Atypical Myosin Tunes Dendrite Arbor Subdivision

Neuron. 2020 May 6;106(3):452-467.e8. doi: 10.1016/j.neuron.2020.02.002. Epub 2020 Mar 9.

Abstract

Dendrite arbor pattern determines the functional characteristics of a neuron. It is founded on primary branch structure, defined through cell intrinsic and transcription-factor-encoded mechanisms. Developing arbors have extensive acentrosomal microtubule dynamics, and here, we report an unexpected role for the atypical actin motor Myo6 in creating primary branch structure by specifying the position, polarity, and targeting of these events. We carried out in vivo time-lapse imaging of Drosophila adult sensory neuron differentiation, integrating machine-learning-based quantification of arbor patterning with molecular-level tracking of cytoskeletal remodeling. This revealed that Myo6 and the transcription factor Knot regulate transient surges of microtubule polymerization at dendrite tips; they drive retrograde extension of an actin filament array that specifies anterograde microtubule polymerization and guides these microtubules to subdivide the tip into multiple branches. Primary branches delineate functional compartments; this tunable branching mechanism is key to define and diversify dendrite arbor compartmentalization.

Keywords: automated feature detection; automated neurite tracing; branching; dendrite; fascin; filopodia; growth cone; microtubule polarity; myosin; transcription factor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line
  • Cells, Cultured
  • Dendrites / metabolism*
  • Dendrites / physiology
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster
  • Microtubules / metabolism
  • Myosin Heavy Chains / genetics
  • Myosin Heavy Chains / metabolism*
  • Neurogenesis*
  • Transcription Factors / metabolism

Substances

  • Drosophila Proteins
  • Transcription Factors
  • kn protein, Drosophila
  • myosin VI
  • Myosin Heavy Chains