Positive shifts of the GABAA receptor reversal potential due to altered chloride homeostasis is widespread after status epilepticus

Epilepsia. 2011 Sep;52(9):1570-8. doi: 10.1111/j.1528-1167.2011.03247.x.

Abstract

Purpose: γ-Aminobutyric acid (GABA)ergic transmission plays an important role in the initiation of epileptic activity and the generation of ictal discharges. The functional alterations in the epileptiform hippocampus critically depend on GABAergic mechanisms and cation-chloride cotransporters.

Methods: To understand the cellular basis of specific functional alterations in the epileptic hippocampus, we studied physiologic characteristics and pharmacologically isolated evoked GABA(A) receptor-mediated inhibitory postsynaptic currents (IPSCs) recorded from principal neurons in hippocampal slices from status epilepticus (SE) and control rats using whole-cell and gramicidin perforated patch-clamp recordings.

Key findings: Whereas the resting membrane potential and input resistance were not significantly different between control and epileptic tissue, the reversal potential (E(GABA) ) of IPSCs was significantly shifted to more positive values in SE rats with regard to the resting membrane potential. Pharmacologic experiments and quantitative reverse transcriptase polymerase chain reaction (RT-PCR) showed that the observed changes in the epileptic tissue were due to a decreased ratio of the main Cl(-) extrusion transporter (K(+) -Cl(-) cotransporter, KCC2) to the main Cl(-) uptake transporter (Na(+) -K(+) -2Cl(-) cotransporter, NKCC1).

Significance: Our results suggest that alterations of cation-chloride cotransporter functions, comprising a higher NKCC1 action, contribute to hyperexcitability within the hippocampus following SE.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2-Amino-5-phosphonovalerate / pharmacology
  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Analysis of Variance
  • Animals
  • Biophysical Phenomena / drug effects
  • Bumetanide / pharmacology
  • Chlorides / metabolism*
  • Disease Models, Animal
  • Drug Interactions
  • Electric Stimulation / methods
  • Excitatory Amino Acid Antagonists / pharmacology
  • Furosemide / pharmacology
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology
  • Hippocampus / pathology
  • Homeostasis / drug effects
  • Homeostasis / physiology*
  • In Vitro Techniques
  • Inhibitory Postsynaptic Potentials / drug effects
  • K Cl- Cotransporters
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology*
  • Neurons / drug effects
  • Neurons / metabolism*
  • Patch-Clamp Techniques
  • Pilocarpine
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Wistar
  • Receptors, GABA-A / genetics
  • Receptors, GABA-A / metabolism*
  • Sodium Potassium Chloride Symporter Inhibitors / pharmacology
  • Status Epilepticus / chemically induced
  • Status Epilepticus / metabolism*
  • Status Epilepticus / pathology
  • Symporters / genetics
  • Symporters / metabolism

Substances

  • Chlorides
  • Excitatory Amino Acid Antagonists
  • RNA, Messenger
  • Receptors, GABA-A
  • Sodium Potassium Chloride Symporter Inhibitors
  • Symporters
  • Pilocarpine
  • Bumetanide
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • 2-Amino-5-phosphonovalerate
  • Furosemide