Viscosity and elasticity during collagen assembly in vitro: relevance to matrix-driven translocation

In order to better understand the gelation process associated with collagen assembly, and the mechanism of the in vitro morphogenetic phenomenon of "matrix-driven translocation" [S.A. Newman et al. (1985) Science, 228, 885-889], the viscosity and elastic modulus of assembling collagen matrices in the presence and absence of polystyrene latex beads was investigated. Viscosity measurements at very low shear rates (0.016-0.0549 s(-1)) were performed over a range of temperatures (6.9-11.5 degrees C) in a Couette viscometer. A magnetic levitation sphere rheometer was used to measure the shear elastic modulus of the assembling matrices during the late phase of the gelation process. Gelation was detected by the rapid increase in viscosity that occurred after a lag time tL that varied between O and approximately 500 s. After a rise in viscosity that occurred over an additional approximately 500 s, the collagen matrix was characterized by an elastic modulus of the order of several Pa. The lag time of the assembly process was relatively insensitive to differences in shear rate within the variability of the sample preparation, but was inversely proportional to the time the sample spent on ice before being raised to the test temperature, for test temperatures > 9 degrees C. This suggests that structures important for fibrillogenesis are capable of forming at 0 degrees C. The time dependence of the gelation process is well-described by an exponential law with a rate constant K approximately 0.1 s(-1). Significantly, K was consistently larger in collagen preparations that contained cell-sized polystyrene beads. From these results, along with prior information on effective surface tension differences of bead-containing and bead-lacking collagen matrices, we conclude that changes in matrix organization contributing to matrix-driven translocation are initiated during the lag phase of fibrillogenesis when the viscosity is < or = 0.1 Poise. The phenomenon may make use of small differentials in viscosity and/or elasticity, resulting from the interaction of the beads with the assembling matrix. These properties are well described by standard models of concentrated solutions.