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Actin blobs prefigure dendrite branching sites.

ABSTRACT: The actin cytoskeleton provides structural stability and adaptability to the cell. Neuronal dendrites frequently undergo morphological changes by emanating, elongating, and withdrawing branches. However, the knowledge about actin dynamics in dendrites during these processes is limited. By performing in vivo imaging of F-actin markers, we found that F-actin was highly dynamic and heterogeneously distributed in dendritic shafts with enrichment at terminal dendrites. A dynamic F-actin population that we named actin blobs propagated bidirectionally at an average velocity of 1 µm/min. Interestingly, these actin blobs stalled at sites where new dendrites would branch out in minutes. Overstabilization of F-actin by the G15S mutant abolished actin blobs and dendrite branching. We identified the F-actin-severing protein Tsr/cofilin as a regulator of dynamic actin blobs and branching activity. Hence, actin blob localization at future branching sites represents a dendrite-branching mechanism to account for highly diversified dendritic morphology.

SUBMITTER: Nithianandam V

PROVIDER: S-EPMC6168249 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Actin blobs prefigure dendrite branching sites.

Nithianandam Vanitha V Chien Cheng-Ting CT

The Journal of cell biology 20180724 10

The actin cytoskeleton provides structural stability and adaptability to the cell. Neuronal dendrites frequently undergo morphological changes by emanating, elongating, and withdrawing branches. However, the knowledge about actin dynamics in dendrites during these processes is limited. By performing in vivo imaging of F-actin markers, we found that F-actin was highly dynamic and heterogeneously distributed in dendritic shafts with enrichment at terminal dendrites. A dynamic F-actin population th ...[more]

PMID: 30042190

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Project description:BackgroundDendrite morphogenesis plays an essential role in establishing the connectivity and receptive fields of neurons during the development of the nervous system. To generate the diverse morphologies of branched dendrites, neurons use external cues and cell surface receptors to coordinate intracellular cytoskeletal organization; however, the molecular mechanisms of how this signaling forms branched dendrites are not fully understood.MethodsWe performed in vivo time-lapse imaging of the PVD neuron in C. elegans in several mutants of actin regulatory proteins, such as the WAVE Regulatory Complex (WRC) and UNC-34 (homolog of Enabled/Vasodilator-stimulated phosphoprotein (Ena/VASP)). We examined the direct interaction between the WRC and UNC-34 and analyzed the localization of UNC-34 in vivo using transgenic worms expressing UNC-34 fused to GFP.ResultsWe identify a stereotyped sequence of morphological events during dendrite outgrowth in the PVD neuron in C. elegans. Specifically, local increases in width ("swellings") give rise to filopodia to facilitate a "rapid growth and pause" mode of growth. In unc-34 mutants, filopodia fail to form but swellings are intact. In WRC mutants, dendrite growth is largely absent, resulting from a lack of both swelling and filopodia formation. We also found that UNC-34 can directly bind to the WRC. Disrupting this binding by deleting the UNC-34 EVH1 domain prevented UNC-34 from localizing to swellings and dendrite tips, resulting in a stunted dendritic arbor and reduced filopodia outgrowth.ConclusionsWe propose that regulators of branched and linear F-actin cooperate to establish dendritic branches. By combining our work with existing literature, we propose that the dendrite guidance receptor DMA-1 recruits the WRC, which polymerizes branched F-actin to generate "swellings" on a mother dendrite. Then, WRC recruits the actin elongation factor UNC-34/Ena/VASP to initiate growth of a new dendritic branch from the swelling, with the help of the actin-binding protein UNC-115/abLIM. Extension of existing dendrites also proceeds via swelling formation at the dendrite tip followed by UNC-34-mediated outgrowth. Following dendrite initiation and extension, the stabilization of branches by guidance receptors further recruits WRC, resulting in an iterative process to build a complex dendritic arbor.

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Actin blobs prefigure dendrite branching sites.

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Actin blobs prefigure dendrite branching sites.

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