On the energy efficiency of cell migration in diverse physical environments

Significance Cell migration requires energy, but the metabolic cost of migration has not been quantitatively explored in detail. Here, we use a 2-phase model of the cell cytoplasm to compute cell velocities and energy efficiencies during cell movement. This model predicts that actin polymerization-driven migration is very inefficient in high-hydraulic-resistance environments. Instead, cells can adopt the water-driven mechanism. Therefore, the energetics and mechanical efficiencies of cell movement are predicted to depend on the physical environment.
In this work, we explore fundamental energy requirements during mammalian cell movement. Starting with the conservation of mass and momentum for the cell cytosol and the actin-network phase, we develop useful identities that compute dissipated energies during extensions of the cell boundary. We analyze 2 complementary mechanisms of cell movement: actin-driven and water-driven. The former mechanism occurs on 2-dimensional cell-culture substrate without appreciable external hydraulic resistance, while the latter mechanism is prominent in confined channels where external hydraulic resistance is high. By considering various forms of energy input and dissipation, we find that the water-driven cell-migration mechanism is inefficient and requires more energy. However, in environments with sufficiently high hydraulic resistance, the efficiency of actin-polymerization-driven cell migration decreases considerably, and the water-based mechanism becomes more efficient. Hence, the most efficient way for cells to move depends on the physical environment. This work can be extended to higher dimensions and has implication for understanding energetics of morphogenesis in early embryonic development and cancer-cell metastasis and provides a physical basis for understanding changing metabolic requirements for cell movement in different conditions.