Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.

Exposure to silver nanoparticles (AgNP) used in consumer products carries potential health risks including increased susceptibility to infectious pathogens. Systematic assessments of antimicrobial macrophage immune responses in the context of AgNP exposure are important because uptake of AgNP by mac...

Full description

Saved in:
Bibliographic Details
Main Authors: Srijata Sarkar, Bey Fen Leo, Claudia Carranza, Shu Chen, Cesar Rivas-Santiago, Alexandra E Porter, Mary P Ryan, Andrew Gow, Kian Fan Chung, Teresa D Tetley, Junfeng Jim Zhang, Panos G Georgopoulos, Pamela A Ohman-Strickland, Stephan Schwander
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0143077&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849726621086384128
author Srijata Sarkar
Bey Fen Leo
Claudia Carranza
Shu Chen
Cesar Rivas-Santiago
Alexandra E Porter
Mary P Ryan
Andrew Gow
Kian Fan Chung
Teresa D Tetley
Junfeng Jim Zhang
Panos G Georgopoulos
Pamela A Ohman-Strickland
Stephan Schwander
author_facet Srijata Sarkar
Bey Fen Leo
Claudia Carranza
Shu Chen
Cesar Rivas-Santiago
Alexandra E Porter
Mary P Ryan
Andrew Gow
Kian Fan Chung
Teresa D Tetley
Junfeng Jim Zhang
Panos G Georgopoulos
Pamela A Ohman-Strickland
Stephan Schwander
author_sort Srijata Sarkar
collection DOAJ
description Exposure to silver nanoparticles (AgNP) used in consumer products carries potential health risks including increased susceptibility to infectious pathogens. Systematic assessments of antimicrobial macrophage immune responses in the context of AgNP exposure are important because uptake of AgNP by macrophages may lead to alterations of innate immune cell functions. In this study we examined the effects of exposure to AgNP with different particle sizes (20 and 110 nm diameters) and surface chemistry (citrate or polyvinlypyrrolidone capping) on cellular toxicity and innate immune responses against Mycobacterium tuberculosis (M.tb) by human monocyte-derived macrophages (MDM). Exposures of MDM to AgNP significantly reduced cellular viability, increased IL8 and decreased IL10 mRNA expression. Exposure of M.tb-infected MDM to AgNP suppressed M.tb-induced expression of IL1B, IL10, and TNFA mRNA. Furthermore, M.tb-induced IL-1β, a cytokine critical for host resistance to M.tb, was inhibited by AgNP but not by carbon black particles indicating that the observed immunosuppressive effects of AgNP are particle specific. Suppressive effects of AgNP on the M.tb-induced host immune responses were in part due to AgNP-mediated interferences with the TLR signaling pathways that culminate in the activation of the transcription factor NF-κB. AgNP exposure suppressed M.tb-induced expression of a subset of NF-κB mediated genes (CSF2, CSF3, IFNG, IL1A, IL1B, IL6, IL10, TNFA, NFKB1A). In addition, AgNP exposure increased the expression of HSPA1A mRNA and the corresponding stress-induced Hsp72 protein. Up-regulation of Hsp72 by AgNP can suppress M.tb-induced NF-κB activation and host immune responses. The observed ability of AgNP to modulate infectious pathogen-induced immune responses has important public health implications.
format Article
id doaj-art-95dc6d0bf8704c56a3ff5ae7b7fc8a95
institution DOAJ
issn 1932-6203
language English
publishDate 2015-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-95dc6d0bf8704c56a3ff5ae7b7fc8a952025-08-20T03:10:07ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-011011e014307710.1371/journal.pone.0143077Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.Srijata SarkarBey Fen LeoClaudia CarranzaShu ChenCesar Rivas-SantiagoAlexandra E PorterMary P RyanAndrew GowKian Fan ChungTeresa D TetleyJunfeng Jim ZhangPanos G GeorgopoulosPamela A Ohman-StricklandStephan SchwanderExposure to silver nanoparticles (AgNP) used in consumer products carries potential health risks including increased susceptibility to infectious pathogens. Systematic assessments of antimicrobial macrophage immune responses in the context of AgNP exposure are important because uptake of AgNP by macrophages may lead to alterations of innate immune cell functions. In this study we examined the effects of exposure to AgNP with different particle sizes (20 and 110 nm diameters) and surface chemistry (citrate or polyvinlypyrrolidone capping) on cellular toxicity and innate immune responses against Mycobacterium tuberculosis (M.tb) by human monocyte-derived macrophages (MDM). Exposures of MDM to AgNP significantly reduced cellular viability, increased IL8 and decreased IL10 mRNA expression. Exposure of M.tb-infected MDM to AgNP suppressed M.tb-induced expression of IL1B, IL10, and TNFA mRNA. Furthermore, M.tb-induced IL-1β, a cytokine critical for host resistance to M.tb, was inhibited by AgNP but not by carbon black particles indicating that the observed immunosuppressive effects of AgNP are particle specific. Suppressive effects of AgNP on the M.tb-induced host immune responses were in part due to AgNP-mediated interferences with the TLR signaling pathways that culminate in the activation of the transcription factor NF-κB. AgNP exposure suppressed M.tb-induced expression of a subset of NF-κB mediated genes (CSF2, CSF3, IFNG, IL1A, IL1B, IL6, IL10, TNFA, NFKB1A). In addition, AgNP exposure increased the expression of HSPA1A mRNA and the corresponding stress-induced Hsp72 protein. Up-regulation of Hsp72 by AgNP can suppress M.tb-induced NF-κB activation and host immune responses. The observed ability of AgNP to modulate infectious pathogen-induced immune responses has important public health implications.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0143077&type=printable
spellingShingle Srijata Sarkar
Bey Fen Leo
Claudia Carranza
Shu Chen
Cesar Rivas-Santiago
Alexandra E Porter
Mary P Ryan
Andrew Gow
Kian Fan Chung
Teresa D Tetley
Junfeng Jim Zhang
Panos G Georgopoulos
Pamela A Ohman-Strickland
Stephan Schwander
Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.
PLoS ONE
title Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.
title_full Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.
title_fullStr Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.
title_full_unstemmed Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.
title_short Modulation of Human Macrophage Responses to Mycobacterium tuberculosis by Silver Nanoparticles of Different Size and Surface Modification.
title_sort modulation of human macrophage responses to mycobacterium tuberculosis by silver nanoparticles of different size and surface modification
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0143077&type=printable
work_keys_str_mv AT srijatasarkar modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT beyfenleo modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT claudiacarranza modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT shuchen modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT cesarrivassantiago modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT alexandraeporter modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT marypryan modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT andrewgow modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT kianfanchung modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT teresadtetley modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT junfengjimzhang modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT panosggeorgopoulos modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT pamelaaohmanstrickland modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification
AT stephanschwander modulationofhumanmacrophageresponsestomycobacteriumtuberculosisbysilvernanoparticlesofdifferentsizeandsurfacemodification