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

Author

Listed:
  • Matthew R. Zanotelli

    (Cornell University
    Vanderbilt University)

  • Aniqua Rahman-Zaman

    (Cornell University
    Vanderbilt University)

  • Jacob A. VanderBurgh

    (Cornell University
    Vanderbilt University)

  • Paul V. Taufalele

    (Vanderbilt University)

  • Aadhar Jain

    (Cornell University)

  • David Erickson

    (Cornell University)

  • Francois Bordeleau

    (Vanderbilt University
    Université Laval Cancer Research Center and Faculty of Medicine, Université Laval)

  • Cynthia A. Reinhart-King

    (Cornell University
    Vanderbilt University)

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.

Suggested Citation

  • Matthew R. Zanotelli & Aniqua Rahman-Zaman & Jacob A. VanderBurgh & Paul V. Taufalele & Aadhar Jain & David Erickson & Francois Bordeleau & Cynthia A. Reinhart-King, 2019. "Energetic costs regulated by cell mechanics and confinement are predictive of migration path during decision-making," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12155-z
    DOI: 10.1038/s41467-019-12155-z
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