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Local 3D matrix microenvironment regulates cell migration through spatiotemporal dynamics of contractility-dependent adhesions

Author

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  • Andrew D. Doyle

    (Laboratory of Cell and Developmental Biology, Cell Biology Section, National Institute of Dental and Craniofacial Research, National Institutes of Health)

  • Nicole Carvajal

    (Laboratory of Cellular Imaging and Macromolecular Biophysics, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health)

  • Albert Jin

    (Laboratory of Cellular Imaging and Macromolecular Biophysics, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health)

  • Kazue Matsumoto

    (Laboratory of Cell and Developmental Biology, Cell Biology Section, National Institute of Dental and Craniofacial Research, National Institutes of Health)

  • Kenneth M. Yamada

    (Laboratory of Cell and Developmental Biology, Cell Biology Section, National Institute of Dental and Craniofacial Research, National Institutes of Health)

Abstract

The physical properties of two-dimensional (2D) extracellular matrices (ECMs) modulate cell adhesion dynamics and motility, but little is known about the roles of local microenvironmental differences in three-dimensional (3D) ECMs. Here we generate 3D collagen gels of varying matrix microarchitectures to characterize their regulation of 3D adhesion dynamics and cell migration. ECMs containing bundled fibrils demonstrate enhanced local adhesion-scale stiffness and increased adhesion stability through balanced ECM/adhesion coupling, whereas highly pliable reticular matrices promote adhesion retraction. 3D adhesion dynamics are locally regulated by ECM rigidity together with integrin/ECM association and myosin II contractility. Unlike 2D migration, abrogating contractility stalls 3D migration regardless of ECM pore size. We find force is not required for clustering of activated integrins on 3D native collagen fibrils. We propose that efficient 3D migration requires local balancing of contractility with ECM stiffness to stabilize adhesions, which facilitates the detachment of activated integrins from ECM fibrils.

Suggested Citation

  • Andrew D. Doyle & Nicole Carvajal & Albert Jin & Kazue Matsumoto & Kenneth M. Yamada, 2015. "Local 3D matrix microenvironment regulates cell migration through spatiotemporal dynamics of contractility-dependent adhesions," Nature Communications, Nature, vol. 6(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms9720
    DOI: 10.1038/ncomms9720
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    Cited by:

    1. Yuechuan Lin & Nichaluk Leartprapun & Justin C. Luo & Steven G. Adie, 2022. "Light-sheet photonic force optical coherence elastography for high-throughput quantitative 3D micromechanical imaging," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Richard J. Hewitt & Franz Puttur & David C. A. Gaboriau & Frédéric Fercoq & Maryline Fresquet & William J. Traves & Laura L. Yates & Simone A. Walker & Philip L. Molyneaux & Samuel V. Kemp & Andrew G., 2023. "Lung extracellular matrix modulates KRT5+ basal cell activity in pulmonary fibrosis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Eva Crosas-Molist & Vittoria Graziani & Oscar Maiques & Pahini Pandya & Joanne Monger & Remi Samain & Samantha L. George & Saba Malik & Jerrine Salise & Valle Morales & Adrien Le Guennec & R. Andrew A, 2023. "AMPK is a mechano-metabolic sensor linking cell adhesion and mitochondrial dynamics to Myosin-dependent cell migration," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

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