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Extracellular fluid viscosity regulates human mesenchymal stem cell lineage and function.

Alice Amitrano1,2, Qinling Yuan1,2, Bhawana Agarwal1,2

  • 1Department of Chemical and Biomolecular Engineering, Johns Hopkins University, Baltimore, MD 21218, USA.

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Extracellular fluid viscosity significantly influences human mesenchymal stem cell (hMSC) differentiation. Elevated viscosity promotes osteogenic differentiation and an immunosuppressive M2 macrophage phenotype, acting as a key physical cue.

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Area of Science:

  • Biomaterials Science
  • Cell Biology
  • Mechanobiology

Background:

  • Human mesenchymal stem cells (hMSCs) are known to respond to substrate mechanical properties like stiffness and viscoelasticity.
  • The impact of extracellular fluid viscosity on hMSC behavior, particularly in conjunction with substrate properties, remains largely unexplored.

Purpose of the Study:

  • To investigate the role of extracellular fluid viscosity as a physical cue influencing hMSC function.
  • To determine how fluid viscosity affects hMSC differentiation and phenotype on substrates with varying stiffness and viscoelasticity.

Main Methods:

  • Utilized varying substrate stiffness and viscoelasticity with controlled extracellular fluid viscosity.
  • Analyzed hMSC differentiation pathways, including actin remodeling, membrane tension, ion channel activity, and key protein translocations.
  • Assessed macrophage phenotype polarization in response to hMSC behavior under different viscosity conditions.

Main Results:

  • Elevated fluid viscosity biased hMSCs toward an osteogenic phenotype, independent of substrate properties.
  • Increased viscosity induced Arp2/3-dependent actin remodeling, enhanced NHE1 activity, and promoted hMSC spreading.
  • Fluid viscosity modulated membrane tension, activating TRPV4 channels, calcium influx, and the RhoA/ROCK/YAP pathway, leading to RUNX2 nuclear translocation.
  • hMSCs cultured in elevated viscosity on soft gels favored an M2 macrophage phenotype.

Conclusions:

  • Extracellular fluid viscosity is a critical physical cue that dictates hMSC differentiation, imparting an osteogenic memory.
  • Elevated viscosity promotes osteogenesis and induces an immunosuppressive M2 macrophage phenotype, highlighting its potential in regenerative medicine and tissue engineering.