Dictyostelium myosin 1F and myosin 1E inhibit actin waves in a lipid‐binding‐dependent and motor‐independent manner

Abstract

Actin waves are F-actin-rich entities traveling on the ventral plasma membrane by the treadmilling mechanism. Actin waves were first discovered and are best characterized in Dictyostelium. Class I myosins are unconventional monomeric myosins that bind lipids through their tails. Dictyostelium has seven class I myosins, six of these have tails (Myo1A-F) while one has a very short tail (Myo1K), and three of them (Myo1D, Myo1E and Myo1F) bind PIP3 with high affinity. Localization of five Dictyostelium Class I myosins synchronizes with localization and propagation of actin waves. Myo1B and Myo1C colocalize with actin in actin waves, whereas Myo1D, E and F localize to the PIP3-rich region surrounded by actin waves. Here, we studied the effect of overexpression of the three PIP3 specific Class I myosins on actin waves. We found that ectopic expression of the short-tail Myo1F inhibits wave formation, short-tail Myo1E has similar but weaker inhibitory effect, but long-tail Myo1D does not affect waves. A study of Myo1F mutants shows that its membrane-binding site is absolutely required for wave inhibition, but the head portion is not. The results suggest that PIP3 specificity and the presence of two membrane-binding sites are required for inhibition of actin waves, and that inhibition may be caused by crosslinking of PIP3 heads groups.

From actin waves to mechanism and back: How theory aids biological understanding

“…In addition, both regions exhibit distinct network architectures ( Jasnin et al, 2019 ) and surface charges ( Banerjee et al, 2022 ). The different class I myosins colocalize with the wave or the inner region and may inhibit wave formation in a lipid-binding dependent manner ( Brzeska et al, 2014 ; Brzeska et al, 2020 ). When traveling over larger cortical areas of oversized cells, waves maintain a preferred size and may annihilate upon collision ( Gerhardt et al, 2014a ; Miao et al, 2019 ).…”