Actomyosin Pulsing in Tissue Integrity Maintenance during Morphogenesis

Abstract

Summary The actomyosin cytoskeleton is responsible for many changes in cell and tissue shape. For a long time, the actomyosin cytoskeleton has been known to exhibit dynamic contractile behavior. Recently, discrete actomyosin assembly/disassembly cycles have also been observed in cells. These so-called actomyosin pulses have been observed in a variety of contexts, including cell polarization and division, and in epithelia, where they occur during tissue contraction, folding, and extension. In epithelia, evidence suggests that actomyosin pulsing, and more generally, actomyosin turnover, is required to maintain tissue integrity during contractile processes. This review explores possible functions for pulsing in the many instances during which pulsing has been observed, and also highlights proposed molecular mechanisms that drive pulsing.

Rho GTPases and actomyosin: Partners in regulating epithelial cell-cell junction structure and function

“…In addition to resisting mechanical forces from neighboring cells, the contractile actomyosin network associated with AJs can also transmit tension across cell-cell junctions to neighboring cells, actively shaping tissues during development. For example, pulsatile contraction of actomyosin coupled to AJs promotes apical constriction of individual cells, which collectively leads to tissue folding (Coravos et al, 2016; Takeichi, 2014), and promotes intercalation, during which cells remodel their cell-cell contacts through neighbor exchange (Lecuit and Yap, 2015). Each of these functional roles of AJs is dependent on regulated linkage of the core molecular components of AJs to the actomyosin cytoskeleton.…”

“…It is currently debated whether these bundles form a ring or terminate at tricellular junctions, making each bicellular junction a singular contractile unit (Choi et al, 2016). Additionally, junctions are linked to medial-apical actomyosin, which spans the apical surface of epithelial cells and drives pulsatile contractions that cause cell-scale apical constriction and tissue-scale invagination (Coravos et al, 2016; Lecuit and Yap, 2015). …”

Cell ingression: Relevance to limb development and for adaptive evolution

“…Oscillatory contractions that drive apical constriction among delaminating neuroblasts in the Drosophila embryo Simões et al, 2017) may be regulated by non-muscle myosin dynamics (reviewed in Coravos et al, 2017). Oscillatory mechanisms are conserved among vertebrate epithelial cells that intercalate (Lau et al, 2015;Wen et al, 2017), although few upstream signalling pathways that regulate actomyosin kinetics have been identified (Gorfinkiel, 2016).…”

Cell-type specific mechanical response and myosin dynamics during retinal lens development in Drosophila

“…meshwork is pulsatile, with cycles of discrete node contraction and relaxation that occur over tens of seconds, and that can promote apical area fluctuations and AJ remodelling over similar time scales (Coravos et al, 2017). Contractile pulses appear to be self-organizing and associated with cycles of phosphorylation and dephosphorylation of the MyoII regulatory light chain, and thus cycles of 70 assembly/disassembly of the meshworks (Kasza et al, 2014;Vasquez et al, 2014;Munjal et al, 2015;Mason et al, 2016).…”

“…These two pools are linked, as the medial meshwork is anchored to the AJ through discrete points of contact (Roh-Johnson et al, 2012;Heisenberg and Bellaiche, 2013). The medial 4 harness the contractile forces applied onto the AJ by the medial meshwork to promote AJ remodelling (Coravos et al, 2017). As morphogenesis proceeds in a simple 75 epithelium, individual cell heterogeneities tend to be 'averaged out' to produce a homogenous tissue, consisting of cells with very similar apical geometry (Gibson et al, 2006;Farhadifar et al, 2007).…”