The branching code: a model of actin-driven dendrite arborisation

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Abstract

Summary Dendrites display a striking variety of neuronal type-specific morphologies, but the mechanisms and principles underlying such diversity remain elusive. A major player in defining the morphology of dendrites is the neuronal cytoskeleton, including evolutionarily conserved actin-modulatory proteins (AMPs). Still, we lack a clear understanding of how AMPs might support developmental phenomena such as neuron-type specific dendrite dynamics. To address precisely this level of in vivo specificity, we concentrated on a defined neuronal type, the class III dendritic arborisation (c3da) neuron of Drosophila larvae, displaying actin-enriched short terminal branchlets (STBs). Computational modelling reveals that the main branches of c3da neurons follow a general growth model based on optimal wiring, but the STBs do not. Instead, model STBs are defined by a short reach and a high affinity to grow towards the main branches. We thus concentrated on c3da STBs and developed new methods to quantitatively describe dendrite morphology and dynamics based on in vivo time-lapse imaging of mutants lacking individual AMPs. In this way, we extrapolated the role of these AMPs in defining STB properties. We propose that dendrite diversity is supported by the combination of a common step, refined by a neuron type-specific second level. For c3da neurons, we present a molecular model of how the combined action of multiple AMPs in vivo define the properties of these second level specialisations, the STBs. In brief A quantitative morphological dissection of the concerted actin-modulatory protein actions provides a model of dendrite branchlet outgrowth. Highlights Actin organisation in small terminal branchlets of Drosophila class III dendritic arborisation neurons Six actin-modulatory proteins individually control the characteristic morphology and dynamics of branchlets Quantitative tools for dendrite morphology and branch dynamics enable a comparative analysis A two-step computational growth model reproduces c3da dendrite morphology

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crossref
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License: CC-BY-NC-ND-4.0