Immunomodulatory role for membrane vesicles released by THP-1 macrophages and respiratory pathogens during macrophage infection

Charlotte Volgers, Birke J. Benedikter, Gert E. Grauls, Paul H.M. Savelkoul, Frank R.M. Stassen

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Background: During infection, inflammation is partially driven by the release of mediators which facilitate intercellular communication. Amongst these mediators are small membrane vesicles (MVs) that can be released by both host cells and Gram-negative and -positive bacteria. Bacterial membrane vesicles are known to exert immuno-modulatory and -stimulatory actions. Moreover, it has been proposed that host cell-derived vesicles, released during infection, also have immunostimulatory properties. In this study, we assessed the release and activity of host cell-derived and bacterial MVs during the first hours following infection of THP-1 macrophages with the common respiratory pathogens non-typeable Haemophilus influenzae, Moraxella catarrhalis, Streptococcus pneumoniae, and Pseudomonas aeruginosa. Results: Using a combination of flow cytometry, tunable resistive pulse sensing (TRPS)-based analysis and electron microscopy, we demonstrated that the release of MVs occurs by both host cells and bacteria during infection. MVs released during infection and bacterial culture were found to induce a strong pro-inflammatory response by naive THP-1 macrophages. Yet, these MVs were also found to induce tolerance of host cells to secondary immunogenic stimuli and to enhance bacterial adherence and the number of intracellular bacteria. Conclusions: Bacterial MVs may play a dual role during infection, as they can both trigger and dampen immune responses thereby contributing to immune defence and bacterial survival.

Original languageEnglish
Article number216
JournalBMC Microbiology
Volume17
Issue number1
DOIs
Publication statusPublished - 13 Nov 2017

Cite this

Volgers, Charlotte ; Benedikter, Birke J. ; Grauls, Gert E. ; Savelkoul, Paul H.M. ; Stassen, Frank R.M. / Immunomodulatory role for membrane vesicles released by THP-1 macrophages and respiratory pathogens during macrophage infection. In: BMC Microbiology. 2017 ; Vol. 17, No. 1.
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title = "Immunomodulatory role for membrane vesicles released by THP-1 macrophages and respiratory pathogens during macrophage infection",
abstract = "Background: During infection, inflammation is partially driven by the release of mediators which facilitate intercellular communication. Amongst these mediators are small membrane vesicles (MVs) that can be released by both host cells and Gram-negative and -positive bacteria. Bacterial membrane vesicles are known to exert immuno-modulatory and -stimulatory actions. Moreover, it has been proposed that host cell-derived vesicles, released during infection, also have immunostimulatory properties. In this study, we assessed the release and activity of host cell-derived and bacterial MVs during the first hours following infection of THP-1 macrophages with the common respiratory pathogens non-typeable Haemophilus influenzae, Moraxella catarrhalis, Streptococcus pneumoniae, and Pseudomonas aeruginosa. Results: Using a combination of flow cytometry, tunable resistive pulse sensing (TRPS)-based analysis and electron microscopy, we demonstrated that the release of MVs occurs by both host cells and bacteria during infection. MVs released during infection and bacterial culture were found to induce a strong pro-inflammatory response by naive THP-1 macrophages. Yet, these MVs were also found to induce tolerance of host cells to secondary immunogenic stimuli and to enhance bacterial adherence and the number of intracellular bacteria. Conclusions: Bacterial MVs may play a dual role during infection, as they can both trigger and dampen immune responses thereby contributing to immune defence and bacterial survival.",
keywords = "Bacterial infection, Extracellular vesicles, Immuno-modulation, Inflammatory response, Membrane vesicles, Moraxella catarrhalis, Non-typeable Haemophilus influenzae, Outer membrane vesicles, Pseudomonas Aeruginosa, Streptococcus Pneumoniae",
author = "Charlotte Volgers and Benedikter, {Birke J.} and Grauls, {Gert E.} and Savelkoul, {Paul H.M.} and Stassen, {Frank R.M.}",
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Immunomodulatory role for membrane vesicles released by THP-1 macrophages and respiratory pathogens during macrophage infection. / Volgers, Charlotte; Benedikter, Birke J.; Grauls, Gert E.; Savelkoul, Paul H.M.; Stassen, Frank R.M.

In: BMC Microbiology, Vol. 17, No. 1, 216, 13.11.2017.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Immunomodulatory role for membrane vesicles released by THP-1 macrophages and respiratory pathogens during macrophage infection

AU - Volgers, Charlotte

AU - Benedikter, Birke J.

AU - Grauls, Gert E.

AU - Savelkoul, Paul H.M.

AU - Stassen, Frank R.M.

PY - 2017/11/13

Y1 - 2017/11/13

N2 - Background: During infection, inflammation is partially driven by the release of mediators which facilitate intercellular communication. Amongst these mediators are small membrane vesicles (MVs) that can be released by both host cells and Gram-negative and -positive bacteria. Bacterial membrane vesicles are known to exert immuno-modulatory and -stimulatory actions. Moreover, it has been proposed that host cell-derived vesicles, released during infection, also have immunostimulatory properties. In this study, we assessed the release and activity of host cell-derived and bacterial MVs during the first hours following infection of THP-1 macrophages with the common respiratory pathogens non-typeable Haemophilus influenzae, Moraxella catarrhalis, Streptococcus pneumoniae, and Pseudomonas aeruginosa. Results: Using a combination of flow cytometry, tunable resistive pulse sensing (TRPS)-based analysis and electron microscopy, we demonstrated that the release of MVs occurs by both host cells and bacteria during infection. MVs released during infection and bacterial culture were found to induce a strong pro-inflammatory response by naive THP-1 macrophages. Yet, these MVs were also found to induce tolerance of host cells to secondary immunogenic stimuli and to enhance bacterial adherence and the number of intracellular bacteria. Conclusions: Bacterial MVs may play a dual role during infection, as they can both trigger and dampen immune responses thereby contributing to immune defence and bacterial survival.

AB - Background: During infection, inflammation is partially driven by the release of mediators which facilitate intercellular communication. Amongst these mediators are small membrane vesicles (MVs) that can be released by both host cells and Gram-negative and -positive bacteria. Bacterial membrane vesicles are known to exert immuno-modulatory and -stimulatory actions. Moreover, it has been proposed that host cell-derived vesicles, released during infection, also have immunostimulatory properties. In this study, we assessed the release and activity of host cell-derived and bacterial MVs during the first hours following infection of THP-1 macrophages with the common respiratory pathogens non-typeable Haemophilus influenzae, Moraxella catarrhalis, Streptococcus pneumoniae, and Pseudomonas aeruginosa. Results: Using a combination of flow cytometry, tunable resistive pulse sensing (TRPS)-based analysis and electron microscopy, we demonstrated that the release of MVs occurs by both host cells and bacteria during infection. MVs released during infection and bacterial culture were found to induce a strong pro-inflammatory response by naive THP-1 macrophages. Yet, these MVs were also found to induce tolerance of host cells to secondary immunogenic stimuli and to enhance bacterial adherence and the number of intracellular bacteria. Conclusions: Bacterial MVs may play a dual role during infection, as they can both trigger and dampen immune responses thereby contributing to immune defence and bacterial survival.

KW - Bacterial infection

KW - Extracellular vesicles

KW - Immuno-modulation

KW - Inflammatory response

KW - Membrane vesicles

KW - Moraxella catarrhalis

KW - Non-typeable Haemophilus influenzae

KW - Outer membrane vesicles

KW - Pseudomonas Aeruginosa

KW - Streptococcus Pneumoniae

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U2 - 10.1186/s12866-017-1122-3

DO - 10.1186/s12866-017-1122-3

M3 - Article

VL - 17

JO - BMC Microbiology

JF - BMC Microbiology

SN - 1471-2180

IS - 1

M1 - 216

ER -