A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]

<p dir="ltr">Mesenchymal stem/stromal cells (MSCs) are self-renewing multipotent cells with regenerative, secretory and immunomodulatory capabilities that are beneficial for the treatment of various diseases. To avoid the issues that come with using tissue-derived MSCs in therapy, MS...

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Main Author: Anja M. Billing (1297773) (author)
Other Authors: Shaima S. Dib (1297767) (author), Aditya M. Bhagwat (14152806) (author), Israel T. da Silva (12274334) (author), Rodrigo D. Drummond (17430056) (author), Shahina Hayat (8774135) (author), Rasha Al-Mismar (1297782) (author), Hisham Ben-Hamidane (18808291) (author), Neha Goswami (9500432) (author), Kasper Engholm-Keller (1297761) (author), Martin R. Larsen (375762) (author), Karsten Suhre (67967) (author), Arash Rafii (102768) (author), Johannes Graumann (1297758) (author)
Published: 2019
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author Anja M. Billing (1297773)
author2 Shaima S. Dib (1297767)
Aditya M. Bhagwat (14152806)
Israel T. da Silva (12274334)
Rodrigo D. Drummond (17430056)
Shahina Hayat (8774135)
Rasha Al-Mismar (1297782)
Hisham Ben-Hamidane (18808291)
Neha Goswami (9500432)
Kasper Engholm-Keller (1297761)
Martin R. Larsen (375762)
Karsten Suhre (67967)
Arash Rafii (102768)
Johannes Graumann (1297758)
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author_facet Anja M. Billing (1297773)
Shaima S. Dib (1297767)
Aditya M. Bhagwat (14152806)
Israel T. da Silva (12274334)
Rodrigo D. Drummond (17430056)
Shahina Hayat (8774135)
Rasha Al-Mismar (1297782)
Hisham Ben-Hamidane (18808291)
Neha Goswami (9500432)
Kasper Engholm-Keller (1297761)
Martin R. Larsen (375762)
Karsten Suhre (67967)
Arash Rafii (102768)
Johannes Graumann (1297758)
author_role author
dc.creator.none.fl_str_mv Anja M. Billing (1297773)
Shaima S. Dib (1297767)
Aditya M. Bhagwat (14152806)
Israel T. da Silva (12274334)
Rodrigo D. Drummond (17430056)
Shahina Hayat (8774135)
Rasha Al-Mismar (1297782)
Hisham Ben-Hamidane (18808291)
Neha Goswami (9500432)
Kasper Engholm-Keller (1297761)
Martin R. Larsen (375762)
Karsten Suhre (67967)
Arash Rafii (102768)
Johannes Graumann (1297758)
dc.date.none.fl_str_mv 2019-10-19T06:00:00Z
dc.identifier.none.fl_str_mv 10.1074/mcp.ra119.001356
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/A_Systems-level_Characterization_of_the_Differentiation_of_Human_Embryonic_Stem_Cells_into_Mesenchymal_Stem_Cells_S_/26019478
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Medical biochemistry and metabolomics
Medical biotechnology
Mesenchymal stem/stromal cells
Embryonic stem cells
Cell-based therapy
Stem cell biology
Noncoding RNAs
dc.title.none.fl_str_mv A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr">Mesenchymal stem/stromal cells (MSCs) are self-renewing multipotent cells with regenerative, secretory and immunomodulatory capabilities that are beneficial for the treatment of various diseases. To avoid the issues that come with using tissue-derived MSCs in therapy, MSCs may be generated by the differentiation of human embryonic stems cells (hESCs) in culture. However, the changes that occur during the differentiation process have not been comprehensively characterized. Here, we combined transcriptome, proteome and phosphoproteome profiling to perform an in-depth, multi-omics study of the hESCs-to-MSCs differentiation process. Based on RNA-to-protein correlation, we determined a set of high confidence genes that are important to differentiation. Among the earliest and strongest induced proteins with extensive differential phosphorylation was AHNAK, which we hypothesized to be a defining factor in MSC biology. We observed two distinct expression waves of developmental HOX genes and an AGO2-to-AGO3 switch in gene silencing. Exploring the kinetic of noncoding ORFs during differentiation, we mapped new functions to well annotated long noncoding RNAs (CARMN, MALAT, NEAT1, LINC00152) as well as new candidates which we identified to be important to the differentiation process. Phosphoproteome analysis revealed ESC and MSC-specific phosphorylation motifs with PAK2 and RAF1 as top predicted upstream kinases in MSCs. Our data represent a rich systems-level resource on ESC-to-MSC differentiation that will be useful for the study of stem cell biology.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular & Cellular Proteomics<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1074/mcp.ra119.001356" target="_blank">https://dx.doi.org/10.1074/mcp.ra119.001356</a></p>
eu_rights_str_mv openAccess
id Manara2_328e45160cc3e02559625c3fbfcee3d1
identifier_str_mv 10.1074/mcp.ra119.001356
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/26019478
publishDate 2019
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spelling A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]Anja M. Billing (1297773)Shaima S. Dib (1297767)Aditya M. Bhagwat (14152806)Israel T. da Silva (12274334)Rodrigo D. Drummond (17430056)Shahina Hayat (8774135)Rasha Al-Mismar (1297782)Hisham Ben-Hamidane (18808291)Neha Goswami (9500432)Kasper Engholm-Keller (1297761)Martin R. Larsen (375762)Karsten Suhre (67967)Arash Rafii (102768)Johannes Graumann (1297758)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesMedical biochemistry and metabolomicsMedical biotechnologyMesenchymal stem/stromal cellsEmbryonic stem cellsCell-based therapyStem cell biologyNoncoding RNAs<p dir="ltr">Mesenchymal stem/stromal cells (MSCs) are self-renewing multipotent cells with regenerative, secretory and immunomodulatory capabilities that are beneficial for the treatment of various diseases. To avoid the issues that come with using tissue-derived MSCs in therapy, MSCs may be generated by the differentiation of human embryonic stems cells (hESCs) in culture. However, the changes that occur during the differentiation process have not been comprehensively characterized. Here, we combined transcriptome, proteome and phosphoproteome profiling to perform an in-depth, multi-omics study of the hESCs-to-MSCs differentiation process. Based on RNA-to-protein correlation, we determined a set of high confidence genes that are important to differentiation. Among the earliest and strongest induced proteins with extensive differential phosphorylation was AHNAK, which we hypothesized to be a defining factor in MSC biology. We observed two distinct expression waves of developmental HOX genes and an AGO2-to-AGO3 switch in gene silencing. Exploring the kinetic of noncoding ORFs during differentiation, we mapped new functions to well annotated long noncoding RNAs (CARMN, MALAT, NEAT1, LINC00152) as well as new candidates which we identified to be important to the differentiation process. Phosphoproteome analysis revealed ESC and MSC-specific phosphorylation motifs with PAK2 and RAF1 as top predicted upstream kinases in MSCs. Our data represent a rich systems-level resource on ESC-to-MSC differentiation that will be useful for the study of stem cell biology.</p><h2>Other Information</h2><p dir="ltr">Published in: Molecular & Cellular Proteomics<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1074/mcp.ra119.001356" target="_blank">https://dx.doi.org/10.1074/mcp.ra119.001356</a></p>2019-10-19T06:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1074/mcp.ra119.001356https://figshare.com/articles/journal_contribution/A_Systems-level_Characterization_of_the_Differentiation_of_Human_Embryonic_Stem_Cells_into_Mesenchymal_Stem_Cells_S_/26019478CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/260194782019-10-19T06:00:00Z
spellingShingle A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
Anja M. Billing (1297773)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Medical biochemistry and metabolomics
Medical biotechnology
Mesenchymal stem/stromal cells
Embryonic stem cells
Cell-based therapy
Stem cell biology
Noncoding RNAs
status_str publishedVersion
title A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
title_full A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
title_fullStr A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
title_full_unstemmed A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
title_short A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
title_sort A Systems-level Characterization of the Differentiation of Human Embryonic Stem Cells into Mesenchymal Stem Cells*[S]
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Medical biochemistry and metabolomics
Medical biotechnology
Mesenchymal stem/stromal cells
Embryonic stem cells
Cell-based therapy
Stem cell biology
Noncoding RNAs