Nuclear plasticity increases susceptibility to damage during confined migration

PLoS Comput Biol. 2020 Oct 9;16(10):e1008300. doi: 10.1371/journal.pcbi.1008300. eCollection 2020 Oct.

Abstract

Large nuclear deformations during migration through confined spaces have been associated with nuclear membrane rupture and DNA damage. However, the stresses associated with nuclear damage remain unclear. Here, using a quasi-static plane strain finite element model, we map evolution of nuclear shape and stresses during confined migration of a cell through a deformable matrix. Plastic deformation of the nucleus observed for a cell with stiff nucleus transiting through a stiffer matrix lowered nuclear stresses, but also led to kinking of the nuclear membrane. In line with model predictions, transwell migration experiments with fibrosarcoma cells showed that while nuclear softening increased invasiveness, nuclear stiffening led to plastic deformation and higher levels of DNA damage. In addition to highlighting the advantage of nuclear softening during confined migration, our results suggest that plastic deformations of the nucleus during transit through stiff tissues may lead to bending-induced nuclear membrane disruption and subsequent DNA damage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • Cell Movement / physiology*
  • Cell Nucleus / physiology*
  • DNA Damage
  • Finite Element Analysis
  • Humans
  • Models, Biological*
  • Nuclear Envelope / physiology

Grants and funding

SS acknowledges funding support from Science and Engineering Research Board (SERB), Dept. of Science & Technology, Govt. of India (Grant # EMR/2016/005454). AM was supported by fellowship from IITB-Monash Research Academy. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.