Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis

Macrophages have a vital role in the immune system through elimination of cell debris and microorganisms by phagocytosis. The activation of macrophages by tumour necrosis factor-α induces expression of extracellular cell-surface vimentin and promotes release of this vimentin into the extracellular e...

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Main Authors: Divyendu Goud Thalla, Ashish Chand Rajwar, Annalena Maria Laurent, Johanna Elisabeth Becher, Lucina Kainka, Franziska Lautenschläger
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2022.891281/full
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author Divyendu Goud Thalla
Ashish Chand Rajwar
Annalena Maria Laurent
Johanna Elisabeth Becher
Lucina Kainka
Franziska Lautenschläger
Franziska Lautenschläger
author_facet Divyendu Goud Thalla
Ashish Chand Rajwar
Annalena Maria Laurent
Johanna Elisabeth Becher
Lucina Kainka
Franziska Lautenschläger
Franziska Lautenschläger
author_sort Divyendu Goud Thalla
collection DOAJ
description Macrophages have a vital role in the immune system through elimination of cell debris and microorganisms by phagocytosis. The activation of macrophages by tumour necrosis factor-α induces expression of extracellular cell-surface vimentin and promotes release of this vimentin into the extracellular environment. Vimentin is a cytoskeletal protein that is primarily located in the cytoplasm of cells. However, under circumstances like injury, stress, senescence and activation, vimentin can be expressed on the extracellular cell surface, or it can be released into the extracellular space. The characteristics of this extracellular vimentin, and its implications for the functional role of macrophages and the mechanism of secretion remain unclear. Here, we demonstrate that vimentin is released mainly from the back of macrophage-like cells. This polarisation is strongly enhanced upon macrophage activation. One-dimensional patterned lines showed that extracellular cell-surface vimentin is localised primarily at the back of activated macrophage-like cells. Through two-dimensional migration and phagocytosis assays, we show that this extracellular vimentin enhances migration and phagocytosis of macrophage-like cells. We further show that this extracellular vimentin forms agglomerates on the cell surface, in contrast to its intracellular filamentous form, and that it is released into the extracellular space in the form of small fragments. Taken together, we provide new insights into the release of extracellular cell-surface vimentin and its implications for macrophage functionality.
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spelling doaj.art-a24c8d26d9b4486496bde176bb6eeb3f2022-12-22T03:43:03ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-07-011010.3389/fcell.2022.891281891281Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosisDivyendu Goud Thalla0Ashish Chand Rajwar1Annalena Maria Laurent2Johanna Elisabeth Becher3Lucina Kainka4Franziska Lautenschläger5Franziska Lautenschläger6Experimental Physics, Saarland University, Saarbrücken, GermanyExperimental Physics, Saarland University, Saarbrücken, GermanyExperimental Physics, Saarland University, Saarbrücken, GermanyCentre for Bioinformatics, Saarland University, Saarbrücken, GermanyExperimental Physics, Saarland University, Saarbrücken, GermanyExperimental Physics, Saarland University, Saarbrücken, GermanyCentre for Biophysics, Saarland University, Saarbrücken, GermanyMacrophages have a vital role in the immune system through elimination of cell debris and microorganisms by phagocytosis. The activation of macrophages by tumour necrosis factor-α induces expression of extracellular cell-surface vimentin and promotes release of this vimentin into the extracellular environment. Vimentin is a cytoskeletal protein that is primarily located in the cytoplasm of cells. However, under circumstances like injury, stress, senescence and activation, vimentin can be expressed on the extracellular cell surface, or it can be released into the extracellular space. The characteristics of this extracellular vimentin, and its implications for the functional role of macrophages and the mechanism of secretion remain unclear. Here, we demonstrate that vimentin is released mainly from the back of macrophage-like cells. This polarisation is strongly enhanced upon macrophage activation. One-dimensional patterned lines showed that extracellular cell-surface vimentin is localised primarily at the back of activated macrophage-like cells. Through two-dimensional migration and phagocytosis assays, we show that this extracellular vimentin enhances migration and phagocytosis of macrophage-like cells. We further show that this extracellular vimentin forms agglomerates on the cell surface, in contrast to its intracellular filamentous form, and that it is released into the extracellular space in the form of small fragments. Taken together, we provide new insights into the release of extracellular cell-surface vimentin and its implications for macrophage functionality.https://www.frontiersin.org/articles/10.3389/fcell.2022.891281/fullextracellular vimentinmacrophagesactivationmigrationpolarisationphagocytosis
spellingShingle Divyendu Goud Thalla
Ashish Chand Rajwar
Annalena Maria Laurent
Johanna Elisabeth Becher
Lucina Kainka
Franziska Lautenschläger
Franziska Lautenschläger
Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis
Frontiers in Cell and Developmental Biology
extracellular vimentin
macrophages
activation
migration
polarisation
phagocytosis
title Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis
title_full Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis
title_fullStr Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis
title_full_unstemmed Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis
title_short Extracellular vimentin is expressed at the rear of activated macrophage-like cells: Potential role in enhancement of migration and phagocytosis
title_sort extracellular vimentin is expressed at the rear of activated macrophage like cells potential role in enhancement of migration and phagocytosis
topic extracellular vimentin
macrophages
activation
migration
polarisation
phagocytosis
url https://www.frontiersin.org/articles/10.3389/fcell.2022.891281/full
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