Ordered Patterns of Cell Shape and Orientational Correlation during Spontaneous Cell Migration

Background

In the absence of stimuli, most motile eukaryotic cells move byspontaneously coordinating cell deformation with cell movement in theabsence of stimuli. Yet little is known about how cells change their ownshape and how cells coordinate the deformation and movement. Here, weinvestigated the mechanism of spontaneous cell migration by usingcomputational analyses.

Methodology

We observed spontaneously migrating Dictyostelium cellsin both a vegetative state (round cell shape and slow motion) andstarved one (elongated cell shape and fast motion). We then extractedregular patterns of morphological dynamics and the pattern-dependentsystematic coordination with filamentous actin (F-actin) and cellmovement by statistical dynamic analyses.

Conclusions/Significance

We found that Dictyostelium cells in both vegetative andstarved states commonly organize their own shape into three orderedpatterns, elongation, rotation, and oscillation, in the absence ofexternal stimuli. Further, cells inactivated for PI3-kinase (PI3K)and/or PTEN did not show ordered patterns due to the lack of spatialcontrol in pseudopodial formation in both the vegetative and starvedstates. We also found that spontaneous polarization was achieved instarved cells by asymmetric localization of PTEN and F-actin. Thisbreaking of the symmetry of protein localization maintained the leadingedge and considerably enhanced the persistence of directed migration,and overall random exploration was ensured by switching among thedifferent ordered patterns. Our findings suggest thatDictyostelium cells spontaneously create theordered patterns of cell shape mediated by PI3K/PTEN/F-actin and controlthe direction of cell movement by coordination with these patterns evenin the absence of external stimuli.