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Short Report
Mechanical stability of the cell nucleus – roles played by the cytoskeleton in nuclear deformation and strain recovery
Xian Wang, Haijiao Liu, Min Zhu, Changhong Cao, Zhensong Xu, Yonit Tsatskis, Kimberly Lau, Chikin Kuok, Tobin Filleter, Helen McNeill, Craig A. Simmons, Sevan Hopyan, Yu Sun
Journal of Cell Science 2018 131: jcs209627 doi: 10.1242/jcs.209627 Published 4 July 2018
Xian Wang
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
2Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G9
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  • ORCID record for Xian Wang
Haijiao Liu
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
2Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G9
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Min Zhu
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
3Program in Developmental and Stem Cell Biology, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
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Changhong Cao
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
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Zhensong Xu
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
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Yonit Tsatskis
4Lunenfeld-Tanenbaum Research Institute, Mt. Sinai Hospital, Toronto, Ontario, Canada M5G 1X5
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Kimberly Lau
3Program in Developmental and Stem Cell Biology, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
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Chikin Kuok
4Lunenfeld-Tanenbaum Research Institute, Mt. Sinai Hospital, Toronto, Ontario, Canada M5G 1X5
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Tobin Filleter
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
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Helen McNeill
4Lunenfeld-Tanenbaum Research Institute, Mt. Sinai Hospital, Toronto, Ontario, Canada M5G 1X5
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  • For correspondence: sun@mie.utoronto.ca sevan.hopyan@sickkids.ca simmons@mie.utoronto.ca mcneill@lunenfeld.ca
Craig A. Simmons
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
2Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G9
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  • For correspondence: sun@mie.utoronto.ca sevan.hopyan@sickkids.ca simmons@mie.utoronto.ca mcneill@lunenfeld.ca
Sevan Hopyan
3Program in Developmental and Stem Cell Biology, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada M5G 1X8
5Division of Orthopaedic Surgery, Hospital for Sick Children and University of Toronto, Toronto, Ontario, Canada M5G 1X8
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  • For correspondence: sun@mie.utoronto.ca sevan.hopyan@sickkids.ca simmons@mie.utoronto.ca mcneill@lunenfeld.ca
Yu Sun
1Department of Mechanical and Industrial Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G8
2Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada M5S 3G9
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ABSTRACT

Extracellular forces transmitted through the cytoskeleton can deform the cell nucleus. Large nuclear deformations increase the risk of disrupting the integrity of the nuclear envelope and causing DNA damage. The mechanical stability of the nucleus defines its capability to maintain nuclear shape by minimizing nuclear deformation and allowing strain to be minimized when deformed. Understanding the deformation and recovery behavior of the nucleus requires characterization of nuclear viscoelastic properties. Here, we quantified the decoupled viscoelastic parameters of the cell membrane, cytoskeleton, and the nucleus. The results indicate that the cytoskeleton enhances nuclear mechanical stability by lowering the effective deformability of the nucleus while maintaining nuclear sensitivity to mechanical stimuli. Additionally, the cytoskeleton decreases the strain energy release rate of the nucleus and might thus prevent shape change-induced structural damage to chromatin.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: X.W., H.L., C.C., T.F., Y.S.; Methodology: X.W., H.L., C.C., Z.X., Y.T., H.M.; Software: X.W.; Validation: X.W., H.L., C.C., Z.X., C.K.; Formal analysis: X.W.; Investigation: X.W., H.L., M.Z.; Resources: X.W., H.L.; Data curation: X.W., M.Z., K.L.; Writing - original draft: X.W.; Writing - review & editing: H.L., T.F., H.M., C.A.S., S.H., Y.S.; Visualization: X.W., Z.X., Y.T., K.L.; Supervision: H.M., C.A.S., S.H., Y.S.; Project administration: X.W., S.H., Y.S.; Funding acquisition: H.M., Y.S.

  • Funding

    This work was supported by the Natural Sciences and Engineering Research Council of Canada via an NSERC Steacie Memorial Fellowship, the Canada Research Chairs program and the Canadian Institutes of Health Research (143319 to H.M.).

  • Data availability

    The AFM datasets, microscope images and custom-made code for data analysis are available through the link https://github.com/XianShawn/Nuclear_Mechanics. The MATLAB code is for the purpose of reproducible research and not for commercial usage. The other data that support the findings of this study are available from the corresponding author upon reasonable request.

  • Supplementary information

    Supplementary information available online at http://jcs.biologists.org/lookup/doi/10.1242/jcs.209627.supplemental

  • Received August 15, 2017.
  • Accepted May 14, 2018.
  • © 2018. Published by The Company of Biologists Ltd
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Keywords

  • Nuclear mechanics
  • Viscoelasticity
  • cytoskeleton
  • Strain recovery
  • AFM

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Short Report
Mechanical stability of the cell nucleus – roles played by the cytoskeleton in nuclear deformation and strain recovery
Xian Wang, Haijiao Liu, Min Zhu, Changhong Cao, Zhensong Xu, Yonit Tsatskis, Kimberly Lau, Chikin Kuok, Tobin Filleter, Helen McNeill, Craig A. Simmons, Sevan Hopyan, Yu Sun
Journal of Cell Science 2018 131: jcs209627 doi: 10.1242/jcs.209627 Published 4 July 2018
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Short Report
Mechanical stability of the cell nucleus – roles played by the cytoskeleton in nuclear deformation and strain recovery
Xian Wang, Haijiao Liu, Min Zhu, Changhong Cao, Zhensong Xu, Yonit Tsatskis, Kimberly Lau, Chikin Kuok, Tobin Filleter, Helen McNeill, Craig A. Simmons, Sevan Hopyan, Yu Sun
Journal of Cell Science 2018 131: jcs209627 doi: 10.1242/jcs.209627 Published 4 July 2018

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