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Probing cytoskeletal pre-stress and nuclear mechanics in endothelial cells with spatiotemporally controlled (de-)adhesion kinetics on micropatterned substrates

Marie Versaevel, Maryam Riaz, Tobias Corne UGent, Thomas Grevesse, Joséphine Lantoine, Danahe Mohammed, Céline Bruyère, Laura Alaimo, Winnok De Vos UGent and Sylvain Gabriele (2017) CELL ADHESION & MIGRATION. 11(1). p.98-109
abstract
The mechanical properties of living cells reflect their propensity to migrate and respond to external forces. Both cellular and nuclear stiffnesses are strongly influenced by the rigidity of the extracellular matrix (ECM) through reorganization of the cyto- and nucleoskeletal protein connections. Changes in this architectural continuum affect cell mechanics and underlie many pathological conditions. In this context, an accurate and combined quantification of the mechanical properties of both cells and nuclei can contribute to a better understanding of cellular (dys-) function. To address this challenge, we have established a robust method for probing cellular and nuclear deformation during spreading and detachment from micropatterned substrates. We show that (de-)adhesion kinetics of endothelial cells are modulated by substrate stiffness and rely on the actomyosin network. We combined this approach with measurements of cell stiffness by magnetic tweezers to show that relaxation dynamics can be considered as a reliable parameter of cellular pre- stress in adherent cells. During the adhesion stage, large cellular and nuclear deformations occur over a long time span (>60 min). Conversely, nuclear deformation and condensed chromatin are relaxed in a few seconds after detachment. Finally, our results show that accumulation of farnesylated prelamin leads to modifications of the nuclear viscoelastic properties, as reflected by increased nuclear relaxation times. Our method offers an original and non-intrusive way of simultaneously gauging cellular and nuclear mechanics, which can be extended to high-throughput screens of pathological conditions and potential countermeasures.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
cytoskeleton, (de-)adhesion, matrix rigidity, nucleus, pre-stress, STIFFNESS, REVEALS, RHO, ELASTICITY, INHIBITORS, DYNAMICS, LAMINA, KINASE
journal title
CELL ADHESION & MIGRATION
Cell Adhes. Migr.
volume
11
issue
1
pages
98 - 109
Web of Science type
Article
Web of Science id
000395144300008
ISSN
1933-6918
DOI
10.1080/19336918.2016.1182290
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
8040710
handle
http://hdl.handle.net/1854/LU-8040710
date created
2016-07-28 09:47:49
date last changed
2017-08-01 11:50:14
@article{8040710,
  abstract     = {The mechanical properties of living cells reflect their propensity to migrate and respond to external forces. Both cellular and nuclear stiffnesses are strongly influenced by the rigidity of the extracellular matrix (ECM) through reorganization of the cyto- and nucleoskeletal protein connections. Changes in this architectural continuum affect cell mechanics and underlie many pathological conditions. In this context, an accurate and combined quantification of the mechanical properties of both cells and nuclei can contribute to a better understanding of cellular (dys-) function. To address this challenge, we have established a robust method for probing cellular and nuclear deformation during spreading and detachment from micropatterned substrates. We show that (de-)adhesion kinetics of endothelial cells are modulated by substrate stiffness and rely on the actomyosin network. We combined this approach with measurements of cell stiffness by magnetic tweezers to show that relaxation dynamics can be considered as a reliable parameter of cellular pre- stress in adherent cells. During the adhesion stage, large cellular and nuclear deformations occur over a long time span ({\textrangle}60 min). Conversely, nuclear deformation and condensed chromatin are relaxed in a few seconds after detachment. Finally, our results show that accumulation of farnesylated prelamin leads to modifications of the nuclear viscoelastic properties, as reflected by increased nuclear relaxation times. Our method offers an original and non-intrusive way of simultaneously gauging cellular and nuclear mechanics, which can be extended to high-throughput screens of pathological conditions and potential countermeasures.},
  author       = {Versaevel, Marie and Riaz, Maryam and Corne, Tobias and Grevesse, Thomas and Lantoine, Jos{\'e}phine and Mohammed, Danahe and Bruy{\`e}re, C{\'e}line and Alaimo, Laura and De Vos, Winnok and Gabriele, Sylvain},
  issn         = {1933-6918},
  journal      = {CELL ADHESION \& MIGRATION},
  keyword      = {cytoskeleton,(de-)adhesion,matrix rigidity,nucleus,pre-stress,STIFFNESS,REVEALS,RHO,ELASTICITY,INHIBITORS,DYNAMICS,LAMINA,KINASE},
  language     = {eng},
  number       = {1},
  pages        = {98--109},
  title        = {Probing cytoskeletal pre-stress and nuclear mechanics in endothelial cells with spatiotemporally controlled (de-)adhesion kinetics on micropatterned substrates},
  url          = {http://dx.doi.org/10.1080/19336918.2016.1182290},
  volume       = {11},
  year         = {2017},
}

Chicago
Versaevel, Marie, Maryam Riaz, Tobias Corne, Thomas Grevesse, Joséphine Lantoine, Danahe Mohammed, Céline Bruyère, Laura Alaimo, Winnok De Vos, and Sylvain Gabriele. 2017. “Probing Cytoskeletal Pre-stress and Nuclear Mechanics in Endothelial Cells with Spatiotemporally Controlled (de-)adhesion Kinetics on Micropatterned Substrates.” Cell Adhesion & Migration 11 (1): 98–109.
APA
Versaevel, M., Riaz, M., Corne, T., Grevesse, T., Lantoine, J., Mohammed, D., Bruyère, C., et al. (2017). Probing cytoskeletal pre-stress and nuclear mechanics in endothelial cells with spatiotemporally controlled (de-)adhesion kinetics on micropatterned substrates. CELL ADHESION & MIGRATION, 11(1), 98–109.
Vancouver
1.
Versaevel M, Riaz M, Corne T, Grevesse T, Lantoine J, Mohammed D, et al. Probing cytoskeletal pre-stress and nuclear mechanics in endothelial cells with spatiotemporally controlled (de-)adhesion kinetics on micropatterned substrates. CELL ADHESION & MIGRATION. 2017;11(1):98–109.
MLA
Versaevel, Marie, Maryam Riaz, Tobias Corne, et al. “Probing Cytoskeletal Pre-stress and Nuclear Mechanics in Endothelial Cells with Spatiotemporally Controlled (de-)adhesion Kinetics on Micropatterned Substrates.” CELL ADHESION & MIGRATION 11.1 (2017): 98–109. Print.