TrkA mediates retrograde semaphorin 3A signaling through plexin A4 to regulate dendritic branching

J Cell Sci. 2016 May 1;129(9):1802-14. doi: 10.1242/jcs.184580. Epub 2016 Mar 4.

Abstract

Semaphorin 3A (Sema3A), a secretory semaphorin, exerts various biological actions through a complex between neuropilin-1 and plexin-As (PlexAs). Sema3A induces retrograde signaling, which is involved in regulating dendritic localization of GluA2 (also known as GRIA2), an AMPA receptor subunit. Here, we investigated a possible interaction between retrograde signaling pathways for Sema3A and nerve growth factor (NGF). Sema3A induces colocalization of PlexA4 (also known as PLXNA4) signals with those of tropomyosin-related kinase A (TrkA, also known as NTRK1) in growth cones, and these colocalized signals were then observed along the axons. The time-lapse imaging of PlexA4 and several TrkA mutants showed that the kinase and dynein-binding activity of TrkA were required for Sema3A-induced retrograde transport of the PlexA4-TrkA complex along the axons. The inhibition of the phosphoinositide 3-kinase (PI3K)-Akt signal, a downstream signaling pathway of TrkA, in the distal axon suppressed Sema3A-induced dendritic localization of GluA2. The knockdown of TrkA suppressed Sema3A-induced dendritic localization of GluA2 and that suppressed Sema3A-regulated dendritic branching both in vitro and in vivo These findings suggest that by interacting with PlexA4, TrkA plays a crucial role in redirecting local Sema3A signaling to retrograde axonal transport, thereby regulating dendritic GluA2 localization and patterning.

Keywords: Axonal transport; Hippocampus; NGF; PlexA4; Semaphorin 3A; TrkA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Avian Proteins / genetics
  • Avian Proteins / metabolism*
  • Chickens / genetics
  • Chickens / metabolism*
  • Female
  • Growth Cones / metabolism*
  • Humans
  • Male
  • Mice
  • Nerve Growth Factor / genetics
  • Nerve Growth Factor / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor, trkA / genetics
  • Receptor, trkA / metabolism*
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism*
  • Semaphorin-3A / genetics
  • Semaphorin-3A / metabolism*
  • Signal Transduction / physiology*

Substances

  • Avian Proteins
  • Nerve Tissue Proteins
  • Plxna4 protein, mouse
  • Receptors, Cell Surface
  • Semaphorin-3A
  • Nerve Growth Factor
  • Phosphatidylinositol 3-Kinases
  • Receptor, trkA
  • Proto-Oncogene Proteins c-akt