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Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages

Although filamentous morphology in bacteria has been associated with resistance to phagocytosis, our understanding of the cellular mechanisms behind this process is limited. To investigate this, we followed the phagocytosis of both viable and dead Legionella pneumophila filaments. The engulfment of...

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Autores principales: Prashar, Akriti, Bhatia, Sonam, Gigliozzi, Darren, Martin, Tonya, Duncan, Carla, Guyard, Cyril, Terebiznik, Mauricio R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Rockefeller University Press 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3871431/
https://www.ncbi.nlm.nih.gov/pubmed/24368810
http://dx.doi.org/10.1083/jcb.201304095
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author Prashar, Akriti
Bhatia, Sonam
Gigliozzi, Darren
Martin, Tonya
Duncan, Carla
Guyard, Cyril
Terebiznik, Mauricio R.
author_facet Prashar, Akriti
Bhatia, Sonam
Gigliozzi, Darren
Martin, Tonya
Duncan, Carla
Guyard, Cyril
Terebiznik, Mauricio R.
author_sort Prashar, Akriti
collection PubMed
description Although filamentous morphology in bacteria has been associated with resistance to phagocytosis, our understanding of the cellular mechanisms behind this process is limited. To investigate this, we followed the phagocytosis of both viable and dead Legionella pneumophila filaments. The engulfment of these targets occurred gradually and along the longitudinal axis of the filament, therefore defining a long-lasting phagocytic cup stage that determined the outcome of phagocytosis. We found that these phagocytic cups fused with endosomes and lysosomes, events linked to the maturation of phagosomes according to the canonical pathway, and not with the remodeling of phagocytic cups. Nevertheless, despite acquiring phagolysosomal features these phagocytic cups failed to develop hydrolytic capacity before their sealing. This phenomenon hampered the microbicidal activity of the macrophage and enhanced the capacity of viable filamentous L. pneumophila to escape phagosomal killing in a length-dependent manner. Our results demonstrate that key aspects in phagocytic cup remodeling and phagosomal maturation could be influenced by target morphology.
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spelling pubmed-38714312014-06-23 Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages Prashar, Akriti Bhatia, Sonam Gigliozzi, Darren Martin, Tonya Duncan, Carla Guyard, Cyril Terebiznik, Mauricio R. J Cell Biol Research Articles Although filamentous morphology in bacteria has been associated with resistance to phagocytosis, our understanding of the cellular mechanisms behind this process is limited. To investigate this, we followed the phagocytosis of both viable and dead Legionella pneumophila filaments. The engulfment of these targets occurred gradually and along the longitudinal axis of the filament, therefore defining a long-lasting phagocytic cup stage that determined the outcome of phagocytosis. We found that these phagocytic cups fused with endosomes and lysosomes, events linked to the maturation of phagosomes according to the canonical pathway, and not with the remodeling of phagocytic cups. Nevertheless, despite acquiring phagolysosomal features these phagocytic cups failed to develop hydrolytic capacity before their sealing. This phenomenon hampered the microbicidal activity of the macrophage and enhanced the capacity of viable filamentous L. pneumophila to escape phagosomal killing in a length-dependent manner. Our results demonstrate that key aspects in phagocytic cup remodeling and phagosomal maturation could be influenced by target morphology. The Rockefeller University Press 2013-12-23 /pmc/articles/PMC3871431/ /pubmed/24368810 http://dx.doi.org/10.1083/jcb.201304095 Text en © 2013 Prashar et al. This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 3.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/3.0/).
spellingShingle Research Articles
Prashar, Akriti
Bhatia, Sonam
Gigliozzi, Darren
Martin, Tonya
Duncan, Carla
Guyard, Cyril
Terebiznik, Mauricio R.
Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
title Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
title_full Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
title_fullStr Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
title_full_unstemmed Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
title_short Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
title_sort filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3871431/
https://www.ncbi.nlm.nih.gov/pubmed/24368810
http://dx.doi.org/10.1083/jcb.201304095
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