Relevance of intracellular polarity to accuracy of eukaryotic chemotaxis

Abstract

Chemotactic cells establish cell polarity in the absence of external guidance cues. Such self-organized polarity is induced by spontaneous symmetry breaking in the intracellular activities, which produces an emergent memory effect associated with slow-changing mode. Therefore, spontaneously established polarity should play a pivotal role in efficient chemotaxis. In this study, we develop a model of chemotactic cell migration that demonstrates the connection between intracellular polarity and chemotactic accuracy. Spontaneous polarity formation and gradient sensing are described by a stochastic differential equation. We demonstrate that the direction of polarity persists over a characteristic time that is predicted to depend on the chemoattractant concentration. Next, we theoretically derive the chemotactic accuracy as a function of both the gradient sensing ability and the characteristic time of polarity direction. The results indicate that the accuracy can be improved by the polarity. Furthermore, the analysis of chemotactic accuracy suggests that accuracy is maximized at some optimal responsiveness to extracellular perturbations. To obtain the model parameters, we studied the correlation time of random cell migration in cell tracking analysis of Dictyostelium cells. As predicted, the persistence time depended on the chemoattractant concentration. From the fitted parameters, we inferred that polarized Dictyosteium cells can respond optimally to a chemical gradient. Chemotactic accuracy was almost 10 times larger than can be achieved by non-polarized gradient sensing. Using the obtained parameter values, we show that polarity also improves the dynamic range of chemotaxis.