Effect of cell migration on the maintenance of tension on a collagen matrix.

Although it is known that cells promote structural reorganization of the collagen architecture, how individual cells exert mechanical tension on the matrix is not clearly understood. In the present study we have investigated the mechanical interaction of individual corneal fibroblasts with a collagen matrix using an improved version of our previously described in vitro force-measurement system (Roy, P. et al. Exp. Cell Res. 232:106-117, 1997). The elastic distortion of the collagen matrix exerted by cells was temporally recorded and analyzed using a two-dimensional finite-element model to quantify the forces exerted on the matrix. Time-lapse videomicroscopy of serum-cultured cells on the matrix for up to 6 h revealed that individual fibroblasts generated measurable tension on the matrix during pseudopodial extension and slow retraction. Fast retraction, an event observed during active cell migration, was associated with dramatic release of tension on the matrix. An apparent inverse correlation was observed between cell translocation and maintenance of matrix tension. Additional experiments with cells under serum-free conditions revealed that these cells fail to generate any detectable tension on the matrix despite undergoing filopodial extension and retraction. Since serum-free cells do not form focal adhesions or stress fibers, these experimental data suggest that contractility of nonmotile cells, coupled with strong cell-matrix adhesion, is the most favorable mechanism of generating and maintaining tension on the extracellular matrix.