New Role of ATM in Controlling GABAergic Tone During Development

Cereb Cortex. 2016 Oct;26(10):3879-88. doi: 10.1093/cercor/bhw125. Epub 2016 May 10.

Abstract

The capacity to guarantee the proper excitatory/inhibitory balance is one of the most critical steps during early development responsible for the correct brain organization, function, and plasticity. GABAergic neurons guide this process leading to the right structural organization, brain circuitry, and neuronal firing. Here, we identified the ataxia telangiectasia mutated (ATM), a serine/threonine protein kinase linked to DNA damage response, as crucial in regulating neurotransmission. We found that reduced levels of ATM in the hippocampal neuronal cultures produce an excitatory/inhibitory unbalance toward inhibition as indicated by the higher frequency of miniature inhibitory postsynaptic current events and an increased number of GABAergic synapses. In vivo, the increased inhibition still persists and, even if a higher excitation is also present, a reduced neuronal excitability is found as indicated by the lower action potential frequency generated in response to high-current intensity stimuli. Finally, we found an elevated extracellular signal-regulated kinase 1/2 (ERK1/2) phosphorylation in heterozygous hippocampi associated with lower expression levels of the ERK1/2 phosphatase PP1. Given that the neurodegenerative condition associated with genetic mutations in the Atm gene, ataxia telangiectasia, presents a variable phenotype with impairment in cognition, our molecular findings provide a logical frame for a more clear comprehension of cognitive defects in the pathology, opening to novel therapeutic strategies.

Keywords: ATM; KCC2; hippocampus; kinase–phosphatase cycle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism
  • Cells, Cultured
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Hippocampus / cytology
  • Hippocampus / embryology
  • Hippocampus / metabolism*
  • K Cl- Cotransporters
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neural Inhibition / physiology
  • Neurons / cytology
  • Neurons / metabolism*
  • Phosphorylation
  • Symporters / metabolism
  • Synaptic Transmission / physiology*
  • Tissue Culture Techniques
  • gamma-Aminobutyric Acid / administration & dosage
  • gamma-Aminobutyric Acid / metabolism*

Substances

  • Symporters
  • gamma-Aminobutyric Acid
  • Ataxia Telangiectasia Mutated Proteins
  • Atm protein, mouse
  • Extracellular Signal-Regulated MAP Kinases