Pneumococcal Extracellular Vesicles Modulate Host Immunity

ABSTRACT Extracellular vesicles (EVs) have recently garnered attention for their participation in host-microbe interactions in pneumococcal infections. However, the effect of EVs on the host immune system remain poorly understood. Our studies focus on EVs produced by Streptococcus pneumoniae (pEVs),...

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Autores principales:	Saigopalakrishna S. Yerneni, Sarah Werner, Juliana H. Azambuja, Nils Ludwig, Rory Eutsey, Surya D. Aggarwal, Peter C. Lucas, Nathanael Bailey, Theresa L. Whiteside, Phil G. Campbell, N. Luisa Hiller
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Gram-positive bacteria Streptococcus pneumoniae extracellular vesicles EVs macrophage signaling alternative activation pathway Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/daf0bbbac4384c3cb6fb8c58d8262fcc
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spelling	oai:doaj.org-article:daf0bbbac4384c3cb6fb8c58d8262fcc2021-11-10T18:37:52ZPneumococcal Extracellular Vesicles Modulate Host Immunity10.1128/mBio.01657-212150-7511https://doaj.org/article/daf0bbbac4384c3cb6fb8c58d8262fcc2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01657-21https://doaj.org/toc/2150-7511ABSTRACT Extracellular vesicles (EVs) have recently garnered attention for their participation in host-microbe interactions in pneumococcal infections. However, the effect of EVs on the host immune system remain poorly understood. Our studies focus on EVs produced by Streptococcus pneumoniae (pEVs), and reveal that pEVs are internalized by macrophages, T cells, and epithelial cells. In vitro, pEVs induce NF-κB activation in a dosage-dependent manner and polarize human macrophages to an alternative (M2) phenotype. In addition, pEV pretreatment conditions macrophages to increase bacteria uptake and such macrophages may act as a reservoir for pneumococcal cells by increasing survival of the phagocytosed bacteria. When administered systemically in mice, pEVs induce cytokine release; when immobilized locally, they recruit lymphocytes and macrophages. Taken together, pEVs emerge as critical contributors to inflammatory responses and tissue damage in mammalian hosts. IMPORTANCE Over the last decade, pathogen-derived extracellular vesicles (EVs) have emerged as important players in several human diseases. Therefore, a thorough understanding of EV-mediated mechanisms could provide novel insights into vaccine/therapeutic development. A critical question in the field is: do pathogen-derived EVs help the pathogen evade the harsh environment in the host or do they help the host to mount a robust immune response against the pathogen? This study is a step towards answering this critical question for the Gram-positive pathogen, Streptococcus pneumoniae. Our study shows that while S. pneumoniae EVs (pEVs) induce inflammatory response both in vitro and in vivo, they may also condition the host macrophages to serve as a reservoir for the bacteria.Saigopalakrishna S. YerneniSarah WernerJuliana H. AzambujaNils LudwigRory EutseySurya D. AggarwalPeter C. LucasNathanael BaileyTheresa L. WhitesidePhil G. CampbellN. Luisa HillerAmerican Society for MicrobiologyarticleGram-positive bacteriaStreptococcus pneumoniaeextracellular vesiclesEVsmacrophage signalingalternative activation pathwayMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Gram-positive bacteria Streptococcus pneumoniae extracellular vesicles EVs macrophage signaling alternative activation pathway Microbiology QR1-502
spellingShingle	Gram-positive bacteria Streptococcus pneumoniae extracellular vesicles EVs macrophage signaling alternative activation pathway Microbiology QR1-502 Saigopalakrishna S. Yerneni Sarah Werner Juliana H. Azambuja Nils Ludwig Rory Eutsey Surya D. Aggarwal Peter C. Lucas Nathanael Bailey Theresa L. Whiteside Phil G. Campbell N. Luisa Hiller Pneumococcal Extracellular Vesicles Modulate Host Immunity
description	ABSTRACT Extracellular vesicles (EVs) have recently garnered attention for their participation in host-microbe interactions in pneumococcal infections. However, the effect of EVs on the host immune system remain poorly understood. Our studies focus on EVs produced by Streptococcus pneumoniae (pEVs), and reveal that pEVs are internalized by macrophages, T cells, and epithelial cells. In vitro, pEVs induce NF-κB activation in a dosage-dependent manner and polarize human macrophages to an alternative (M2) phenotype. In addition, pEV pretreatment conditions macrophages to increase bacteria uptake and such macrophages may act as a reservoir for pneumococcal cells by increasing survival of the phagocytosed bacteria. When administered systemically in mice, pEVs induce cytokine release; when immobilized locally, they recruit lymphocytes and macrophages. Taken together, pEVs emerge as critical contributors to inflammatory responses and tissue damage in mammalian hosts. IMPORTANCE Over the last decade, pathogen-derived extracellular vesicles (EVs) have emerged as important players in several human diseases. Therefore, a thorough understanding of EV-mediated mechanisms could provide novel insights into vaccine/therapeutic development. A critical question in the field is: do pathogen-derived EVs help the pathogen evade the harsh environment in the host or do they help the host to mount a robust immune response against the pathogen? This study is a step towards answering this critical question for the Gram-positive pathogen, Streptococcus pneumoniae. Our study shows that while S. pneumoniae EVs (pEVs) induce inflammatory response both in vitro and in vivo, they may also condition the host macrophages to serve as a reservoir for the bacteria.
format	article
author	Saigopalakrishna S. Yerneni Sarah Werner Juliana H. Azambuja Nils Ludwig Rory Eutsey Surya D. Aggarwal Peter C. Lucas Nathanael Bailey Theresa L. Whiteside Phil G. Campbell N. Luisa Hiller
author_facet	Saigopalakrishna S. Yerneni Sarah Werner Juliana H. Azambuja Nils Ludwig Rory Eutsey Surya D. Aggarwal Peter C. Lucas Nathanael Bailey Theresa L. Whiteside Phil G. Campbell N. Luisa Hiller
author_sort	Saigopalakrishna S. Yerneni
title	Pneumococcal Extracellular Vesicles Modulate Host Immunity
title_short	Pneumococcal Extracellular Vesicles Modulate Host Immunity
title_full	Pneumococcal Extracellular Vesicles Modulate Host Immunity
title_fullStr	Pneumococcal Extracellular Vesicles Modulate Host Immunity
title_full_unstemmed	Pneumococcal Extracellular Vesicles Modulate Host Immunity
title_sort	pneumococcal extracellular vesicles modulate host immunity
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/daf0bbbac4384c3cb6fb8c58d8262fcc
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Pneumococcal Extracellular Vesicles Modulate Host Immunity

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