Mitotic Cortical Waves Predict Future Division Sites by Encoding Positional and Size Information

Abstract

Dynamic spatial patterns such as traveling waves could theoretically encode spatial information, but little is known about whether or how they are employed by biological systems, especially higher eukaryotes. Here, we show that concentric target or spiral waves of active Cdc42 and the F-BAR protein FBP17 are invoked in adherent cells at the onset of mitosis. These waves predict the future sites of cell divisions and represent the earliest known spatial cues for furrow assembly. Unlike interphase waves, the frequencies and wavelengths of the mitotic waves display size-dependent scaling properties. While the positioning role of the metaphase waves requires microtubule dynamics, spindle and microtubule-independent inhibitory signals are propagated by the mitotic waves to ensure the singularity of furrow formation. Taken together, we propose that metaphase cortical waves integrate positional and cell size information for division-plane specification in adhesion-dependent cytokinesis.

Chemical waves in cell and developmental biology

“…This coupling might arise from a traveling wave of Cdk1 activity in frog embryos ( Chang and Ferrell, 2013 ) and a gradient of Cdk1 activity in starfish embryos ( Bischof et al, 2017 ). In cultured adherent cells, mitotic cortical waves of Cdc42 activity and of the F-BAR protein FBP17 might provide both positional and size information to specify the cell division plane ( Xiao et al, 2017 ), suggesting a role for chemical waves in cell size control. It has been speculated that linear waves in reaction–diffusion systems represent a strategy for size control in biological systems ( Laughlin, 2015 ).…”

How cells sense their own shape – mechanisms to probe cell geometry and their implications in cellular organization and function

“…Remarkably, the Min proteins can self-assemble into dynamic patterns in vitro and probe the geometry to define a long axis, even in triangular or squared shapes (Schweizer et al, 2012;Wu et al, 2015;Zieske and Schwille, 2014). Thus, a system based on reaction-diffusion can generate specific positional protein patterns with respect to the geometry of a cell and may represent an additional important feature to connect cell shape with division position (Xiao et al, 2017).…”

Comparative study of curvature sensing mediated by F-BAR domain and an intrinsically disordered region of FBP17

“…In addition, the IDR of the cytokinetic F-BAR protein Cdc15 in fission yeast was shown to be important for the maintenance of cytokinetic ring (Mangione et al, 2019). Cell protrusions and leading edge dynamics as well as cytokinesis are often simplified as actin cytoskeletal-centric rearrangement but there are also controlled by cortical propagating waves and interlinked oscillatory networks that remain to be elucidated (Bement et al, 2015;Bolado-Carrancio et al, 2020;Katsuno et al, 2015;Miao et al, 2017;Ruthel and Banker, 1999;Xiao et al, 2017). An intriguing possibility is that these kinetic parameter changes could have implications in the conversion between regimes of dynamical systems (also known as bifurcations) which then result in morphogenetic outcomes.…”