Energetic costs regulated by cell mechanics and confinement are predictive of migration path during decision-making

Matthew R. Zanotelli, Aniqua Rahman-Zaman, Jacob A. VanderBurgh, Paul V. Taufalele, Aadhar Jain, David Erickson, Francois Bordeleau () and Cynthia A. Reinhart-King ()
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Matthew R. Zanotelli: Cornell University
Aniqua Rahman-Zaman: Cornell University
Jacob A. VanderBurgh: Cornell University
Paul V. Taufalele: Vanderbilt University
Aadhar Jain: Cornell University
David Erickson: Cornell University
Francois Bordeleau: Vanderbilt University
Cynthia A. Reinhart-King: Cornell University

Nature Communications, 2019, vol. 10, issue 1, 1-12

Abstract: Abstract Cell migration during the invasion-metastasis cascade requires cancer cells to navigate a spatially complex microenvironment that presents directional choices to migrating cells. Here, we investigate cellular energetics during migration decision-making in confined spaces. Theoretical and experimental data show that energetic costs for migration through confined spaces are mediated by a balance between cell and matrix compliance as well as the degree of spatial confinement to direct decision-making. Energetic costs, driven by the cellular work needed to generate force for matrix displacement, increase with increasing cell stiffness, matrix stiffness, and degree of spatial confinement, limiting migration. By assessing energetic costs between possible migration paths, we can predict the probability of migration choice. Our findings indicate that motility in confined spaces imposes high energetic demands on migrating cells, and cells migrate in the direction of least confinement to minimize energetic costs. Therefore, therapeutically targeting metabolism may limit cancer cell migration and metastasis.

Date: 2019
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DOI: 10.1038/s41467-019-12155-z

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