Measuring nucleus mechanics within a living multicellular organism: Physical decoupling and attenuated recovery rate are physiological protective mechanisms of the cell nucleus under high mechanical load

Noam Zuela-Sopilniak, Daniel Bar-Sela, Chayki Charar, Oren Wintner, Yosef Gruenbaum*, Amnon Buxboim*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

Abstract

Nuclei within cells are constantly subjected to compressive, tensile, and shear forces, which regulate nucleoskeletal and cytoskeletal remodeling, activate signaling pathways, and direct cell-fate decisions. Multiple rheological methods have been adapted for characterizing the response to applied forces of isolated nuclei and nuclei within intact cells. However, in vitro measurements fail to capture the viscoelastic modulation of nuclear stressstrain relationships by the physiological tethering to the surrounding cytoskeleton, extracellular matrix and cells, and tissue-level architectures. Using an equiaxial stretching apparatus, we applied a step stress and measured nucleus deformation dynamics within living Caenorhabditis elegans nematodes. Nuclei deformed nonmonotonically under constant load. Nonmonotonic deformation was conserved across tissues and robust to nucleoskeletal and cytoskeletal perturbations, but it required intact linker of nucleoskeleton and cytoskeleton complex attachments. The transition from creep to strain recovery fits a tensile-compressive linear viscoelastic model that is indicative of nucleoskeletal-cytoskeletal decoupling under high load. Ce-lamin (lmn-1) knockdown softened the nucleus, whereas nematode aging stiffened the nucleus and decreased deformation recovery rate. Recovery lasted minutes rather than seconds due to physiological damping of the released mechanical energy, thus protecting nuclear integrity and preventing chromatin damage.

Original languageAmerican English
Pages (from-to)1943-1950
Number of pages8
JournalMolecular Biology of the Cell
Volume31
Issue number17
DOIs
StatePublished - 1 Aug 2020

Bibliographical note

Publisher Copyright:
© 2020 Zuela-Sopilniak et al.

Fingerprint

Dive into the research topics of 'Measuring nucleus mechanics within a living multicellular organism: Physical decoupling and attenuated recovery rate are physiological protective mechanisms of the cell nucleus under high mechanical load'. Together they form a unique fingerprint.

Cite this