Processive flow by biased polymerization mediates the slow axonal transport of actin

Chakrabarty, Nilaj; Dubey, P K; Tang, Yong; Ganguly, Archan; Ladt, Kelsey; Leterrier, Christophe; Jung, P.; Roy, Subhojit

doi:10.1083/jcb.201711022

Cited by 28 publications

(36 citation statements)

References 70 publications

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“…Farina et al [6] described that centrosomal F-actin polymerization is Arp2/3 dependent. In contrast, we found that formins but not Arp2/3 contribute to the somatic F-actin organization in neurons, as shown for axonal Factin organization of mature neurons [42,43]. Furthermore, a novel actin network was described, which mediates long-range vesicle transport and asymmetric oocyte division [46,47].…”

Section: Discussionmentioning

confidence: 63%

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Radial somatic F‐actin organization affects growth cone dynamics during early neuronal development

et al. 2019

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The centrosome is thought to be the major neuronal microtubule‐organizing center (MTOC) in early neuronal development, producing microtubules with a radial organization. In addition, albeit in vitro, recent work showed that isolated centrosomes could serve as an actin‐organizing center, raising the possibility that neuronal development may, in addition, require a centrosome‐based actin radial organization. Here, we report, using super‐resolution microscopy and live‐cell imaging of cultured rodent neurons, F‐actin organization around the centrosome with dynamic F‐actin aster‐like structures with F‐actin fibers extending and retracting actively. Photoactivation/photoconversion experiments and molecular manipulations of F‐actin stability reveal a robust flux of somatic F‐actin toward the cell periphery. Finally, we show that somatic F‐actin intermingles with centrosomal PCM‐1 (pericentriolar material 1 protein) satellites. Knockdown of PCM‐1 and disruption of centrosomal activity not only affect F‐actin dynamics near the centrosome but also in distal growth cones. Collectively, the data show a radial F‐actin organization during early neuronal development, which might be a cellular mechanism for providing peripheral regions with a fast and continuous source of actin polymers, hence sustaining initial neuronal development.

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Section: Discussionmentioning

confidence: 63%

“…It was previously shown that axons of mature neurons contain F‐actin “hotspots” which are the source of dynamic actin trails . Importantly, Ganguly et al showed that the activity of axonal F‐actin “hotspots” correlates with stationary endosomes and are Formins‐dependent.…”

Section: Resultsmentioning

confidence: 99%

Radial somatic F‐actin organization affects growth cone dynamics during early neuronal development

et al. 2019

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“…More recently, an anterograde F-actin flow was described during neuronal migration (He, Zhang, Guan, Xia, & Yuan, 2010;Solecki et al, 2009) and at the base of the growth cones (Burnette et al, 2008). Importantly, using high-resolution microscopy techniques, it was demonstrated that mature axonal shafts contain actin "hotspots" and "trails," which contribute to axon anterograde actin transport (Chakrabarty et al, 2019;Ganguly et al, 2015). Altogether, these studies suggest a strong centrifugal component to the neuronal F-actin organization, in addition to the existing local assembly of filaments of F-actin in the growth cones.…”

Section: Centrosome As An F-actin Organization Center During Early mentioning

confidence: 99%

Emerging roles of the centrosome in neuronal development

2020

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The role of the centrosome—a microtubule‐organizing center—in neuronal development has been under scrutiny and is controversial. The function and position of the centrosome have been shown to play an important role in selecting the position of axon outgrowth in cultured neurons and in situ. However, other studies have shown that axonal growth is independent of centrosomal functions. Recent discoveries define the centrosome as an F‐actin organizing organelle in various cell types; thus, giving a whole new perspective to the role of the centrosome in lymphocyte polarity, cell division, and neuronal development. These discoveries compel the need to revisit centrosomal functions by investigating the fundamental mechanisms that regulate centrosomal F‐actin remodeling during neuronal differentiation and polarization. In this review, we summarize the up‐to‐date knowledge regarding the function of the centrosome in neuronal differentiation. We put special emphasis on recent findings describing the centrosome as an F‐actin organizing center. Additionally, with the available data regarding centrosome, microtubules and F‐actin organization, we provide a model on how centrosomal F‐actin could be modulating neuronal differentiation and polarity.

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“…We have been using STORM since 2013, then DNA-PAINT to study the organization of the axonal cytoskeleton Papandréou and Leterrier, 2018), resolving the architecture of axonal actin and spectrins (Ganguly et al, 2015;C. Y.-M. Huang et al, 2017;Leterrier et al, 2015) as well as the mechanisms of slow axonal transport (Chakrabarty et al, 2019;Ganguly et al, 2017). We have also helped developing SMLM imaging modalities and analysis strategies (Culley et al, 2018;Laine et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

About samples, giving examples: Optimized Single Molecule Localization Microscopy

Jimenez

Friedl

Leterrier

2019

Preprint

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Super-resolution microscopy has profoundly transformed how we study the architecture of cells, revealing unknown structures and refining our view of cellular assemblies. Among the various techniques, the resolution of Single Molecule Localization Microscopy (SMLM) can reach the size of macromolecular complexes and offer key insights on their nanoscale arrangement in situ. SMLM is thus a demanding technique and taking advantage of its full potential requires specifically optimized procedures. Here we describe how we perform the successive steps of an SMLM workflow, focusing on single-color Stochastic Optical Reconstruction Microscopy (STORM) as well as multicolor DNA Points Accumulation for imaging in Nanoscale Topography (DNA-PAINT) of fixed samples. We provide detailed procedures for careful sample fixation and immunostaining of typical cellular structures: cytoskeleton, clathrin-coated pits, and organelles. We then offer guidelines for optimal imaging and processing of SMLM data in order to optimize reconstruction quality and avoid the generation of artifacts. We hope that the tips and tricks we discovered over the years and detail here will be useful for researchers looking to make the best possible SMLM images, a pre-requisite for meaningful biological discovery.

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Processive flow by biased polymerization mediates the slow axonal transport of actin

Cited by 28 publications

References 70 publications

Radial somatic F‐actin organization affects growth cone dynamics during early neuronal development

Radial somatic F‐actin organization affects growth cone dynamics during early neuronal development

Emerging roles of the centrosome in neuronal development

About samples, giving examples: Optimized Single Molecule Localization Microscopy

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