Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion

ABSTRACT Chlamydia trachomatis is an obligate intracellular human pathogen that grows inside a membranous, cytosolic vacuole termed an inclusion. Septins are a group of 13 GTP-binding proteins that assemble into oligomeric complexes and that can form higher-order filaments. We report here that the s...

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Autores principales:	Larisa Volceanov, Katharina Herbst, Martin Biniossek, Oliver Schilling, Dirk Haller, Thilo Nölke, Prema Subbarayal, Thomas Rudel, Barbara Zieger, Georg Häcker
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d99137ab4e224273abb8cd7fc0fa9005
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spelling	oai:doaj.org-article:d99137ab4e224273abb8cd7fc0fa90052021-11-15T15:45:54ZSeptins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion10.1128/mBio.01802-142150-7511https://doaj.org/article/d99137ab4e224273abb8cd7fc0fa90052014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01802-14https://doaj.org/toc/2150-7511ABSTRACT Chlamydia trachomatis is an obligate intracellular human pathogen that grows inside a membranous, cytosolic vacuole termed an inclusion. Septins are a group of 13 GTP-binding proteins that assemble into oligomeric complexes and that can form higher-order filaments. We report here that the septins SEPT2, -9, -11, and probably -7 form fibrillar structures around the chlamydial inclusion. Colocalization studies suggest that these septins combine with F actin into fibers that encase the inclusion. Targeting the expression of individual septins by RNA interference (RNAi) prevented the formation of septin fibers as well as the recruitment of actin to the inclusion. At the end of the developmental cycle of C. trachomatis, newly formed, infectious elementary bodies are released, and this release occurs at least in part through the organized extrusion of intact inclusions. RNAi against SEPT9 or against the combination of SEPT2/7/9 substantially reduced the number of extrusions from a culture of infected HeLa cells. The data suggest that a higher-order structure of four septins is involved in the recruitment or stabilization of the actin coat around the chlamydial inclusion and that this actin recruitment by septins is instrumental for the coordinated egress of C. trachomatis from human cells. The organization of F actin around parasite-containing vacuoles may be a broader response mechanism of mammalian cells to the infection by intracellular, vacuole-dwelling pathogens. IMPORTANCE Chlamydia trachomatis is a frequent bacterial pathogen throughout the world, causing mostly eye and genital infections. C. trachomatis can develop only inside host cells; it multiplies inside a membranous vacuole in the cytosol, termed an inclusion. The inclusion is covered by cytoskeletal “coats” or “cages,” whose organization and function are poorly understood. We here report that a relatively little-characterized group of proteins, septins, is required to organize actin fibers on the inclusion and probably through actin the release of the inclusion. Septins are a group of GTP-binding proteins that can organize into heteromeric complexes and then into large filaments. Septins have previously been found to be involved in the interaction of the cell with bacteria in the cytosol. Our observation that they also organize a reaction to bacteria living in vacuoles suggests that they have a function in the recognition of foreign compartments by a parasitized human cell.Larisa VolceanovKatharina HerbstMartin BiniossekOliver SchillingDirk HallerThilo NölkePrema SubbarayalThomas RudelBarbara ZiegerGeorg HäckerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Larisa Volceanov Katharina Herbst Martin Biniossek Oliver Schilling Dirk Haller Thilo Nölke Prema Subbarayal Thomas Rudel Barbara Zieger Georg Häcker Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion
description	ABSTRACT Chlamydia trachomatis is an obligate intracellular human pathogen that grows inside a membranous, cytosolic vacuole termed an inclusion. Septins are a group of 13 GTP-binding proteins that assemble into oligomeric complexes and that can form higher-order filaments. We report here that the septins SEPT2, -9, -11, and probably -7 form fibrillar structures around the chlamydial inclusion. Colocalization studies suggest that these septins combine with F actin into fibers that encase the inclusion. Targeting the expression of individual septins by RNA interference (RNAi) prevented the formation of septin fibers as well as the recruitment of actin to the inclusion. At the end of the developmental cycle of C. trachomatis, newly formed, infectious elementary bodies are released, and this release occurs at least in part through the organized extrusion of intact inclusions. RNAi against SEPT9 or against the combination of SEPT2/7/9 substantially reduced the number of extrusions from a culture of infected HeLa cells. The data suggest that a higher-order structure of four septins is involved in the recruitment or stabilization of the actin coat around the chlamydial inclusion and that this actin recruitment by septins is instrumental for the coordinated egress of C. trachomatis from human cells. The organization of F actin around parasite-containing vacuoles may be a broader response mechanism of mammalian cells to the infection by intracellular, vacuole-dwelling pathogens. IMPORTANCE Chlamydia trachomatis is a frequent bacterial pathogen throughout the world, causing mostly eye and genital infections. C. trachomatis can develop only inside host cells; it multiplies inside a membranous vacuole in the cytosol, termed an inclusion. The inclusion is covered by cytoskeletal “coats” or “cages,” whose organization and function are poorly understood. We here report that a relatively little-characterized group of proteins, septins, is required to organize actin fibers on the inclusion and probably through actin the release of the inclusion. Septins are a group of GTP-binding proteins that can organize into heteromeric complexes and then into large filaments. Septins have previously been found to be involved in the interaction of the cell with bacteria in the cytosol. Our observation that they also organize a reaction to bacteria living in vacuoles suggests that they have a function in the recognition of foreign compartments by a parasitized human cell.
format	article
author	Larisa Volceanov Katharina Herbst Martin Biniossek Oliver Schilling Dirk Haller Thilo Nölke Prema Subbarayal Thomas Rudel Barbara Zieger Georg Häcker
author_facet	Larisa Volceanov Katharina Herbst Martin Biniossek Oliver Schilling Dirk Haller Thilo Nölke Prema Subbarayal Thomas Rudel Barbara Zieger Georg Häcker
author_sort	Larisa Volceanov
title	Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion
title_short	Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion
title_full	Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion
title_fullStr	Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion
title_full_unstemmed	Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion
title_sort	septins arrange f-actin-containing fibers on the <named-content content-type="genus-species">chlamydia trachomatis</named-content> inclusion and are required for normal release of the inclusion by extrusion
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/d99137ab4e224273abb8cd7fc0fa9005
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Septins Arrange F-Actin-Containing Fibers on the <named-content content-type="genus-species">Chlamydia trachomatis</named-content> Inclusion and Are Required for Normal Release of the Inclusion by Extrusion

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