Apical Cell-Cell Adhesions Reconcile Symmetry and Asymmetry in Zebrafish Neurulation

Chuanyu Guo,Jian Zou,Yi Wen,Wei Fang,Donna Beer Stolz,Ming Sun,Xiangyun Wei

doi:10.1016/j.isci.2018.04.007

Abstract

SummaryThe symmetric tissue and body plans of animals are paradoxically constructed with asymmetric cells. To understand how the yin-yang duality of symmetry and asymmetry are reconciled, we asked whether apical polarity proteins orchestrate the development of the mirror-symmetric zebrafish neural tube by hierarchically modulating apical cell-cell adhesions. We found that apical polarity proteins localize by a pioneer-intermediate-terminal order. Pioneer proteins establish the mirror symmetry of the neural rod by initiating two distinct types of apical adhesions: the parallel apical adhesions (PAAs) cohere cells of parallel orientation and the novel opposing apical adhesions (OAAs) cohere cells of opposing orientation. Subsequently, the intermediate proteins selectively augment the PAAs when the OAAs dissolve by endocytosis. Finally, terminal proteins are required to inflate the neural tube by generating osmotic pressure. Our findings suggest a general mechanism to construct mirror-symmetric tissues: tissue symmetry can be established by organizing asymmetric cells opposingly via adhesions.

Highlights

Symmetry is a hallmark of metazoan body plans as well as tissue and organ architectures (Martindale et al, 2002)
We found that the localization of apical polarity proteins follows a strict three-step spatiotemporal order; we categorize these proteins into three groups: ‘‘pioneer,’’ ‘‘intermediate,’’ and ‘‘terminal’’ proteins
To determine whether apical enrichment of N-Cad and ZO-1 requires new protein synthesis, we treated the embryos with protein synthesis inhibitor cycloheximide; we found that both N-Cad-green fluorescent protein (GFP) and ZO-1-mCherry still enriched apically (Figure 4E), suggesting that N-Cad and ZO-1 could enrich at the midline region by apical translocation to initiate the parallel apical adhesions (PAAs) and opposing apical adhesions (OAAs); accompanying the formation of the PAAs and OAAs was the establishment of the mirror symmetry, which was manifested by equal distribution of cells on the two sides of the midline (Figure S4D)

Summary

Introduction

Symmetry is a hallmark of metazoan body plans as well as tissue and organ architectures (Martindale et al, 2002). Arises the fundamental biological and even philosophical question of just how the yin-yang duality of asymmetry and symmetry is reconciled during tissue morphogenesis. This general question may be addressed by studying vertebrate neurulation because this morphogenesis robustly builds a mirror-symmetric neural tube de novo from asymmetrically polarized neuroepithelial cells through opposing configuration. Cells need to be plastic to reorganize their relative positions and to modify their shapes to form a tube; on the other hand, cells need to be cohesive with each other to maintain certain tissue architectures. The key to a delicate balance between plasticity and cohesiveness is the modulation of cell-cell adhesion. Apical polarity proteins must dynamically modulate apical adhesions, which in turn regulate cellular reorganization during vertebrate neurulation

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Conclusion