Transition to superdiffusive behavior in intracellular actin-based transport mediated by molecular motors

Intracellular transport of large cargoes, such as organelles, vesicles, or large proteins, is a complex dynamical process that involves the interplay of adenosine triphosphate–consuming molecular motors, cytoskeleton filaments, and the viscoelastic cytoplasm. In this work we investigate the motion of pigment organelles (melanosomes) driven by myosin-V motors in Xenopus laevis melanocytes using a high-spatio-temporal resolution tracking technique. By analyzing the obtained trajectories, we show that the melanosomes mean-square displacement undergoes a transition from a subdiffusive to a superdiffusive behavior. A stochastic theoretical model, which explicitly considers the collective action of the molecular motors, is introduced to generalize the interpretation of our data. Starting from a generalized Langevin equation, we derive an analytical expression for the mean square displacement, which also takes into account the experimental noise. By fitting theoretical expressions to experimental data we were able to discriminate the exponents that characterize the passive and active contributions to the dynamics and to estimate the “global” motor forces correctly. Then, our model gives a quantitative description of active transport in living cells with a reduced number of parameters.

Figure 1

A Xenopus laevis melanophore image obtained using bright-field transmission light microscopy. Melanosomes can be clearly identify and followed with high-spatio-temporal resolution using a SPT technique.

Figure 2

A representative trajectory of a melanosome followed during 70 s with 0.07 s resolution. The cell was stimulated with 100 nM of MSH. Scale $\text{bar}=0.5\mu \text{m}$.

Figure 3

(Color online) Double-logarithmic plot of the MSD as a function of the time lag. Experimental data points for wild-type cells are symbolized by squares (aggregation) and circles (dispersion), while the data corresponding to mutant cells are symbolized by rhomboids. The symbols represent an average over all the trajectories. Inset: MSD vs time lag plot for all trajectories in wild-type cells.

Figure 4

(Color online) The logarithmic derivative of the MSD as a function of the time lag [Eq. (2)]. The experimental data for wild-type cells are symbolized with squares (aggregation) and circles (dispersion). The solid lines represent the fit to $\beta$ of the expression given by Eq. (23). Inset: The same plot for mutant cells. The solid line represents the fit of Eq. (25). The symbols represent ensemble averages.