<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading

ABSTRACT Listeria monocytogenes moves from one cell to another using actin-rich membrane protrusions that propel the bacterium toward neighboring cells. Despite cholesterol being required for this transfer process, the precise host internalization mechanism remains elusive. Here, we show that caveol...

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Autores principales:	Aaron S. Dhanda, Connie Yu, Katarina T. Lulic, A. Wayne Vogl, Valentina Rausch, Diana Yang, Benjamin J. Nichols, Sung Hyun Kim, Simona Polo, Carsten G. Hansen, Julian A. Guttman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	endocytosis epsin-1 membrane protrusion invaginations actin Listeria monocytogenes Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f192d030cbcf439984a879535aeec796
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spelling	oai:doaj.org-article:f192d030cbcf439984a879535aeec7962021-11-15T15:56:57Z<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading10.1128/mBio.02857-192150-7511https://doaj.org/article/f192d030cbcf439984a879535aeec7962020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02857-19https://doaj.org/toc/2150-7511ABSTRACT Listeria monocytogenes moves from one cell to another using actin-rich membrane protrusions that propel the bacterium toward neighboring cells. Despite cholesterol being required for this transfer process, the precise host internalization mechanism remains elusive. Here, we show that caveolin endocytosis is key to this event as bacterial cell-to-cell transfer is severely impaired when cells are depleted of caveolin-1. Only a subset of additional caveolar components (cavin-2 and EHD2) are present at sites of bacterial transfer, and although clathrin and the clathrin-associated proteins Eps15 and AP2 are absent from the bacterial invaginations, efficient L. monocytogenes spreading requires the clathrin-interacting protein epsin-1. We also directly demonstrated that isolated L. monocytogenes membrane protrusions can trigger the recruitment of caveolar proteins in a neighboring cell. The engulfment of these bacterial and cytoskeletal structures through a caveolin-based mechanism demonstrates that the classical nanometer-scale theoretical size limit for this internalization pathway is exceeded by these bacterial pathogens. IMPORTANCE Listeria monocytogenes moves from one cell to another as it disseminates within tissues. This bacterial transfer process depends on the host actin cytoskeleton as the bacterium forms motile actin-rich membranous protrusions that propel the bacteria into neighboring cells, thus forming corresponding membrane invaginations. Here, we examine these membrane invaginations and demonstrate that caveolin-1–based endocytosis is crucial for efficient bacterial cell-to-cell spreading. We show that only a subset of caveolin-associated proteins (cavin-2 and EHD2) are involved in this process. Despite the absence of clathrin at the invaginations, the classical clathrin-associated protein epsin-1 is also required for efficient bacterial spreading. Using isolated L. monocytogenes protrusions added onto naive host cells, we demonstrate that actin-based propulsion is dispensable for caveolin-1 endocytosis as the presence of the protrusion/invagination interaction alone triggers caveolin-1 recruitment in the recipient cells. Finally, we provide a model of how this caveolin-1–based internalization event can exceed the theoretical size limit for this endocytic pathway.Aaron S. DhandaConnie YuKatarina T. LulicA. Wayne VoglValentina RauschDiana YangBenjamin J. NicholsSung Hyun KimSimona PoloCarsten G. HansenJulian A. GuttmanAmerican Society for Microbiologyarticleendocytosisepsin-1membrane protrusioninvaginationsactinListeria monocytogenesMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	endocytosis epsin-1 membrane protrusion invaginations actin Listeria monocytogenes Microbiology QR1-502
spellingShingle	endocytosis epsin-1 membrane protrusion invaginations actin Listeria monocytogenes Microbiology QR1-502 Aaron S. Dhanda Connie Yu Katarina T. Lulic A. Wayne Vogl Valentina Rausch Diana Yang Benjamin J. Nichols Sung Hyun Kim Simona Polo Carsten G. Hansen Julian A. Guttman <named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading
description	ABSTRACT Listeria monocytogenes moves from one cell to another using actin-rich membrane protrusions that propel the bacterium toward neighboring cells. Despite cholesterol being required for this transfer process, the precise host internalization mechanism remains elusive. Here, we show that caveolin endocytosis is key to this event as bacterial cell-to-cell transfer is severely impaired when cells are depleted of caveolin-1. Only a subset of additional caveolar components (cavin-2 and EHD2) are present at sites of bacterial transfer, and although clathrin and the clathrin-associated proteins Eps15 and AP2 are absent from the bacterial invaginations, efficient L. monocytogenes spreading requires the clathrin-interacting protein epsin-1. We also directly demonstrated that isolated L. monocytogenes membrane protrusions can trigger the recruitment of caveolar proteins in a neighboring cell. The engulfment of these bacterial and cytoskeletal structures through a caveolin-based mechanism demonstrates that the classical nanometer-scale theoretical size limit for this internalization pathway is exceeded by these bacterial pathogens. IMPORTANCE Listeria monocytogenes moves from one cell to another as it disseminates within tissues. This bacterial transfer process depends on the host actin cytoskeleton as the bacterium forms motile actin-rich membranous protrusions that propel the bacteria into neighboring cells, thus forming corresponding membrane invaginations. Here, we examine these membrane invaginations and demonstrate that caveolin-1–based endocytosis is crucial for efficient bacterial cell-to-cell spreading. We show that only a subset of caveolin-associated proteins (cavin-2 and EHD2) are involved in this process. Despite the absence of clathrin at the invaginations, the classical clathrin-associated protein epsin-1 is also required for efficient bacterial spreading. Using isolated L. monocytogenes protrusions added onto naive host cells, we demonstrate that actin-based propulsion is dispensable for caveolin-1 endocytosis as the presence of the protrusion/invagination interaction alone triggers caveolin-1 recruitment in the recipient cells. Finally, we provide a model of how this caveolin-1–based internalization event can exceed the theoretical size limit for this endocytic pathway.
format	article
author	Aaron S. Dhanda Connie Yu Katarina T. Lulic A. Wayne Vogl Valentina Rausch Diana Yang Benjamin J. Nichols Sung Hyun Kim Simona Polo Carsten G. Hansen Julian A. Guttman
author_facet	Aaron S. Dhanda Connie Yu Katarina T. Lulic A. Wayne Vogl Valentina Rausch Diana Yang Benjamin J. Nichols Sung Hyun Kim Simona Polo Carsten G. Hansen Julian A. Guttman
author_sort	Aaron S. Dhanda
title	<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading
title_short	<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading
title_full	<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading
title_fullStr	<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading
title_full_unstemmed	<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading
title_sort	<named-content content-type="genus-species">listeria monocytogenes</named-content> exploits host caveolin for cell-to-cell spreading
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/f192d030cbcf439984a879535aeec796
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<named-content content-type="genus-species">Listeria monocytogenes</named-content> Exploits Host Caveolin for Cell-to-Cell Spreading

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