Dynamic determinations: patterning the cell behaviours that close the amphibian blastopore

Abstract

We review the dynamic patterns of cell behaviours in the marginal zone of amphibians with a focus on how the progressive nature and the geometry of these behaviours drive blastopore closure. Mediolateral cell intercalation behaviour and epithelial-mesenchymal transition are used in different combinations in several species of amphibian to generate a conserved pattern of circumblastoporal hoop stresses. Although these cell behaviours are quite different and involve different germ layers and tissue organization, they are expressed in similar patterns. They are expressed progressively along presumptive lateral-medial and anterior-posterior axes of the body plan in highly ordered geometries of functional significance in the context of the biomechanics of blastopore closure, thereby accounting for the production of similar patterns of circumblastoporal forces. It is not the nature of the cell behaviour alone, but the context, the biomechanical connectivity and spatial and temporal pattern of its expression that determine specificity of morphogenic output during gastrulation and blastopore closure. Understanding the patterning of these dynamic features of cell behaviour is important and will require analysis of signalling at much greater spatial and temporal resolution than that has been typical in the analysis of patterning tissue differentiation.

PDGF-A controls mesoderm cell orientation and radial intercalation duringXenopusgastrulation

“…Development 138 (3) the LEM converges in the process of mantle closure (Davidson et al, 2002), and behind it, convergence of the posterior mesoderm closes the blastopore (Keller et al, 2003;Keller and Shook, 2008). Importantly, spreading depends on an interaction with the BCR, but not with its FN matrix (Winklbauer and Schurfeld, 1999).…”

Mechanics of blastopore closure during amphibian gastrulation

“…A number of cellular behaviors are thought to drive closure but the precise biomechanics of these processes and their relative contributions to the integrated tissue mechanics that drives closure remain unknown (Keller and Shook, 2008). On the dorsoanterior face of the embryo, presumptive notochordal and somitic mesoderm cells involute and undergo convergent extension.…”

“…On the dorsoanterior face of the embryo, presumptive notochordal and somitic mesoderm cells involute and undergo convergent extension. Mesoderm involution and convergent extension are thought to be driven by active mediolateral intercalation, which elongates the tissue and is proposed to generate an arc of tension that contributes to BC (Keller et al, 2003; Keller and Shook, 2008). In the posterior-ventral region, involuting marginal zone cells undergo convergent thickening which produces a thicker tissue further contributing to BC (Keller and Shook, 2008).…”

“…Cell and tissue movements accompanying Xenopus gastrulation have been described previously (Ewald et al, 2002; Keller et al, 2003; Keller and Shook, 2008; Moosmann et al, 2013; Tyszka et al, 2005) but to understand the physical mechanics of BC requires quantitative measurement of spatial and temporal changes in cell and tissue rearrangement, cellular force generation, and tissue mechanical properties. Such quantitative studies require tools with which strain or strain rates can be measured after application of known forces or loads (Davidson and Keller, 2007).…”

Introduction. Calcium signals and developmental patterning

“…Wnt/Ca signalling is also necessary for the development of Brachet's cleft (essential for involution) by modulating ectoderm-mesoderm adhesion ( Winklbauer et al 2001). Keller & Shook (2008) describe in this issue how convergent extension movements induce gastrulation in Xenopus.…”