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Inhibition of protein translation under matrix-deprivation stress in breast cancer cells

Matrix-deprivation stress leads to cell-death by anoikis, whereas overcoming anoikis is critical for cancer metastasis. Work from our lab and others has identified a crucial role for the cellular energy sensor AMPK in anoikis-resistance, highlighting a key role for metabolic reprogramming in stress...

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Autores principales: Warrier, Shweta, Srinivasan, Shivaani, Chedere, Adithya, Rangarajan, Annapoorni
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10324034/
https://www.ncbi.nlm.nih.gov/pubmed/37425300
http://dx.doi.org/10.3389/fmed.2023.1124514
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author Warrier, Shweta
Srinivasan, Shivaani
Chedere, Adithya
Rangarajan, Annapoorni
author_facet Warrier, Shweta
Srinivasan, Shivaani
Chedere, Adithya
Rangarajan, Annapoorni
author_sort Warrier, Shweta
collection PubMed
description Matrix-deprivation stress leads to cell-death by anoikis, whereas overcoming anoikis is critical for cancer metastasis. Work from our lab and others has identified a crucial role for the cellular energy sensor AMPK in anoikis-resistance, highlighting a key role for metabolic reprogramming in stress survival. Protein synthesis is a major energy-consuming process that is tightly regulated under stress. Although an increase in protein synthesis in AMPK-depleted experimentally-transformed MEFs has been associated with anoikis, the status and regulation of protein translation in epithelial-origin cancer cells facing matrix-detachment remains largely unknown. Our study shows that protein translation is mechanistically abrogated at both initiation and elongation stages by the activation of the unfolded protein response (UPR) pathway and inactivation of elongation factor eEF2, respectively. Additionally, we show inhibition of the mTORC1 pathway known for regulation of canonical protein synthesis. We further functionally assay this inhibition using SUnSET assay, which demonstrates repression of global protein synthesis in MDA-MB-231 and MCF7 breast cancer cells when subjected to matrix-deprivation. In order to gauge the translational status of matrix-deprived cancer cells, we undertook polysome profiling. Our data revealed reduced but continuous mRNA translation under matrix-deprivation stress. An integrated analysis of transcriptomic and proteomic data further identifies novel targets that may aid cellular adaptations to matrix-deprivation stress and can be explored for therapeutic intervention.
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spelling pubmed-103240342023-07-07 Inhibition of protein translation under matrix-deprivation stress in breast cancer cells Warrier, Shweta Srinivasan, Shivaani Chedere, Adithya Rangarajan, Annapoorni Front Med (Lausanne) Medicine Matrix-deprivation stress leads to cell-death by anoikis, whereas overcoming anoikis is critical for cancer metastasis. Work from our lab and others has identified a crucial role for the cellular energy sensor AMPK in anoikis-resistance, highlighting a key role for metabolic reprogramming in stress survival. Protein synthesis is a major energy-consuming process that is tightly regulated under stress. Although an increase in protein synthesis in AMPK-depleted experimentally-transformed MEFs has been associated with anoikis, the status and regulation of protein translation in epithelial-origin cancer cells facing matrix-detachment remains largely unknown. Our study shows that protein translation is mechanistically abrogated at both initiation and elongation stages by the activation of the unfolded protein response (UPR) pathway and inactivation of elongation factor eEF2, respectively. Additionally, we show inhibition of the mTORC1 pathway known for regulation of canonical protein synthesis. We further functionally assay this inhibition using SUnSET assay, which demonstrates repression of global protein synthesis in MDA-MB-231 and MCF7 breast cancer cells when subjected to matrix-deprivation. In order to gauge the translational status of matrix-deprived cancer cells, we undertook polysome profiling. Our data revealed reduced but continuous mRNA translation under matrix-deprivation stress. An integrated analysis of transcriptomic and proteomic data further identifies novel targets that may aid cellular adaptations to matrix-deprivation stress and can be explored for therapeutic intervention. Frontiers Media S.A. 2023-06-22 /pmc/articles/PMC10324034/ /pubmed/37425300 http://dx.doi.org/10.3389/fmed.2023.1124514 Text en Copyright © 2023 Warrier, Srinivasan, Chedere and Rangarajan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Medicine
Warrier, Shweta
Srinivasan, Shivaani
Chedere, Adithya
Rangarajan, Annapoorni
Inhibition of protein translation under matrix-deprivation stress in breast cancer cells
title Inhibition of protein translation under matrix-deprivation stress in breast cancer cells
title_full Inhibition of protein translation under matrix-deprivation stress in breast cancer cells
title_fullStr Inhibition of protein translation under matrix-deprivation stress in breast cancer cells
title_full_unstemmed Inhibition of protein translation under matrix-deprivation stress in breast cancer cells
title_short Inhibition of protein translation under matrix-deprivation stress in breast cancer cells
title_sort inhibition of protein translation under matrix-deprivation stress in breast cancer cells
topic Medicine
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10324034/
https://www.ncbi.nlm.nih.gov/pubmed/37425300
http://dx.doi.org/10.3389/fmed.2023.1124514
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