Cells in Slow Motion: Apparent Undercooling Increases Glassy Behavior at Physiological Temperatures

Adv Mater. 2021 Jul;33(29):e2101840. doi: 10.1002/adma.202101840. Epub 2021 Jun 3.

Abstract

Solvent conditions are unexpectedly sufficient to drastically and reversibly slow down cells. In vitro on the molecular level, protein-solvent interactions drastically change in the presence of heavy water (D2 O) and its stronger hydrogen bonds. Adding D2 O to the cell medium of living cells increases the molecular intracellular viscosity. While cell morphology and phenotype remain unchanged, cellular dynamics transform into slow motion in a changeable manner. This is exemplified in the slowdown of cell proliferation and migration, which is caused by a reversible gelation of the cytoplasm. In analogy to the time-temperature superposition principle, where temperature is replaced by D2 O, an increase in viscosity slows down the effective time. Actin networks, crucial structures in the cytoplasm, switch from a power-law-like viscoelastic to a more rubber-like elastic behavior. The resulting intracellular resistance and dissipation impair cell movement. Since cells are highly adaptive non-equilibrium systems, they usually respond irreversibly from a thermodynamic perspective. D2 O induced changes, however, are fully reversible and their effects are independent of signaling as well as expression. The stronger hydrogen bonds lead to glass-like, drawn-out intramolecular dynamics, which may facilitate longer storage times of biological matter, for instance, during transport of organ transplants.

Keywords: actin; cell mechanics; cell motility; glassy dynamics; heavy water; time-temperature superposition.

MeSH terms

  • Hydrogen Bonding
  • Solvents
  • Temperature*
  • Thermodynamics
  • Viscosity

Substances

  • Solvents