<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose

ABSTRACT Hemophagocytes are cells of the monocyte lineage that have engulfed erythrocytes and leukocytes. Hemophagocytes frequently accumulate in patients with severe acute bacterial infections, such as those caused by Salmonella enterica, Brucella abortus, and Mycobacterium tuberculosis. The relati...

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Autores principales:	M. Carolina Pilonieta, Sarah M. Moreland, Christopher N. English, Corrella S. Detweiler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8b2fcbb6a07f43c4ae98f4726e75a52a
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spelling	oai:doaj.org-article:8b2fcbb6a07f43c4ae98f4726e75a52a2021-11-15T15:47:03Z<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose10.1128/mBio.02211-142150-7511https://doaj.org/article/8b2fcbb6a07f43c4ae98f4726e75a52a2014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02211-14https://doaj.org/toc/2150-7511ABSTRACT Hemophagocytes are cells of the monocyte lineage that have engulfed erythrocytes and leukocytes. Hemophagocytes frequently accumulate in patients with severe acute bacterial infections, such as those caused by Salmonella enterica, Brucella abortus, and Mycobacterium tuberculosis. The relationship between hemophagocytosis and infection is not well understood. In the murine liver, S. enterica serovar Typhimurium resides within hemophagocytic macrophages containing leukocytes. Here we show that S. Typhimurium also resides within hemophagocytes containing erythrocytes. In cell culture, S. Typhimurium benefits from residence within hemophagocytes by accessing iron, but why macrophages hemophagocytose is unknown. We show that treatment of macrophages with a cocktail of the proinflammatory cytokine interferon gamma (IFN-γ) and lipopolysaccharide (LPS) stimulates engulfment of nonsenescent erythrocytes. Exposure of resting or IFN-γ-treated macrophages to live, but not to heat-killed, S. Typhimurium cells also stimulates erythrocyte engulfment. Single-cell analyses show that S. Typhimurium-infected macrophages are more likely to erythrophagocytose and that infected macrophages engulf more erythrocytes than uninfected macrophages within the same culture well. In addition, macrophages containing erythrocytes harbor more bacteria. However, S. Typhimurium does not promote macrophage engulfment of polystyrene beads, suggesting a role for a ligand on the target cell. Finally, neither of the two S. Typhimurium type 3 secretion systems, T3SS1 or T3SS2, is fully required for hemophagocytosis. These results indicate that infection of macrophages with live S. Typhimurium cells stimulates hemophagocytosis. IMPORTANCE Macrophages are white blood cells (leukocytes) that engulf and destroy pathogens. Hemophagocytes, a subset of macrophages, are characteristic of severe acute infection in patients with, for instance, typhoid fever, brucellosis, tuberculosis, and leishmaniasis. Each of these diseases has the potential to become chronic. Hemophagocytes (blood-eating cells) engulf and degrade red and white blood cells for unknown reasons. The bacterial pathogen Salmonella acquires the essential nutrient iron from murine hemophagocytes. We report that Salmonella stimulates macrophages to engulf blood cells, indicating that cells of this bacterium actively promote the formation of a specialized cellular niche in which they can acquire nutrients, evade killing by the host immune system, and potentially transition to chronic infection.M. Carolina PilonietaSarah M. MorelandChristopher N. EnglishCorrella S. DetweilerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 M. Carolina Pilonieta Sarah M. Moreland Christopher N. English Corrella S. Detweiler <named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose
description	ABSTRACT Hemophagocytes are cells of the monocyte lineage that have engulfed erythrocytes and leukocytes. Hemophagocytes frequently accumulate in patients with severe acute bacterial infections, such as those caused by Salmonella enterica, Brucella abortus, and Mycobacterium tuberculosis. The relationship between hemophagocytosis and infection is not well understood. In the murine liver, S. enterica serovar Typhimurium resides within hemophagocytic macrophages containing leukocytes. Here we show that S. Typhimurium also resides within hemophagocytes containing erythrocytes. In cell culture, S. Typhimurium benefits from residence within hemophagocytes by accessing iron, but why macrophages hemophagocytose is unknown. We show that treatment of macrophages with a cocktail of the proinflammatory cytokine interferon gamma (IFN-γ) and lipopolysaccharide (LPS) stimulates engulfment of nonsenescent erythrocytes. Exposure of resting or IFN-γ-treated macrophages to live, but not to heat-killed, S. Typhimurium cells also stimulates erythrocyte engulfment. Single-cell analyses show that S. Typhimurium-infected macrophages are more likely to erythrophagocytose and that infected macrophages engulf more erythrocytes than uninfected macrophages within the same culture well. In addition, macrophages containing erythrocytes harbor more bacteria. However, S. Typhimurium does not promote macrophage engulfment of polystyrene beads, suggesting a role for a ligand on the target cell. Finally, neither of the two S. Typhimurium type 3 secretion systems, T3SS1 or T3SS2, is fully required for hemophagocytosis. These results indicate that infection of macrophages with live S. Typhimurium cells stimulates hemophagocytosis. IMPORTANCE Macrophages are white blood cells (leukocytes) that engulf and destroy pathogens. Hemophagocytes, a subset of macrophages, are characteristic of severe acute infection in patients with, for instance, typhoid fever, brucellosis, tuberculosis, and leishmaniasis. Each of these diseases has the potential to become chronic. Hemophagocytes (blood-eating cells) engulf and degrade red and white blood cells for unknown reasons. The bacterial pathogen Salmonella acquires the essential nutrient iron from murine hemophagocytes. We report that Salmonella stimulates macrophages to engulf blood cells, indicating that cells of this bacterium actively promote the formation of a specialized cellular niche in which they can acquire nutrients, evade killing by the host immune system, and potentially transition to chronic infection.
format	article
author	M. Carolina Pilonieta Sarah M. Moreland Christopher N. English Corrella S. Detweiler
author_facet	M. Carolina Pilonieta Sarah M. Moreland Christopher N. English Corrella S. Detweiler
author_sort	M. Carolina Pilonieta
title	<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose
title_short	<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose
title_full	<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose
title_fullStr	<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose
title_full_unstemmed	<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose
title_sort	<named-content content-type="genus-species">salmonella enterica</named-content> infection stimulates macrophages to hemophagocytose
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/8b2fcbb6a07f43c4ae98f4726e75a52a
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<named-content content-type="genus-species">Salmonella enterica</named-content> Infection Stimulates Macrophages to Hemophagocytose

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