Abstract

The teneurins, also known as Ten-m/Odz, are highly conserved type II transmembrane glycoproteins widely expressed throughout the nervous system. Functioning as dimers, these large cell-surface adhesion proteins play a key role in regulating neurodevelopmental processes such as axon targeting, synaptogenesis and neuronal wiring. Synaptic specificity is driven by molecular interactions, which can occur either in a trans-homophilic manner between teneurins or through a trans-heterophilic interaction across the synaptic cleft between teneurins and other cell-adhesion molecules, such as latrophilins. The significance of teneurins interactions during development is reflected in the widespread expression pattern of the four existing paralogs across interconnected regions of the nervous system, which we demonstrate here via in situ hybridization and the generation of transgenic BAC reporter lines in zebrafish. Focusing on the visual system, we will also highlight the recent developments that have been made in furthering our understanding of teneurin interactions and their functionality, including the instructive role of teneurin-3 in specifying the functional wiring of distinct amacrine and retinal ganglion cells in the vertebrate visual system underlying a particular functionality. Based on the distinct expression pattern of all teneurins in different retinal cells, it is conceivable that the combination of different teneurins is crucial for the generation of discrete visual circuits. Finally, mutations in all four human teneurin genes have been linked to several types of neurodevelopmental disorders. The opportunity therefore arises that findings about the roles of zebrafish teneurins or their orthologs in other species shed light on the molecular mechanisms in the etiology of such human disorders.

Highlights

  • As one of the most complex systems in nature, the functionality of the nervous system is highly dependent on the formation of precise synaptic connections between neurons during development

  • The expression patterns of the four vertebrate paralogs of teneurin were investigated via wholemount in situ hybridization on zebrafish embryos over 1 to 5 dpf

  • We describe here the expression pattern of different members of the teneurin family across the central nervous system in zebrafish during development, focusing on the visual system where they have been shown to play a pivotal role in establishing connectivity, via in situ hybridization and bacterial artificial chromosome (BAC) transgenesis

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Summary

Introduction

As one of the most complex systems in nature, the functionality of the nervous system is highly dependent on the formation of precise synaptic connections between neurons during development. The teneurins, known as Ten-m/Odz, are one family of such cell adhesion molecules that has been implicated, among others, in regulating the specificity of synaptic connections. A phylogenetically conserved family of type II transmembrane glycoproteins first discovered in the early 1990s in Drosophila, the teneurins have been shown to be involved in intercellular signaling during development (Tucker and Chiquet-Ehrismann, 2006; Tucker et al, 2012). Their key role in mediating basic neurodevelopmental processes such as axon guidance and synaptic. Sequence similarity is high between paralogs, with human teneurin paralogs sharing 58–70% sequence identity (Jackson et al, 2018)

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