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Focal adhesions are large protein complexes organized at the basal surface of cells, which physically connect the extracellular matrix to the cytoskeleton and have long been speculated to mediate cell migration. However, whether clustering of these molecular components into focal adhesions per se is actually required for these proteins to regulate cell motility is unclear. Here, we use quantitative microscopy to characterize large families of focal adhesion and cell motility descriptors across a wide range of matrix compliance, following genetic manipulations of focal adhesion proteins. This analysis revealed a tight, biphasic relationship between mean size of focal adhesions-not their number, surface density, or shape-and cell speed. The predictive power of this relationship was comprehensively validated by disrupting non-focal adhesion proteins and subcellular organelles (mitochondria, etc.) not known to affect …