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Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments

During the intracellular life of Salmonella enterica, a unique membrane-bound compartment termed Salmonella-containing vacuole, or SCV, is formed. By means of translocated effector proteins, intracellular Salmonella also induce the formation of extensive, highly dynamic membrane tubules termed Salmo...

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Autores principales: Krieger, Viktoria, Liebl, David, Zhang, Yuying, Rajashekar, Roopa, Chlanda, Petr, Giesker, Katrin, Chikkaballi, Deepak, Hensel, Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4177991/
https://www.ncbi.nlm.nih.gov/pubmed/25254663
http://dx.doi.org/10.1371/journal.ppat.1004374
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author Krieger, Viktoria
Liebl, David
Zhang, Yuying
Rajashekar, Roopa
Chlanda, Petr
Giesker, Katrin
Chikkaballi, Deepak
Hensel, Michael
author_facet Krieger, Viktoria
Liebl, David
Zhang, Yuying
Rajashekar, Roopa
Chlanda, Petr
Giesker, Katrin
Chikkaballi, Deepak
Hensel, Michael
author_sort Krieger, Viktoria
collection PubMed
description During the intracellular life of Salmonella enterica, a unique membrane-bound compartment termed Salmonella-containing vacuole, or SCV, is formed. By means of translocated effector proteins, intracellular Salmonella also induce the formation of extensive, highly dynamic membrane tubules termed Salmonella-induced filaments or SIF. Here we report the first detailed ultrastructural analyses of the SCV and SIF by electron microscopy (EM), EM tomography and live cell correlative light and electron microscopy (CLEM). We found that a subset of SIF is composed of double membranes that enclose portions of host cell cytosol and cytoskeletal filaments within its inner lumen. Despite some morphological similarities, we found that the formation of SIF double membranes is independent from autophagy and requires the function of the effector proteins SseF and SseG. The lumen of SIF network is accessible to various types of endocytosed material and our CLEM analysis of double membrane SIF demonstrated that fluid phase markers accumulate only between the inner and outer membrane of these structures, a space continual with endosomal lumen. Our work reveals how manipulation of the endosomal membrane system by an intracellular pathogen results in a unique tubular membrane compartmentalization of the host cell, generating a shielded niche permissive for intracellular proliferation of Salmonella.
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spelling pubmed-41779912014-10-02 Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments Krieger, Viktoria Liebl, David Zhang, Yuying Rajashekar, Roopa Chlanda, Petr Giesker, Katrin Chikkaballi, Deepak Hensel, Michael PLoS Pathog Research Article During the intracellular life of Salmonella enterica, a unique membrane-bound compartment termed Salmonella-containing vacuole, or SCV, is formed. By means of translocated effector proteins, intracellular Salmonella also induce the formation of extensive, highly dynamic membrane tubules termed Salmonella-induced filaments or SIF. Here we report the first detailed ultrastructural analyses of the SCV and SIF by electron microscopy (EM), EM tomography and live cell correlative light and electron microscopy (CLEM). We found that a subset of SIF is composed of double membranes that enclose portions of host cell cytosol and cytoskeletal filaments within its inner lumen. Despite some morphological similarities, we found that the formation of SIF double membranes is independent from autophagy and requires the function of the effector proteins SseF and SseG. The lumen of SIF network is accessible to various types of endocytosed material and our CLEM analysis of double membrane SIF demonstrated that fluid phase markers accumulate only between the inner and outer membrane of these structures, a space continual with endosomal lumen. Our work reveals how manipulation of the endosomal membrane system by an intracellular pathogen results in a unique tubular membrane compartmentalization of the host cell, generating a shielded niche permissive for intracellular proliferation of Salmonella. Public Library of Science 2014-09-25 /pmc/articles/PMC4177991/ /pubmed/25254663 http://dx.doi.org/10.1371/journal.ppat.1004374 Text en © 2014 Krieger et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Krieger, Viktoria
Liebl, David
Zhang, Yuying
Rajashekar, Roopa
Chlanda, Petr
Giesker, Katrin
Chikkaballi, Deepak
Hensel, Michael
Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments
title Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments
title_full Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments
title_fullStr Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments
title_full_unstemmed Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments
title_short Reorganization of the Endosomal System in Salmonella-Infected Cells: The Ultrastructure of Salmonella-Induced Tubular Compartments
title_sort reorganization of the endosomal system in salmonella-infected cells: the ultrastructure of salmonella-induced tubular compartments
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4177991/
https://www.ncbi.nlm.nih.gov/pubmed/25254663
http://dx.doi.org/10.1371/journal.ppat.1004374
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