Stereotyped terminal axon branching of leg motor neurons mediated by IgSF proteins DIP-α and Dpr10.

Lalanti Venkatasubramanian,Zhenhao Guo,Shuwa Xu,Richard S Mann,Sonal Nagarkar-Jaiswal,Qi Xiao,Liming Tan

doi:10.7554/elife.42692

Lalanti Venkatasubramanian, Zhenhao Guo + Show 5 more

Open Access

https://doi.org/10.7554/elife.42692

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Abstract

For animals to perform coordinated movements requires the precise organization of neural circuits controlling motor function. Motor neurons (MNs), key components of these circuits, project their axons from the central nervous system and form precise terminal branching patterns at specific muscles. Focusing on the Drosophila leg neuromuscular system, we show that the stereotyped terminal branching of a subset of MNs is mediated by interacting transmembrane Ig superfamily proteins DIP-α and Dpr10, present in MNs and target muscles, respectively. The DIP-α/Dpr10 interaction is needed only after MN axons reach the vicinity of their muscle targets. Live imaging suggests that precise terminal branching patterns are gradually established by DIP-α/Dpr10-dependent interactions between fine axon filopodia and developing muscles. Further, different leg MNs depend on the DIP-α and Dpr10 interaction to varying degrees that correlate with the morphological complexity of the MNs and their muscle targets.

Highlights

Animal behavior depends on the stereotyped morphologies of neurons and their assembly into complex neural circuits
To characterize the role of the DIP and Dpr proteins in motor neurons (MNs) development we first describe the process by which leg MN axons achieve their stereotyped muscle targeting and terminal branching patterns
We focused on the development of leg MNs targeting the foreleg (T1), the developmental processes described here are consistent across all three pairs of legs

Summary

Introduction

Animal behavior depends on the stereotyped morphologies of neurons and their assembly into complex neural circuits. Distinct neurons in many neural systems use combinations of effector molecules, such as cell-surface proteins, to form stereotyped connections with specific synaptic partners during circuit assembly (Catela et al, 2015; Hong and Luo, 2014; Hattori et al, 2008). The precise location of NMJ formation along each muscle fiber, defined by MN branch innervation as well as pre-patterned sites along each fiber, might require reproducible terminal branching patterns (Kummer et al, 2006) This precision is observed in Drosophila MNs that target larval body-wall muscles, where there are stereotyped differences between synapse size, terminal branching morphologies and electrophysiological properties (Newman et al, 2017; Choi et al, 2004; Hoang and Chiba, 2001). The accompanying paper (Ashley et al, 2018) shows that the DIP-aDpr interaction plays a similar role in the larval neuromuscular system, suggesting a remarkably conserved function for these IgSF proteins at two stages of Drosophila development

Results

Discussion

Materials and methods

Funding Funder National Institutes of Health