Models of convergent extension during morphogenesis

Abstract

Convergent extension (CE) is a fundamental and conserved collective cell movement that forms elongated tissues during embryonic development. Thus far, studies have demonstrated two different mechanistic models of collective cell movements during CE. The first, termed the crawling mode, was discovered in the process of notochord formation in Xenopus laevis embryos, and has been the established model of CE for decades. The second model, known as the contraction mode, was originally reported in studies of germband extension in Drosophila melanogaster embryos and was recently demonstrated to be a conserved mechanism of CE among tissues and stages of development across species. This review summarizes the two modes of CE by focusing on the differences in cytoskeletal behaviors and relative expression of cell adhesion molecules. The upstream molecules regulating these machineries are also discussed. There are abundant studies of notochord formation in X. laevis embryos, as this was one of the pioneering model systems in this field. Therefore, the present review discusses these findings as an approach to the fundamental biological question of collective cell regulation. WIREs Dev Biol 2018, 7:e293. doi: 10.1002/wdev.293This article is categorized under: Early Embryonic Development > Gastrulation and NeurulationComparative Development and Evolution > Model Systems

Self-sustained Planar Intercalations due to Mechanosignaling Feedbacks Lead to Robust Axis Extension during Morphogenesis

“…oriented mechanical responses. A notable example is the convergentextension (CE) phenomenon due to cell intercalation events [9][10][11][12]. In other cases, a directed developmental expansion is achieved by translating polarity into differential growth events, oriented divisions, and/or active migration [13][14][15].…”

Differential expression and homotypic enrichment of a classic Cadherin directs tissue-level contractile asymmetry during neural tube closure

“…For example, apical localization and/or activation of factors such as Fog, T48 and Shroom family members can promote local activation of Myosin II and apical constriction to drive tissue bending/invagination (reviewed in (Gilmour et al, 2017;Heisenberg and Bellaiche, 2013;Lecuit et al, 2011;Martin and Goldstein, 2014)). Alternatively, polarized activation of Myosin II at cell-cell junctions by core members of the Planar Cell Polarity (PCP) pathway can drive planar-polarized junction contraction, leading to cell-cell intercalation and tissue elongation (reviewed in (Harris, 2018;Heisenberg and Bellaiche, 2013;Shindo, 2018;Walck-Shannon and Hardin, 2014)). For example, in chick embryos, local enrichment of PCP proteins Celser1, on mediolaterally oriented apical junctions, promotes planar polarized myosin activation, junction contraction and cell intercalation to induce tissue invagination and elongation during neural tube closure (Nishimura et al, 2012).…”

Frequency and synchrony of actomyosin oscillation during PCP-dependent convergent extension

“…During convergent extension, cells rearrange by intercalating specifically in the mediolateral axis, thereby elongating the tissue in the perpendicular, anteroposterior axis (Walck-Shannon and Hardin, 2014). Two sub-cellular mechanisms have been shown to contribute to mediolateral cell intercalation (Shindo, 2017): First, mediolaterally-oriented protrusions act in a manner analogous to the leading edge of a migrating cell, driving cell intercalation via cell crawling (Shih and Keller, 1992). Second, pulsed actomyosin contractions actively shrink mediolaterally-oriented junctions (so called v-junctions, Figure S1A), thereby driving intercalation (Bertet et al, 2004, Blankenship et al, 2006.…”