Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells

Stress granules (SGs) are assemblies of selective messenger RNAs (mRNAs), translation factors, and RNA-binding proteins in small untranslated messenger ribonucleoprotein (mRNP) complexes in the cytoplasm. Evidence indicates that different types of cells have shown different mechanisms to respond to...

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Main Authors: Salam Salloum-Asfar, Rudolf Engelke, Hanaa Mousa, Neha Goswami, I. Richard Thompson, Freshteh Palangi, Kamal Kamal, Muna N. Al-Noubi, Frank Schmidt, Sara A. Abdulla, Mohamed M. Emara
Format: Article
Language:English
Published: Wiley 2021-01-01
Series:Stem Cells International
Online Access:http://dx.doi.org/10.1155/2021/8274936
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author Salam Salloum-Asfar
Rudolf Engelke
Hanaa Mousa
Neha Goswami
I. Richard Thompson
Freshteh Palangi
Kamal Kamal
Muna N. Al-Noubi
Frank Schmidt
Sara A. Abdulla
Mohamed M. Emara
author_facet Salam Salloum-Asfar
Rudolf Engelke
Hanaa Mousa
Neha Goswami
I. Richard Thompson
Freshteh Palangi
Kamal Kamal
Muna N. Al-Noubi
Frank Schmidt
Sara A. Abdulla
Mohamed M. Emara
author_sort Salam Salloum-Asfar
collection DOAJ
description Stress granules (SGs) are assemblies of selective messenger RNAs (mRNAs), translation factors, and RNA-binding proteins in small untranslated messenger ribonucleoprotein (mRNP) complexes in the cytoplasm. Evidence indicates that different types of cells have shown different mechanisms to respond to stress and the formation of SGs. In the present work, we investigated how human-induced pluripotent stem cells (hiPSCs/IMR90-1) overcome hyperosmotic stress compared to a cell line that does not harbor pluripotent characteristics (SH-SY5Y cell line). Gradient concentrations of NaCl showed a different pattern of SG formation between hiPSCs/IMR90-1 and the nonpluripotent cell line SH-SY5Y. Other pluripotent stem cell lines (hiPSCs/CRTD5 and hESCs/H9 (human embryonic stem cell line)) as well as nonpluripotent cell lines (BHK-21 and MCF-7) were used to confirm this phenomenon. Moreover, the formation of hyperosmotic SGs in hiPSCs/IMR90-1 was independent of eIF2α phosphorylation and was associated with low apoptosis levels. In addition, a comprehensive proteomics analysis was performed to identify proteins involved in regulating this specific pattern of hyperosmotic SG formation in hiPSCs/IMR90-1. We found possible implications of microtubule organization on the response to hyperosmotic stress in hiPSCs/IMR90-1. We have also unveiled a reduced expression of tubulin that may protect cells against hyperosmolarity stress while inhibiting SG formation without affecting stem cell self-renewal and pluripotency. Our observations may provide a possible cellular mechanism to better understand SG dynamics in pluripotent stem cells.
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spelling doaj-art-1205d84d15c8408f8cc7c6e1293284642025-02-03T05:45:19ZengWileyStem Cells International1687-966X1687-96782021-01-01202110.1155/2021/82749368274936Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem CellsSalam Salloum-Asfar0Rudolf Engelke1Hanaa Mousa2Neha Goswami3I. Richard Thompson4Freshteh Palangi5Kamal Kamal6Muna N. Al-Noubi7Frank Schmidt8Sara A. Abdulla9Mohamed M. Emara10Neurological Disorders Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Education City, Qatar Foundation (QF), Doha, QatarProteomics Core, Weill Cornell Medical College-Qatar, Qatar Foundation, Doha, QatarBasic Medical Sciences Department, College of Medicine, QU Health, Qatar University, Doha, QatarProteomics Core, Weill Cornell Medical College-Qatar, Qatar Foundation, Doha, QatarDiabetes Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Education City, Qatar Foundation (QF), Doha, QatarNeurological Disorders Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Education City, Qatar Foundation (QF), Doha, QatarNeurological Disorders Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Education City, Qatar Foundation (QF), Doha, QatarProteomics Core, Weill Cornell Medical College-Qatar, Qatar Foundation, Doha, QatarProteomics Core, Weill Cornell Medical College-Qatar, Qatar Foundation, Doha, QatarNeurological Disorders Research Center, Qatar Biomedical Research Institute (QBRI), Hamad Bin Khalifa University (HBKU), Education City, Qatar Foundation (QF), Doha, QatarBasic Medical Sciences Department, College of Medicine, QU Health, Qatar University, Doha, QatarStress granules (SGs) are assemblies of selective messenger RNAs (mRNAs), translation factors, and RNA-binding proteins in small untranslated messenger ribonucleoprotein (mRNP) complexes in the cytoplasm. Evidence indicates that different types of cells have shown different mechanisms to respond to stress and the formation of SGs. In the present work, we investigated how human-induced pluripotent stem cells (hiPSCs/IMR90-1) overcome hyperosmotic stress compared to a cell line that does not harbor pluripotent characteristics (SH-SY5Y cell line). Gradient concentrations of NaCl showed a different pattern of SG formation between hiPSCs/IMR90-1 and the nonpluripotent cell line SH-SY5Y. Other pluripotent stem cell lines (hiPSCs/CRTD5 and hESCs/H9 (human embryonic stem cell line)) as well as nonpluripotent cell lines (BHK-21 and MCF-7) were used to confirm this phenomenon. Moreover, the formation of hyperosmotic SGs in hiPSCs/IMR90-1 was independent of eIF2α phosphorylation and was associated with low apoptosis levels. In addition, a comprehensive proteomics analysis was performed to identify proteins involved in regulating this specific pattern of hyperosmotic SG formation in hiPSCs/IMR90-1. We found possible implications of microtubule organization on the response to hyperosmotic stress in hiPSCs/IMR90-1. We have also unveiled a reduced expression of tubulin that may protect cells against hyperosmolarity stress while inhibiting SG formation without affecting stem cell self-renewal and pluripotency. Our observations may provide a possible cellular mechanism to better understand SG dynamics in pluripotent stem cells.http://dx.doi.org/10.1155/2021/8274936
spellingShingle Salam Salloum-Asfar
Rudolf Engelke
Hanaa Mousa
Neha Goswami
I. Richard Thompson
Freshteh Palangi
Kamal Kamal
Muna N. Al-Noubi
Frank Schmidt
Sara A. Abdulla
Mohamed M. Emara
Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells
Stem Cells International
title Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells
title_full Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells
title_fullStr Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells
title_full_unstemmed Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells
title_short Hyperosmotic Stress Induces a Specific Pattern for Stress Granule Formation in Human-Induced Pluripotent Stem Cells
title_sort hyperosmotic stress induces a specific pattern for stress granule formation in human induced pluripotent stem cells
url http://dx.doi.org/10.1155/2021/8274936
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