Molecular Remodeling of the Presynaptic Active Zone of Drosophila Photoreceptors via Activity-Dependent Feedback

Neuron. 2015 May 6;86(3):711-25. doi: 10.1016/j.neuron.2015.03.046. Epub 2015 Apr 16.

Abstract

Neural activity contributes to the regulation of the properties of synapses in sensory systems, allowing for adjustment to a changing environment. Little is known about how synaptic molecular components are regulated to achieve activity-dependent plasticity at central synapses. Here, we found that after prolonged exposure to natural ambient light the presynaptic active zone in Drosophila photoreceptors undergoes reversible remodeling, including loss of Bruchpilot, DLiprin-α, and DRBP, but not of DSyd-1 or Cacophony. The level of depolarization of the postsynaptic neurons is critical for the light-induced changes in active zone composition in the photoreceptors, indicating the existence of a feedback signal. In search of this signal, we have identified a crucial role of microtubule meshwork organization downstream of the divergent canonical Wnt pathway, potentially via Kinesin-3 Imac. These data reveal that active zone composition can be regulated in vivo and identify the underlying molecular machinery.

Publication types

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

MeSH terms

  • Animals
  • Drosophila
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Feedback, Physiological / physiology*
  • Intracellular Signaling Peptides and Proteins
  • Ion Channels
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Mice, Transgenic
  • Microscopy, Electron, Transmission
  • Models, Biological
  • Phenotype
  • Phosphoproteins / metabolism
  • Photic Stimulation
  • Photoreceptor Cells, Invertebrate / classification
  • Photoreceptor Cells, Invertebrate / cytology*
  • Photoreceptor Cells, Invertebrate / metabolism
  • Presynaptic Terminals / physiology*
  • Presynaptic Terminals / ultrastructure
  • Signal Transduction / genetics
  • Synapses / physiology
  • Synapses / ultrastructure
  • TRPA1 Cation Channel
  • TRPC Cation Channels / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • BRP protein, Drosophila
  • Drosophila Proteins
  • GAL4 protein, Drosophila
  • Intracellular Signaling Peptides and Proteins
  • Ion Channels
  • Liprin-alpha protein, Drosophila
  • Luminescent Proteins
  • Phosphoproteins
  • TRPA1 Cation Channel
  • TRPC Cation Channels
  • Transcription Factors
  • TrpA1 protein, Drosophila