Abstract

Oriented cell intercalation is an essential developmental process that shapes tissue morphologies through the directional insertion of cells between their neighbors. Previous research has focused on properties of cell-cell interfaces, while the function of tricellular vertices has remained unaddressed. Here, we identify a highly novel mechanism in which vertices demonstrate independent sliding behaviors along cell peripheries to produce the topological deformations responsible for intercalation. Through systematic analysis, we find that the motion of vertices connected by contracting interfaces is not physically coupled, but instead possess strong radial coupling. E-cadherin and Myosin II exist in previously unstudied populations at cell vertices and undergo oscillatory cycles of accumulation and dispersion that are coordinated with changes in cell area. Additionally, peak enrichment of vertex E-cadherin/Myosin II coincides with interface length stabilization. Our results suggest a model in which asymmetric radial force balance directs the progressive, ratcheted motion of individual vertices to drive intercalation.

Highlights

  • A common characteristic of many tissues and organisms is an elongation along a primary dimensional axis

  • And in contrast to the previously reported homogenous distribution of E-cadherin along DV interfaces at mid-germband extension (GBE) (Blankenship et al, 2006), we found that E-cadherin was highly enriched at vertices (Figure 1A, B and C, and Figure 1—figure supplement 1A–C)

  • This strong vertex-association of E-cadherin began at the onset of GBE, with E-cadherin diffusely present at apical cell interfaces prior to intercalation (Figure 1D and D’)

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Summary

Introduction

A common characteristic of many tissues and organisms is an elongation along a primary dimensional axis. The intercalary behaviors driving GBE occur through a remodeling of cell topologies, with cells contracting shared anterior-posterior (AP, vertical or T1) interfaces to a single point, followed by newly juxtaposed dorsal-ventral (DV) cells constructing horizontally-oriented interfaces between them (Irvine and Wieschaus, 1994; Bertet et al, 2004; Blankenship et al, 2006; Collinet et al, 2015; Yu and Fernandez-Gonzalez, 2016) This is referred to as a topological T1 process, and results in a cumulative contraction of the embryonic epithelium along the DV axis, which helps to drive a perpendicular elongation along the AP axis

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