Extrinsic activin signaling cooperates with an intrinsic temporal program to increase mushroom body neuronal diversity

Elife. 2020 Jul 6:9:e58880. doi: 10.7554/eLife.58880.

Abstract

Temporal patterning of neural progenitors leads to the sequential production of diverse neurons. To understand how extrinsic cues influence intrinsic temporal programs, we studied Drosophila mushroom body progenitors (neuroblasts) that sequentially produce only three neuronal types: γ, then α'β', followed by αβ. Opposing gradients of two RNA-binding proteins Imp and Syp comprise the intrinsic temporal program. Extrinsic activin signaling regulates the production of α'β' neurons but whether it affects the intrinsic temporal program was not known. We show that the activin ligand Myoglianin from glia regulates the temporal factor Imp in mushroom body neuroblasts. Neuroblasts missing the activin receptor Baboon have a delayed intrinsic program as Imp is higher than normal during the α'β' temporal window, causing the loss of α'β' neurons, a decrease in αβ neurons, and a likely increase in γ neurons, without affecting the overall number of neurons produced. Our results illustrate that an extrinsic cue modifies an intrinsic temporal program to increase neuronal diversity.

Keywords: D. melanogaster; Drosophila; activin; developmental biology; kenyon cells; mushroom body; myoglianin; neuroscience; temporal patterning.

Publication types

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

MeSH terms

  • Activins / metabolism*
  • Animals
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology*
  • Ligands
  • Mushroom Bodies / physiology*
  • Neural Stem Cells / physiology
  • Neurons / physiology*
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Signal Transduction*
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism

Substances

  • Drosophila Proteins
  • Imp protein, Drosophila
  • Ligands
  • RNA-Binding Proteins
  • Syp protein, Drosophila
  • Transforming Growth Factor beta
  • myo protein, Drosophila
  • Activins

Associated data

  • GEO/GSE71103