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Cholesterol is required for activity-dependent synaptic growth.

Amber Shaheen1, Claire L Richter Gorey1, Adam Sghaier1

  • 1Department of Biomedical Sciences, University of Windsor, Windsor, Ontario, N9B 3P4, Canada.

Journal of Cell Science
|October 30, 2023
PubMed
Summary

Synaptic activity increases neuronal cholesterol, essential for synaptic growth and function. This cholesterol acts downstream of cAMP and influences protein kinase A activity, impacting neuronal development.

Keywords:
DrosophilaCholesterolLipidsPKAPresynaptic plasticitySynaptic activitycAMP

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Area of Science:

  • Neuroscience
  • Molecular Biology
  • Cell Biology

Background:

  • Neuronal membrane cholesterol levels change during development and aging.
  • The regulation of neuronal cholesterol by synaptic activity is poorly understood.
  • The impact of synaptic activity-induced cholesterol changes on neuronal development and function remains unclear.

Purpose of the Study:

  • To investigate whether synaptic activity regulates cholesterol levels in neuronal membranes.
  • To determine the role of synaptic activity-modulated cholesterol in neuronal development and function.
  • To elucidate the molecular pathway linking synaptic activity, cholesterol, and neuronal growth.

Main Methods:

  • Generated transgenic Drosophila expressing a cholesterol-binding domain to quantify presynaptic cholesterol.
  • Utilized genetic manipulations in Drosophila, including knockdown of adenylyl cyclase and phosphodiesterase activity.
  • Employed a protein kinase A (PKA) activity sensor in presynaptic terminals.

Main Results:

  • Increased synaptic activity led to elevated cholesterol levels in presynaptic terminals.
  • Reduced cholesterol impaired synaptic growth and activity-dependent growth.
  • Knocking down adenylyl cyclase mimicked cholesterol reduction effects, indicating a shared pathway.
  • Cholesterol acts downstream of cyclic adenosine monophosphate (cAMP) in this pathway.
  • Reduced cholesterol levels diminished presynaptic PKA activity.

Conclusions:

  • Enhanced synaptic activity increases presynaptic cholesterol levels.
  • Activity-dependent synaptic growth is regulated by cholesterol.
  • The cAMP-PKA signaling pathway is involved in activity-dependent synaptic growth, with cholesterol acting downstream of cAMP and influencing PKA activity.