Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells

Abstract We have recently demonstrated that long-term exposure of cigarette smoke condensate (CSC) to HIV-uninfected (U937) and -infected (U1) macrophages induce packaging of pro-inflammatory molecules, particularly IL-1β, in extracellular vesicles (EVs). Therefore, we hypothesize that exposure of E...

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Main Authors: Sunitha Kodidela, Namita Sinha, Asit Kumar, Lina Zhou, Sandip Godse, Santosh Kumar
Format: Article
Language:English
Published: Nature Portfolio 2023-02-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-29746-y
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author Sunitha Kodidela
Namita Sinha
Asit Kumar
Lina Zhou
Sandip Godse
Santosh Kumar
author_facet Sunitha Kodidela
Namita Sinha
Asit Kumar
Lina Zhou
Sandip Godse
Santosh Kumar
author_sort Sunitha Kodidela
collection DOAJ
description Abstract We have recently demonstrated that long-term exposure of cigarette smoke condensate (CSC) to HIV-uninfected (U937) and -infected (U1) macrophages induce packaging of pro-inflammatory molecules, particularly IL-1β, in extracellular vesicles (EVs). Therefore, we hypothesize that exposure of EVs derived from CSC-treated macrophages to CNS cells can increase their IL-1β levels contributing to neuroinflammation. To test this hypothesis, we treated the U937 and U1 differentiated macrophages once daily with CSC (10 µg/ml) for 7 days. Then, we isolated EVs from these macrophages and treated these EVs with human astrocytic (SVGA) and neuronal (SH-SY5Y) cells in the absence and presence of CSC. We then examined the protein expression of IL-1β and oxidative stress related proteins, cytochrome P450 2A6 (CYP2A6), superoxide dismutase-1 (SOD1), catalase (CAT). We observed that the U937 cells have lower expression of IL-1β compared to their respective EVs, confirming that most of the produced IL-1β are packaged into EVs. Further, EVs isolated from HIV-infected and uninfected cells, both in the absence and presence of CSC, were treated to SVGA and SH-SY5Y cells. These treatments showed a significant increase in the levels of IL-1β in both SVGA and SH-SY5Y cells. However, under the same conditions, the levels of CYP2A6, SOD1, and catalase were only markedly altered. These findings suggest that the macrophages communicate with astrocytes and neuronal cells via EVs-containing IL-1β in both HIV and non-HIV setting and could contribute to neuroinflammation.
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spelling doaj.art-683732b9ed684159a6683fa19613df352023-03-22T10:55:57ZengNature PortfolioScientific Reports2045-23222023-02-0113111210.1038/s41598-023-29746-yExtracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cellsSunitha Kodidela0Namita Sinha1Asit Kumar2Lina Zhou3Sandip Godse4Santosh Kumar5Department of Pharmaceutical Sciences, College of Pharmacy, The University of Tennessee Health Science CenterDepartment of Pharmaceutical Sciences, College of Pharmacy, The University of Tennessee Health Science CenterDepartment of Pharmaceutical Sciences, College of Pharmacy, The University of Tennessee Health Science CenterDepartment of Pharmaceutical Sciences, College of Pharmacy, The University of Tennessee Health Science CenterDepartment of Pharmaceutical Sciences, College of Pharmacy, The University of Tennessee Health Science CenterDepartment of Pharmaceutical Sciences, College of Pharmacy, The University of Tennessee Health Science CenterAbstract We have recently demonstrated that long-term exposure of cigarette smoke condensate (CSC) to HIV-uninfected (U937) and -infected (U1) macrophages induce packaging of pro-inflammatory molecules, particularly IL-1β, in extracellular vesicles (EVs). Therefore, we hypothesize that exposure of EVs derived from CSC-treated macrophages to CNS cells can increase their IL-1β levels contributing to neuroinflammation. To test this hypothesis, we treated the U937 and U1 differentiated macrophages once daily with CSC (10 µg/ml) for 7 days. Then, we isolated EVs from these macrophages and treated these EVs with human astrocytic (SVGA) and neuronal (SH-SY5Y) cells in the absence and presence of CSC. We then examined the protein expression of IL-1β and oxidative stress related proteins, cytochrome P450 2A6 (CYP2A6), superoxide dismutase-1 (SOD1), catalase (CAT). We observed that the U937 cells have lower expression of IL-1β compared to their respective EVs, confirming that most of the produced IL-1β are packaged into EVs. Further, EVs isolated from HIV-infected and uninfected cells, both in the absence and presence of CSC, were treated to SVGA and SH-SY5Y cells. These treatments showed a significant increase in the levels of IL-1β in both SVGA and SH-SY5Y cells. However, under the same conditions, the levels of CYP2A6, SOD1, and catalase were only markedly altered. These findings suggest that the macrophages communicate with astrocytes and neuronal cells via EVs-containing IL-1β in both HIV and non-HIV setting and could contribute to neuroinflammation.https://doi.org/10.1038/s41598-023-29746-y
spellingShingle Sunitha Kodidela
Namita Sinha
Asit Kumar
Lina Zhou
Sandip Godse
Santosh Kumar
Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells
Scientific Reports
title Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells
title_full Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells
title_fullStr Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells
title_full_unstemmed Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells
title_short Extracellular vesicles released from macrophages modulates interleukin-1β in astrocytic and neuronal cells
title_sort extracellular vesicles released from macrophages modulates interleukin 1β in astrocytic and neuronal cells
url https://doi.org/10.1038/s41598-023-29746-y
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