Synapse formation and mRNA localization in cultured Aplysia neurons

Neuron. 2006 Feb 2;49(3):349-56. doi: 10.1016/j.neuron.2005.12.029.

Abstract

mRNA localization and regulated translation provide a means of spatially restricting gene expression within neurons during axon guidance and long-term synaptic plasticity. Here we show that synapse formation specifically alters the localization of the mRNA encoding sensorin, a peptide neurotransmitter with neurotrophin-like properties. In isolated Aplysia sensory neurons, which do not form chemical synapses, sensorin mRNA is diffusely distributed throughout distal neurites. Upon contact with a target motor neuron, sensorin mRNA rapidly concentrates at synapses. This redistribution only occurs in the presence of a target motor neuron and parallels the distribution of sensorin protein. Reduction of sensorin mRNA, but not protein, with dsRNA inhibits synapse formation. Our results indicate that synapse formation can alter mRNA localization within individual neurons. They further suggest that translation of a specific localized mRNA, encoding the neuropeptide sensorin, is required for synapse formation between sensory and motor neurons.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Animals
  • Aplysia / cytology*
  • Blotting, Western / methods
  • Cells, Cultured
  • Coculture Techniques / methods
  • Dactinomycin / pharmacology
  • Diagnostic Imaging / methods
  • Electric Stimulation / methods
  • Electrophysiologic Techniques, Cardiac / methods
  • Excitatory Postsynaptic Potentials / physiology
  • Gene Expression Regulation / physiology
  • Green Fluorescent Proteins / metabolism
  • Immunohistochemistry / methods
  • In Situ Hybridization / methods
  • Microinjections / methods
  • Motor Neurons / metabolism
  • Motor Neurons / physiology
  • Neurites / drug effects
  • Neurites / metabolism
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / physiology*
  • Neurons / radiation effects
  • Neurons, Afferent / classification
  • Neurons, Afferent / cytology
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / physiology
  • Neurons, Afferent / radiation effects
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Potassium Chloride / pharmacology
  • Protein Synthesis Inhibitors / pharmacology
  • RNA, Double-Stranded / pharmacology
  • RNA, Messenger / metabolism*
  • Synapses / physiology*

Substances

  • Neuropeptides
  • Protein Synthesis Inhibitors
  • RNA, Double-Stranded
  • RNA, Messenger
  • sensorin A protein, Aplysia
  • Green Fluorescent Proteins
  • Dactinomycin
  • Potassium Chloride