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J Cell Biol. 2019 Jan 7;218(1):112-124. doi: 10.1083/jcb.201711022. Epub 2018 Nov 6.

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

Author information

1
Department of Physics and Astronomy, Neuroscience Program and Quantitative Biology Institute, Ohio University, Athens, OH.
2
Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI.
3
Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, CA.
4
Department of Neurosciences, University of California, San Diego, La Jolla, CA.
5
Aix-Marseille Université, Centre National de la Recherche Scientifique, Institut Neurophysiopathol, NeuroCyto, Marseille, France christophe.leterrier@univ-amu.fr.
6
Department of Physics and Astronomy, Neuroscience Program and Quantitative Biology Institute, Ohio University, Athens, OH jungp@ohio.edu.
7
Department of Pathology and Laboratory Medicine, University of Wisconsin-Madison, Madison, WI roy27@wisc.edu.
8
Department of Neuroscience, University of Wisconsin-Madison, Madison, WI.

Abstract

Classic pulse-chase studies have shown that actin is conveyed in slow axonal transport, but the mechanistic basis for this movement is unknown. Recently, we reported that axonal actin was surprisingly dynamic, with focal assembly/disassembly events ("actin hotspots") and elongating polymers along the axon shaft ("actin trails"). Using a combination of live imaging, superresolution microscopy, and modeling, in this study, we explore how these dynamic structures can lead to processive transport of actin. We found relatively more actin trails elongated anterogradely as well as an overall slow, anterogradely biased flow of actin in axon shafts. Starting with first principles of monomer/filament assembly and incorporating imaging data, we generated a quantitative model simulating axonal hotspots and trails. Our simulations predict that the axonal actin dynamics indeed lead to a slow anterogradely biased flow of the population. Collectively, the data point to a surprising scenario where local assembly and biased polymerization generate the slow axonal transport of actin without involvement of microtubules (MTs) or MT-based motors. Mechanistically distinct from polymer sliding, this might be a general strategy to convey highly dynamic cytoskeletal cargoes.

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