Coordinated assembly and release of adhesions builds apical junctional belts during de novo polarisation of an epithelial tube.

Andrew C Symonds,Jonathan D W Clarke,Charlotte A Williams,Clare E Buckley

doi:10.1242/dev.191494

Andrew C Symonds, Jonathan D W Clarke + Show 2 more

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https://doi.org/10.1242/dev.191494

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Abstract

ABSTRACTUsing the zebrafish neural tube as a model, we uncover the in vivo mechanisms allowing the generation of two opposing apical epithelial surfaces within the centre of an initially unpolarised, solid organ. We show that Mpp5a and Rab11a play a dual role in coordinating the generation of ipsilateral junctional belts whilst simultaneously releasing contralateral adhesions across the centre of the tissue. We show that Mpp5a- and Rab11a-mediated resolution of cell-cell adhesions are both necessary for midline lumen opening and contribute to later maintenance of epithelial organisation. We propose that these roles for both Mpp5a and Rab11a operate through the transmembrane protein Crumbs. In light of a recent conflicting publication, we also clarify that the junction-remodelling role of Mpp5a is not specific to dividing cells.

Highlights

Epithelia are one of the fundamental tissue types of the body, forming protective sheets of cells around the outside of the organism and lining the inside surface of many organs or parts of organs
Apical rings of Partitioning-defective 3 (Pard3) and ZO-1 are built up from the ventral floor plate The apical surface of epithelia is characterised by a lattice-like arrangement of polarity and scaffolding proteins [such as Pard3, atypical protein kinase C and zona occludens 1 (ZO-1; known as Tjp1a)] and cell adhesion proteins
The development and remodelling of apical epithelial junctions is likely to be regulated by a complex integration of molecular interactions involving polarity proteins and adhesion proteins (Martin-Belmonte and Mostov, 2008; St Johnston and Ahringer, 2010; Datta et al, 2011), together with biomechanical forces that interpret tissue tensions generated by the actomyosin cyctoskeleton (Pinheiro and Bellaiche, 2018)

Summary

Introduction

Epithelia are one of the fundamental tissue types of the body, forming protective sheets of cells around the outside of the organism and lining the inside surface of many organs or parts of organs. Generating an apical surface from within a rod or ball of cells adds an extra layer of complexity to this process, because cells at the centre of these structures have to lose inappropriate connections to generate a free surface. They must organise that free surface into a typical apical structure comprising a lattice of closely adherent cells connected by apicolateral belts of specialised junctions (typically adherens junctions and tight junctions in vertebrates). A key step, elucidated in epithelial development in flies, is the Crumbs-

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