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A continuum model for the growth of dendritic actin networks.

ABSTRACT: Polymerization of dendritic actin networks underlies important mechanical processes in cell biology such as the protrusion of lamellipodia, propulsion of growth cones in dendrites of neurons, intracellular transport of organelles and pathogens, among others. The forces required for these mechanical functions have been deduced from mechano-chemical models of actin polymerization; most models are focused on single growing filaments, and only a few address polymerization of filament networks through simulations. Here, we propose a continuum model of surface growth and filament nucleation to describe polymerization of dendritic actin networks. The model describes growth and elasticity in terms of macroscopic stresses, strains and filament density rather than focusing on individual filaments. The microscopic processes underlying polymerization are subsumed into kinetic laws characterizing the change of filament density and the propagation of growing surfaces. This continuum model can predict the evolution of actin networks in disparate experiments. A key conclusion of the analysis is that existing laws relating force to polymerization speed of single filaments cannot predict the response of growing networks. Therefore, a new kinetic law, consistent with the dissipation inequality, is proposed to capture the evolution of dendritic actin networks under different loading conditions. This model may be extended to other settings involving a more complex interplay between mechanical stresses and polymerization kinetics, such as the growth of networks of microtubules, collagen filaments, intermediate filaments and carbon nanotubes.

SUBMITTER: Abeyaratne R

PROVIDER: S-EPMC7544340 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Neurite growth is a fundamental process of neuronal development, which requires both membrane expansions by exocytosis and cytoskeletal dynamics. However, the specific contribution of these processes has not been yet assessed quantitatively. To study and quantify the growth process, we construct a biophysical model in which we relate the overall neurite outgrowth rate to the vesicle dynamics. By considering the complex motion of vesicles in the cell soma, we demonstrate from biophysical consideration that the main step of finding the neurite initiation site relies mainly on a two-dimensional diffusion/sequestration/fusion at the cell surface and we obtain a novel formula for the flux of vesicles at the neurite base. In the absence of microtubules, we show that a nascent neurite initiated by vesicular delivery can only reach a small length. By adding the microtubule dynamics to the secretory pathway and using stochastic analysis and simulations, we study the complex dynamics of neurite growth. Within this model, depending on the coupling parameter between the microtubules and the neurite, we find different regimes of growth, which describe dendritic and axonal growth. To validate one aspect of our model, we demonstrate that the experimental flux of TI-VAMP but not Synaptobrevin 2 vesicles contributes to the neurite growth. We conclude that although vesicles can be generated randomly in the cell body, the search for the neurite position using the microtubule network and diffusion is quite fast. Furthermore, when the TI-VAMP vesicular flow is large enough, the interactions between the microtubule bundle and the neurite control the growth process. In addition, all of these processes intimately cooperate to mediate the various modes of neurite growth: the model predicts three different growing modes including, in addition to the stable axonal growth and the stochastic dendritic growth, a fast oscillatory regime. Finally our study demonstrates that cytoskeletal dynamics is necessary to generate long protrusion, while vesicular delivery alone can only generate small neurite.

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A continuum model for the growth of dendritic actin networks.

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