PlexinD1 signaling controls morphological changes and migration termination in newborn neurons

EMBO J. 2018 Feb 15;37(4):e97404. doi: 10.15252/embj.201797404. Epub 2018 Jan 18.

Abstract

Newborn neurons maintain a very simple, bipolar shape, while they migrate from their birthplace toward their destinations in the brain, where they differentiate into mature neurons with complex dendritic morphologies. Here, we report a mechanism by which the termination of neuronal migration is maintained in the postnatal olfactory bulb (OB). During neuronal deceleration in the OB, newborn neurons transiently extend a protrusion from the proximal part of their leading process in the resting phase, which we refer to as a filopodium-like lateral protrusion (FLP). The FLP formation is induced by PlexinD1 downregulation and local Rac1 activation, which coincide with microtubule reorganization and the pausing of somal translocation. The somal translocation of resting neurons is suppressed by microtubule polymerization within the FLP The timing of neuronal migration termination, controlled by Sema3E-PlexinD1-Rac1 signaling, influences the final positioning, dendritic patterns, and functions of the neurons in the OB These results suggest that PlexinD1 signaling controls FLP formation and the termination of neuronal migration through a precise control of microtubule dynamics.

Keywords: microtubule; neuronal migration; olfactory bulb; photoactivation; postnatal neurogenesis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Cell Movement*
  • Cell Surface Extensions / physiology*
  • Cells, Cultured
  • Cytoskeletal Proteins
  • Glycoproteins / genetics
  • Glycoproteins / metabolism
  • Intracellular Signaling Peptides and Proteins
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurogenesis*
  • Neurons / cytology*
  • Neurons / physiology*
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Semaphorins
  • Signal Transduction
  • rac1 GTP-Binding Protein / genetics
  • rac1 GTP-Binding Protein / metabolism

Substances

  • Cytoskeletal Proteins
  • Glycoproteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Glycoproteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Neuropeptides
  • Plxnd1 protein, mouse
  • Rac1 protein, mouse
  • Sema3e protein, mouse
  • Semaphorins
  • rac1 GTP-Binding Protein