Stages and transitions in dendrite arbor differentiation

Yoong, Li-Foong; Pai, Yun-Jin; Moore, Adrian W.

doi:10.1016/j.neures.2018.09.015

Cited by 11 publications

(20 citation statements)

References 134 publications

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“…Taken together, our results demonstrate that a specialised dendritic tree pattern that minimises wire can be obtained by the precise temporal arrangement of stochastic developmental programs. Interestingly, evidence can be found that similar stages and strategies may be preserved across different cell types (Richardson and Shen, 2019;Gao et al, 2000;Sugimura et al, 2003Sugimura et al, , 2007Baltruschat et al, 2020) and species (Yoong et al, 2019). The flexible usage of such self-organisational programs provides developmental resilience and robustness to perturbations in the growth medium (Hiesinger and Hassan, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Within the egg (Figure 1A), the main branch (MB) emerged from the soma at around 16hrs AEL and extended in a dorsal orientation. Afterwards, a number of second-order lateral interstitial branches appeared from the initial MB extending in both the anterior and posterior directions, with the MB dorsal position potentially biasing their growth direction along the anteroposterior axis (Yoong et al, 2019). Then, shorter third-order lateral branches sprouted interstitially from the second-order lateral branches mainly along the dorsoventral axis.…”

Section: /57mentioning

confidence: 99%

“…In the past, studies based on low temporal resolution static data of dendrite development suggested that distinct growth and retraction phases may happen sequentially during development (Lázár, 1973;Huttenlocher and Dabholkar, 1997;Bystron et al, 2008). At higher temporal resolution, time-lapse movies showed that branch additions and retractions seem to happen rather concurrently during arbour elaboration (Hua and Smith, 2004;Hossain et al, 2012;Cline, 2001;Dailey and Smith, 1996;Yoong et al, 2019). In our dataset on c1vpda, we observed parallel growth and retraction of branches with changes in their proportions leading to separate phases of predominant outgrowth, retraction and then stabilisation.…”

Section: Phases Of C1vpda Developmentmentioning

confidence: 99%

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Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Castro

Baltruschat

Stuerner

et al. 2020

Preprint

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Class I ventral posterior dendritic arborisation (c1vpda) proprioceptive sensory neurons respond to contractions in the Drosophila larval body wall during crawling. Their dendritic branches run along the direction of contraction, possibly a functional requirement to maximise membrane curvature during crawling contractions. Although the molecular machinery of dendritic patterning in c1vpda has been extensively studied, the process leading to the precise elaboration of their comb-like shapes remains elusive. Here, to link dendrite shape with its proprioceptive role, we performed long-term, non-invasive, in vivo time-lapse imaging of c1vpda embryonic and larval morphogenesis to reveal a sequence of differentiation stages. We combined computer models and dendritic branch dynamics tracking to propose that distinct sequential phases of targeted growth and stochastic retraction achieve efficient dendritic trees both in terms of wire and function. Our study shows how dendrite growth balances structure-function requirements, shedding new light on general principles of self-organisation in functionally specialised dendrites.

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Section: Discussionmentioning

confidence: 99%

Section: /57mentioning

confidence: 99%

Section: Phases Of C1vpda Developmentmentioning

confidence: 99%

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Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Castro

Baltruschat

Stuerner

et al. 2020

Preprint

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“…Extracellular cues that modulate axonal branch patterns act through Rho GTPases and other cytosolic factors to regulate changes in cytoskeletal dynamics (Spillane and Gallo, 2014). Given that axon branching can affect the functional properties of a neuron (Yoong et al, 2019), it is important to consider how cues in development dictate the differences in branch morphol-ogy. In this report, we show that Semaphorin-5B controls the branching behaviors of auditory neurons within the cochlea.…”

Section: Introductionmentioning

confidence: 99%

Semaphorin-5B Controls Spiral Ganglion Neuron Branch Refinement during Development

et al. 2019

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During nervous system development, axons often undergo elaborate changes in branching patterns before circuits have achieved their mature patterns of innervation. In the auditory system, type I spiral ganglion neurons (SGNs) project their peripheral axons into the cochlear epithelium and then undergo a process of branch refinement before forming synapses with sensory hair cells. Here, we report that Semaphorin-5B (Sema5B) acts as an important mediator of this process. During cochlear development in mouse, immature hair cells express Sema5B, whereas the SGNs express both PlexinA1 and PlexinA3, which are known Sema5B receptors. In these studies, genetic sparse labeling and three-dimensional reconstruction techniques were leveraged to determine the morphologies of individual type I SGNs after manipulations of Sema5B signaling. Treating cultured mouse cochleae with Sema5B-Fc (to activate Plexin-As) led to type I SGNs with less numerous, but longer terminal branches. Conversely, cochleae from Sema5b knockout mice showed type I SGNs with more numerous, but shorter terminal branches. In addition, conditional loss of Plxna1 in SGNs (using Bhlhb5 Cre) led to increased type I SGN branching, suggesting that PlexinA1 normally responds to Sema5B in this process. In these studies, mice of either sex were used. The data presented here suggest that Sema5B-PlexinA1 signaling limits SGN terminal branch numbers without causing axonal repulsion, which is a role that distinguishes Sema5B from other Semaphorins in cochlear development.

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“…In this article, we summarize recent data that reveal several distinct modes of MTOC formation and de novo microtubule generation within a differentiating neuron. Because final complex arbor wiring patterns are generated through a series of morphogenetic differentiation events (Yoong et al, 2019), we then go beyond the level of molecular mechanism to synthesize a view at the systems level. We discuss how the usage of distinct microtubule generation mechanisms changes as arbor formation proceeds, how they are spatially and temporally organized in the differentiating neuron to generate arbor complexity, and how changing the relative activity of distinct MTOC mechanisms diversifies arbor patterning.…”

Section: Introductionmentioning

confidence: 99%

Distinct Microtubule Organizing Center Mechanisms Combine to Generate Neuron Polarity and Arbor Complexity

Wilkes

Moore

2020

Front. Cell. Neurosci.

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Dendrite and axon arbor wiring patterns determine the connectivity and computational characteristics of a neuron. The identities of these dendrite and axon arbors are created by differential polarization of their microtubule arrays, and their complexity and pattern are generated by the extension and organization of these arrays. We describe how several molecularly distinct microtubule organizing center (MTOC) mechanisms function during neuron differentiation to generate and arrange dendrite and axon microtubules. The temporal and spatial organization of these MTOCs generates, patterns, and diversifies arbor wiring.

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Stages and transitions in dendrite arbor differentiation

Cited by 11 publications

References 134 publications

Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Achieving functional neuronal dendrite structure through sequential stochastic growth and retraction

Semaphorin-5B Controls Spiral Ganglion Neuron Branch Refinement during Development

Distinct Microtubule Organizing Center Mechanisms Combine to Generate Neuron Polarity and Arbor Complexity

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