Serotonin-induced regulation of the actin network for learning-related synaptic growth requires Cdc42, N-WASP, and PAK in Aplysia sensory neurons

Neuron. 2005 Mar 24;45(6):887-901. doi: 10.1016/j.neuron.2005.01.044.

Abstract

Application of Clostridium difficile toxin B, an inhibitor of the Rho family of GTPases, at the Aplysia sensory to motor neuron synapse blocks long-term facilitation and the associated growth of new sensory neuron varicosities induced by repeated pulses of serotonin (5-HT). We have isolated cDNAs encoding Aplysia Rho, Rac, and Cdc42 and found that Rho and Rac had no effect but that overexpression in sensory neurons of a dominant-negative mutant of ApCdc42 or the CRIB domains of its downstream effectors PAK and N-WASP selectively reduces the long-term changes in synaptic strength and structure. FRET analysis indicates that 5-HT activates ApCdc42 in a subset of varicosities contacting the postsynaptic motor neuron and that this activation is dependent on the PI3K and PLC signaling pathways. The 5-HT-induced activation of ApCdc42 initiates reorganization of the presynaptic actin network leading to the outgrowth of filopodia, some of which are morphological precursors for the learning-related formation of new sensory neuron varicosities.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / drug effects
  • Actins / metabolism*
  • Amino Acid Sequence
  • Animals
  • Aplysia
  • Cells, Cultured
  • Conserved Sequence / genetics
  • Learning / drug effects
  • Learning / physiology*
  • Molecular Sequence Data
  • Motor Neurons / cytology
  • Motor Neurons / physiology
  • Mutation / genetics
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / isolation & purification
  • Nerve Tissue Proteins / metabolism
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Neurons, Afferent / cytology
  • Neurons, Afferent / drug effects
  • Neurons, Afferent / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / metabolism
  • Presynaptic Terminals / ultrastructure
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / isolation & purification
  • Protein Structure, Tertiary / genetics
  • Pseudopodia / metabolism
  • Serotonin / metabolism*
  • Serotonin / pharmacology
  • Synapses / drug effects
  • Synapses / metabolism*
  • Type C Phospholipases / metabolism
  • Wiskott-Aldrich Syndrome Protein, Neuronal
  • cdc42 GTP-Binding Protein / genetics
  • cdc42 GTP-Binding Protein / isolation & purification
  • cdc42 GTP-Binding Protein / metabolism
  • p21-Activated Kinases
  • rac GTP-Binding Proteins / genetics
  • rac GTP-Binding Proteins / isolation & purification
  • rac GTP-Binding Proteins / metabolism
  • rho GTP-Binding Proteins / genetics
  • rho GTP-Binding Proteins / isolation & purification
  • rho GTP-Binding Proteins / metabolism

Substances

  • Actins
  • Nerve Tissue Proteins
  • Wiskott-Aldrich Syndrome Protein, Neuronal
  • Serotonin
  • Protein Serine-Threonine Kinases
  • p21-Activated Kinases
  • Type C Phospholipases
  • cdc42 GTP-Binding Protein
  • rac GTP-Binding Proteins
  • rho GTP-Binding Proteins