Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?

Background: Under regular culture conditions, mesenchymal stem cells (MSCs) exhibit cytosolic calcium concentration oscillations (Ca oscillations), that change, especially in frequency, after the differentiation of the MSCs. Ca oscillations are known to encode important information in frequency and...

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Authors: Vallet, Leslie A., Sánchez-Petidier, Marina, Fernandes, Romain, Naumova, Nataliia, Merla, Caterina, Consales, Claudia, Innamorati, Giorgia, André, Franck M., Mir, Lluis M.
Format: article
Status:Published version
Publication Date:2025
Country:España
Institution:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repository:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:dnet:recercat____::6be7e7da317e124aeb17f45adda291ac
Online Access:https://hdl.handle.net/10230/73026
http://dx.doi.org/10.1186/s13287-025-04454-8
Access Level:Open access
Keyword:Cell proliferation
Electrical stimulation
Cell cycle control
Microsecond pulsed electric fields
Electroporation
Electropermeabilization
Calcium electroporation
Calcium oscillations frequency
Adipogenic differentiation
Osteogenic differentiation
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oai_identifier_str oai:dnet:recercat____::6be7e7da317e124aeb17f45adda291ac
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
title Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
spellingShingle Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
Vallet, Leslie A.
Cell proliferation
Electrical stimulation
Cell cycle control
Microsecond pulsed electric fields
Electroporation
Electropermeabilization
Calcium electroporation
Calcium oscillations frequency
Adipogenic differentiation
Osteogenic differentiation
title_short Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
title_full Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
title_fullStr Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
title_full_unstemmed Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
title_sort Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?
dc.creator.none.fl_str_mv Vallet, Leslie A.
Sánchez-Petidier, Marina
Fernandes, Romain
Naumova, Nataliia
Merla, Caterina
Consales, Claudia
Innamorati, Giorgia
André, Franck M.
Mir, Lluis M.
author Vallet, Leslie A.
author_facet Vallet, Leslie A.
Sánchez-Petidier, Marina
Fernandes, Romain
Naumova, Nataliia
Merla, Caterina
Consales, Claudia
Innamorati, Giorgia
André, Franck M.
Mir, Lluis M.
author_role author
author2 Sánchez-Petidier, Marina
Fernandes, Romain
Naumova, Nataliia
Merla, Caterina
Consales, Claudia
Innamorati, Giorgia
André, Franck M.
Mir, Lluis M.
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cell proliferation
Electrical stimulation
Cell cycle control
Microsecond pulsed electric fields
Electroporation
Electropermeabilization
Calcium electroporation
Calcium oscillations frequency
Adipogenic differentiation
Osteogenic differentiation
topic Cell proliferation
Electrical stimulation
Cell cycle control
Microsecond pulsed electric fields
Electroporation
Electropermeabilization
Calcium electroporation
Calcium oscillations frequency
Adipogenic differentiation
Osteogenic differentiation
description Background: Under regular culture conditions, mesenchymal stem cells (MSCs) exhibit cytosolic calcium concentration oscillations (Ca oscillations), that change, especially in frequency, after the differentiation of the MSCs. Ca oscillations are known to encode important information in frequency and amplitude, ultimately controlling many cellular processes such as proliferation and differentiation. Previous studies evidenced that decreasing the frequency of Ca oscillations by physical means can facilitate osteodifferentiation of MSCs. Understanding the relationships between Ca oscillations and MSCs proliferation or differentiation appears necessary in the attractive perspective of influencing cell fate by controlling Ca signaling. Methods: Using fluorescence microscopy we evaluated the evolution of Ca oscillations throughout the adipogenic and osteogenic differentiation processes. Then, using electrical stimulation with microsecond pulsed electric fields (µsPEFs), we manipulated the frequency of Ca oscillations in MSCs and measured its consequences on cell growth. Results: Although the evolution of the Ca oscillation frequencies differed between the adipogenic and osteogenic differentiation pathways in early stages of differentiation, we observed common features in the late stages: a progressive decrease in the Ca oscillations frequencies, before their complete arrest as the differentiations reached their term. It has been reported that most cells undergoing differentiation experience a concomitant commitment to terminal differentiation and cell cycle exit, and prior to this, lengthened G1 phases, where the molecular competition between mitogenic and differentiating signals occurs. A relationship between the frequency of Ca oscillations and the progression of the cell cycle, through some Ca sensitive molecular factors, could explain the evolutions of the frequencies of Ca oscillations observed during proliferation and differentiation. We hypothesized that increasing the frequency of Ca oscillations would promote proliferation, while decreasing it would promote differentiation under differentiating conditions. Using electrical stimulation with µsPEFs, we manipulated the frequency of Ca oscillations in MSCs and its increase actually promoted cell proliferation. Conclusions: Manipulating the frequency of Ca oscillations influences the cell fate of MSCs. We propose hypotheses on the actors that could link the Ca oscillation frequencies with proliferation and differentiation processes, based on data available in the literature.
publishDate 2025
dc.date.none.fl_str_mv 2025
2026
2026
2026
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/10230/73026
http://dx.doi.org/10.1186/s13287-025-04454-8
https://hdl.handle.net/10230/73026
url https://hdl.handle.net/10230/73026
http://dx.doi.org/10.1186/s13287-025-04454-8
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Stem Cell Research and Therapy. 2025 Aug 21;16(1):446
info:eu-repo/grantAgreement/EC/H2020/964562
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
dc.source.none.fl_str_mv reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Calcium oscillations in mesenchymal stem cells, a control on cell cycle progression to influence cell fate towards proliferation or differentiation?Vallet, Leslie A.Sánchez-Petidier, MarinaFernandes, RomainNaumova, NataliiaMerla, CaterinaConsales, ClaudiaInnamorati, GiorgiaAndré, Franck M.Mir, Lluis M.Cell proliferationElectrical stimulationCell cycle controlMicrosecond pulsed electric fieldsElectroporationElectropermeabilizationCalcium electroporationCalcium oscillations frequencyAdipogenic differentiationOsteogenic differentiationBackground: Under regular culture conditions, mesenchymal stem cells (MSCs) exhibit cytosolic calcium concentration oscillations (Ca oscillations), that change, especially in frequency, after the differentiation of the MSCs. Ca oscillations are known to encode important information in frequency and amplitude, ultimately controlling many cellular processes such as proliferation and differentiation. Previous studies evidenced that decreasing the frequency of Ca oscillations by physical means can facilitate osteodifferentiation of MSCs. Understanding the relationships between Ca oscillations and MSCs proliferation or differentiation appears necessary in the attractive perspective of influencing cell fate by controlling Ca signaling. Methods: Using fluorescence microscopy we evaluated the evolution of Ca oscillations throughout the adipogenic and osteogenic differentiation processes. Then, using electrical stimulation with microsecond pulsed electric fields (µsPEFs), we manipulated the frequency of Ca oscillations in MSCs and measured its consequences on cell growth. Results: Although the evolution of the Ca oscillation frequencies differed between the adipogenic and osteogenic differentiation pathways in early stages of differentiation, we observed common features in the late stages: a progressive decrease in the Ca oscillations frequencies, before their complete arrest as the differentiations reached their term. It has been reported that most cells undergoing differentiation experience a concomitant commitment to terminal differentiation and cell cycle exit, and prior to this, lengthened G1 phases, where the molecular competition between mitogenic and differentiating signals occurs. A relationship between the frequency of Ca oscillations and the progression of the cell cycle, through some Ca sensitive molecular factors, could explain the evolutions of the frequencies of Ca oscillations observed during proliferation and differentiation. We hypothesized that increasing the frequency of Ca oscillations would promote proliferation, while decreasing it would promote differentiation under differentiating conditions. Using electrical stimulation with µsPEFs, we manipulated the frequency of Ca oscillations in MSCs and its increase actually promoted cell proliferation. Conclusions: Manipulating the frequency of Ca oscillations influences the cell fate of MSCs. We propose hypotheses on the actors that could link the Ca oscillation frequencies with proliferation and differentiation processes, based on data available in the literature.This research was funded by CNRS, Gustave Roussy, Université Paris-Saclay, and by the FET-OPEN H2020, grant number 964562. Therefore, for the purpose of Open Access, a Creative Commons Attribution (CC BY) public copyright license has been applied by the authors to the present document and will be applied to all subsequent versions up to the Author Accepted Manuscript arising from this submission.Springer2026202620252026info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/10230/73026http://dx.doi.org/10.1186/s13287-025-04454-8https://hdl.handle.net/10230/73026reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésStem Cell Research and Therapy. 2025 Aug 21;16(1):446info:eu-repo/grantAgreement/EC/H2020/964562This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:dnet:recercat____::6be7e7da317e124aeb17f45adda291ac2026-05-29T05:05:01Z
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