Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells
The self-renewal and lineage-specific differentiation of stem cells are regulated by interactions with their microenvironments, called stem cell niche. Stem cells receive both biochemical and biophysical cues from their niche, which leads to the activation of signaling pathways, resulting in the mod...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Physics |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fphy.2022.1052106/full |
| _version_ | 1811178374686572544 |
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| author | Esther Kimmle Zahra Hajian Foroushani Stephan Keppler Judith Thoma Kentaro Hayashi Akihisa Yamamoto Martin Bastmeyer Martin Bastmeyer Martin Bastmeyer Motomu Tanaka Motomu Tanaka |
| author_facet | Esther Kimmle Zahra Hajian Foroushani Stephan Keppler Judith Thoma Kentaro Hayashi Akihisa Yamamoto Martin Bastmeyer Martin Bastmeyer Martin Bastmeyer Motomu Tanaka Motomu Tanaka |
| author_sort | Esther Kimmle |
| collection | DOAJ |
| description | The self-renewal and lineage-specific differentiation of stem cells are regulated by interactions with their microenvironments, called stem cell niche. Stem cells receive both biochemical and biophysical cues from their niche, which leads to the activation of signaling pathways, resulting in the modulation of gene expressions to guide their fate. Most of previous studies are focused on the effect of substrate stiffness using hydrogels with different Young’s moduli, and information is lacking on the effect of the discreteness of cell–substrate contacts on stem cells. Using mouse pluripotent, embryonic stem cells (mESCs) as the model system for early development, we quantitatively investigated the migration, dynamic deformation, and adhesion of mESCs on sparse and dense gelatin nanofibers deposited on glass surfaces, with a continuous layer of gelatin coated on glass substrates as the control. After confirming the maintenance of pluripotency on all the surfaces throughout the experiments, the centroid trajectories were monitored using timelapse imaging. The mean square displacement analysis indicated that both the diffusion coefficient and exponent were largest on sparse nanofibers, while the diffusion coefficient of mESCs on dense nanofibers was comparable to that on the control. Moreover, power spectral analysis of the shape deformation in the Fourier mode indicated that mESCs predominantly underwent elliptic deformation (mode 2), with the largest energy dissipation on sparse nanofibers. These data suggest that mESCs can deform and move on sparse nanofibers owing to the discrete cell–surface contact points. Intriguingly, using a self-developed technique based on laser-induced shock waves, a distinctly larger critical pressure was required to detach cells from nanofibers than from continuous gelatin. This finding suggests that the continuous but weak cell-substrate contacts suppress the deformation-driven mESC migration. As one of the key biological functions of stem cells, the proliferation rate of mESCs on these surfaces was determined. Although the observed difference was not statistically significant, the highest proliferation rate was observed on nanofibers, suggesting that the discreteness of cell–surface contacts can be used to regulate not only spatio-temporal dynamics but also the biological function of pluripotent stem cells. |
| first_indexed | 2024-04-11T06:17:08Z |
| format | Article |
| id | doaj.art-264d673bd634417da567ae66347cfd7e |
| institution | Directory Open Access Journal |
| issn | 2296-424X |
| language | English |
| last_indexed | 2024-04-11T06:17:08Z |
| publishDate | 2022-12-01 |
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| series | Frontiers in Physics |
| spelling | doaj.art-264d673bd634417da567ae66347cfd7e2022-12-22T04:41:01ZengFrontiers Media S.A.Frontiers in Physics2296-424X2022-12-011010.3389/fphy.2022.10521061052106Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cellsEsther Kimmle0Zahra Hajian Foroushani1Stephan Keppler2Judith Thoma3Kentaro Hayashi4Akihisa Yamamoto5Martin Bastmeyer6Martin Bastmeyer7Martin Bastmeyer8Motomu Tanaka9Motomu Tanaka10Physical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, Heidelberg, GermanyPhysical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, Heidelberg, GermanyZoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, GermanyPhysical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, Heidelberg, GermanyCenter for Integrative Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto, JapanCenter for Integrative Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto, JapanZoological Institute, Cell- and Neurobiology, Karlsruhe Institute of Technology, Karlsruhe, GermanyCenter for Integrative Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto, JapanInstitute for Biological and Chemical Systems - Biological Information Processing (IBCS-BIP), Karlsruhe Institute of Technology, Eggenstein-Leopoldshafen, GermanyPhysical Chemistry of Biosystems, Institute of Physical Chemistry, Heidelberg University, Heidelberg, GermanyCenter for Integrative Medicine and Physics, Institute for Advanced Study, Kyoto University, Kyoto, JapanThe self-renewal and lineage-specific differentiation of stem cells are regulated by interactions with their microenvironments, called stem cell niche. Stem cells receive both biochemical and biophysical cues from their niche, which leads to the activation of signaling pathways, resulting in the modulation of gene expressions to guide their fate. Most of previous studies are focused on the effect of substrate stiffness using hydrogels with different Young’s moduli, and information is lacking on the effect of the discreteness of cell–substrate contacts on stem cells. Using mouse pluripotent, embryonic stem cells (mESCs) as the model system for early development, we quantitatively investigated the migration, dynamic deformation, and adhesion of mESCs on sparse and dense gelatin nanofibers deposited on glass surfaces, with a continuous layer of gelatin coated on glass substrates as the control. After confirming the maintenance of pluripotency on all the surfaces throughout the experiments, the centroid trajectories were monitored using timelapse imaging. The mean square displacement analysis indicated that both the diffusion coefficient and exponent were largest on sparse nanofibers, while the diffusion coefficient of mESCs on dense nanofibers was comparable to that on the control. Moreover, power spectral analysis of the shape deformation in the Fourier mode indicated that mESCs predominantly underwent elliptic deformation (mode 2), with the largest energy dissipation on sparse nanofibers. These data suggest that mESCs can deform and move on sparse nanofibers owing to the discrete cell–surface contact points. Intriguingly, using a self-developed technique based on laser-induced shock waves, a distinctly larger critical pressure was required to detach cells from nanofibers than from continuous gelatin. This finding suggests that the continuous but weak cell-substrate contacts suppress the deformation-driven mESC migration. As one of the key biological functions of stem cells, the proliferation rate of mESCs on these surfaces was determined. Although the observed difference was not statistically significant, the highest proliferation rate was observed on nanofibers, suggesting that the discreteness of cell–surface contacts can be used to regulate not only spatio-temporal dynamics but also the biological function of pluripotent stem cells.https://www.frontiersin.org/articles/10.3389/fphy.2022.1052106/fullmouse embryonic stem cellnanofibercell migrationactive deformationadhesion |
| spellingShingle | Esther Kimmle Zahra Hajian Foroushani Stephan Keppler Judith Thoma Kentaro Hayashi Akihisa Yamamoto Martin Bastmeyer Martin Bastmeyer Martin Bastmeyer Motomu Tanaka Motomu Tanaka Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells Frontiers in Physics mouse embryonic stem cell nanofiber cell migration active deformation adhesion |
| title | Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells |
| title_full | Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells |
| title_fullStr | Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells |
| title_full_unstemmed | Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells |
| title_short | Discreteness of cell–surface contacts affects spatio-temporal dynamics, adhesion, and proliferation of mouse embryonic stem cells |
| title_sort | discreteness of cell surface contacts affects spatio temporal dynamics adhesion and proliferation of mouse embryonic stem cells |
| topic | mouse embryonic stem cell nanofiber cell migration active deformation adhesion |
| url | https://www.frontiersin.org/articles/10.3389/fphy.2022.1052106/full |
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