.org/10.1128/IAI.00062-16
url http://hdl.handle.net/10230/30905
http://dx.doi.org/10.1128/IAI.00062-16
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Infection and Immunity. 2016; 84(7): 2149-2158
dc.rights.none.fl_str_mv https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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