On the energy efficiency of cell migration in diverse physical environments

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 anal...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2019-11, Vol.116 (48), p.23894-23900
Main Authors: Li, Yizeng, Yao, Lingxing, Mori, Yoichiro, Sun, Sean X.
Format: Article
Language:English
Subjects:
Actin
Actins - metabolism
Actins - physiology
Cell adhesion & migration
Cell culture
Cell Membrane Permeability
Cell migration
Cell Movement
Cell Shape
Cytosol
Embryogenesis
Embryonic growth stage
Energy conservation
Energy efficiency
Energy Metabolism
Energy requirements
Hydraulics
Metastases
Models, Biological
Morphogenesis
Physical Sciences
Polymerization
Substrates
Water - metabolism
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Summary: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.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1907625116