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Transient mechanical interactions between cells and viscoelastic extracellular matrix.

Brandon Slater1, Jing Li1, Dhiraj Indana2

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Cellular forces remodel the extracellular matrix (ECM). This study reveals how the viscoelasticity of the ECM, influenced by fiber and cross-linker properties, dictates stress dynamics and matrix remodeling during cell migration and wound healing.

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Area of Science:

  • Biophysics
  • Cell Biology
  • Biomaterials Science

Background:

  • Cells mechanically interact with the extracellular matrix (ECM) during physiological processes like wound healing and migration.
  • Cell-generated contractile forces remodel the ECM, but the time-dependent viscoelastic nature of ECMs complicates understanding this process.
  • Existing models often overlook the viscoelastic properties of ECMs, leaving a gap in understanding cell-matrix interactions.

Purpose of the Study:

  • To investigate how the viscoelasticity of the ECM influences matrix remodeling and stress profiles.
  • To explore the role of transient cross-linkers in capturing ECM viscoelasticity.
  • To quantify the time evolution of stress generation, propagation, and relaxation induced by cellular contraction within the ECM.

Main Methods:

  • Employed a discrete modeling approach to simulate cell-ECM interactions.
  • Incorporated explicit transient cross-linkers with varying density and unbinding kinetics to represent ECM viscoelasticity.
  • Quantified mechanical stress and matrix remodeling metrics like fiber displacement and local deformation.
  • Validated simulation findings with in vitro experiments using fibroblasts in a 3D collagen matrix.

Main Results:

  • Matrix connectivity, determined by fiber and cross-linker density, significantly impacts stress magnitude and propagation.
  • Cross-linker unbinding dynamics (rate and force sensitivity) critically regulate stress profiles and ECM remodeling.
  • The model successfully captured the time-dependent evolution of stress and deformation in a viscoelastic ECM.
  • Simulation results were consistent with experimental observations of cell-induced matrix remodeling.

Conclusions:

  • Viscoelasticity plays a crucial role in cell-mediated ECM remodeling.
  • The discrete model with transient cross-linkers provides a robust framework for studying cell-ECM mechanical interactions.
  • Findings offer key insights into the dynamics of cell-ECM mechanical communication in physiological contexts.