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Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA

Increased PDGFRA signaling is an essential pathogenic factor in many subtypes of gliomas. In this context the cell surface expression of PDGFRA is an important determinant of ligand sensing in the glioma microenvironment. However, the regulation of spatial distribution of PDGFRA in glioma cells rema...

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Autores principales: Chen, Dongfeng, Zuo, Duo, Luan, Cheng, Liu, Min, Na, Manli, Ran, Liang, Sun, Yingyu, Persson, Annette, Englund, Elisabet, Salford, Leif G., Renström, Erik, Fan, Xiaolong, Zhang, Enming
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3906156/
https://www.ncbi.nlm.nih.gov/pubmed/24489888
http://dx.doi.org/10.1371/journal.pone.0087281
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author Chen, Dongfeng
Zuo, Duo
Luan, Cheng
Liu, Min
Na, Manli
Ran, Liang
Sun, Yingyu
Persson, Annette
Englund, Elisabet
Salford, Leif G.
Renström, Erik
Fan, Xiaolong
Zhang, Enming
author_facet Chen, Dongfeng
Zuo, Duo
Luan, Cheng
Liu, Min
Na, Manli
Ran, Liang
Sun, Yingyu
Persson, Annette
Englund, Elisabet
Salford, Leif G.
Renström, Erik
Fan, Xiaolong
Zhang, Enming
author_sort Chen, Dongfeng
collection PubMed
description Increased PDGFRA signaling is an essential pathogenic factor in many subtypes of gliomas. In this context the cell surface expression of PDGFRA is an important determinant of ligand sensing in the glioma microenvironment. However, the regulation of spatial distribution of PDGFRA in glioma cells remains poorly characterized. Here, we report that cell surface PDGFRA expression in gliomas is negatively regulated by an ERK-dependent mechanism, resulting in reduced proliferation of glioma cells. Glioma tumor tissues and their corresponding cell lines were isolated from 14 patients and analyzed by single-cell imaging and flow cytometry. In both cell lines and their corresponding tumor samples, glioma cell proliferation correlated with the extent of surface expression of PDGFRA. High levels of surface PDGFRA also correlated to high tubulin expression in glioma tumor tissue in vivo. In glioma cell lines, surface PDGFRA declined following treatment with inhibitors of tubulin, actin and dynamin. Screening of a panel of small molecule compounds identified the MEK inhibitor U0126 as a potent inhibitor of surface PDGFRA expression. Importantly, U0126 inhibited surface expression in a reversible, dose- and time-dependent manner, without affecting general PDGFRA expression. Treatment with U0126 resulted in reduced co-localization between PDGFRA and intracellular trafficking molecules e.g. clathrin, RAB11 and early endosomal antigen-1, in parallel with enhanced co-localization between PDGFRA and the Golgi cisternae maker, Giantin, suggesting a deviation of PDGFRA from the endosomal trafficking and recycling compartment, to the Golgi network. Furthermore, U0126 treatment in glioma cells induced an initial inhibition of ERK1/2 phosphorylation, followed by up-regulated ERK1/2 phosphorylation concomitant with diminished surface expression of PDGFRA. Finally, down-regulation of surface PDGFRA expression by U0126 is concordant with reduced glioma cell proliferation. These findings suggest that manipulation of spatial expression of PDGFRA can potentially be used to combat gliomas.
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spelling pubmed-39061562014-01-31 Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA Chen, Dongfeng Zuo, Duo Luan, Cheng Liu, Min Na, Manli Ran, Liang Sun, Yingyu Persson, Annette Englund, Elisabet Salford, Leif G. Renström, Erik Fan, Xiaolong Zhang, Enming PLoS One Research Article Increased PDGFRA signaling is an essential pathogenic factor in many subtypes of gliomas. In this context the cell surface expression of PDGFRA is an important determinant of ligand sensing in the glioma microenvironment. However, the regulation of spatial distribution of PDGFRA in glioma cells remains poorly characterized. Here, we report that cell surface PDGFRA expression in gliomas is negatively regulated by an ERK-dependent mechanism, resulting in reduced proliferation of glioma cells. Glioma tumor tissues and their corresponding cell lines were isolated from 14 patients and analyzed by single-cell imaging and flow cytometry. In both cell lines and their corresponding tumor samples, glioma cell proliferation correlated with the extent of surface expression of PDGFRA. High levels of surface PDGFRA also correlated to high tubulin expression in glioma tumor tissue in vivo. In glioma cell lines, surface PDGFRA declined following treatment with inhibitors of tubulin, actin and dynamin. Screening of a panel of small molecule compounds identified the MEK inhibitor U0126 as a potent inhibitor of surface PDGFRA expression. Importantly, U0126 inhibited surface expression in a reversible, dose- and time-dependent manner, without affecting general PDGFRA expression. Treatment with U0126 resulted in reduced co-localization between PDGFRA and intracellular trafficking molecules e.g. clathrin, RAB11 and early endosomal antigen-1, in parallel with enhanced co-localization between PDGFRA and the Golgi cisternae maker, Giantin, suggesting a deviation of PDGFRA from the endosomal trafficking and recycling compartment, to the Golgi network. Furthermore, U0126 treatment in glioma cells induced an initial inhibition of ERK1/2 phosphorylation, followed by up-regulated ERK1/2 phosphorylation concomitant with diminished surface expression of PDGFRA. Finally, down-regulation of surface PDGFRA expression by U0126 is concordant with reduced glioma cell proliferation. These findings suggest that manipulation of spatial expression of PDGFRA can potentially be used to combat gliomas. Public Library of Science 2014-01-29 /pmc/articles/PMC3906156/ /pubmed/24489888 http://dx.doi.org/10.1371/journal.pone.0087281 Text en © 2014 Chen et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Chen, Dongfeng
Zuo, Duo
Luan, Cheng
Liu, Min
Na, Manli
Ran, Liang
Sun, Yingyu
Persson, Annette
Englund, Elisabet
Salford, Leif G.
Renström, Erik
Fan, Xiaolong
Zhang, Enming
Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA
title Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA
title_full Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA
title_fullStr Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA
title_full_unstemmed Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA
title_short Glioma Cell Proliferation Controlled by ERK Activity-Dependent Surface Expression of PDGFRA
title_sort glioma cell proliferation controlled by erk activity-dependent surface expression of pdgfra
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3906156/
https://www.ncbi.nlm.nih.gov/pubmed/24489888
http://dx.doi.org/10.1371/journal.pone.0087281
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