Optical imaging reveals cation--Cl(-) cotransporter-mediated transient rapid decrease in intracellular Cl(-) concentration induced by oxygen--glucose deprivation in rat neocortical slices

Neurosci Res. 2001 Mar;39(3):269-80. doi: 10.1016/s0168-0102(00)00221-2.

Abstract

In brain slices from young (postnatal day (P) 10--15) rat somatosensory cortex, real-time neuronal intracellular Cl(-) concentration ([Cl(-)](i)) recordings were made by an optical technique measuring 6-methoxy-N-ethlquinolinium iodide (MEQ) fluorescence. Oxygen--glucose deprivation (in vitro model of ischemia) induced a long-lasting [Cl(-)](i) increase preceded by a rapid, transient [Cl(-)](i) decrease that could not be inhibited by blockers of Cl(-) pumps, Cl(-) channels, or Cl(-) antiporters, but was sensitive to cation-Cl(-) cotransporter inhibitors (bumetanide and furosemide). Use of low external Na(+) or high external K(+) revealed that the Na(+),K(+)-2Cl(-) cotransporter was inhibited by bumetanide and furosemide, whereas the K(+)-Cl(-) cotransporter was preferentially inhibited by furosemide under our experimental conditions. With a reduced inward driving force for Na(+) (reducing Na(+),K(+)-2Cl(-) cotransport), the transient [Cl(-)](i) decrease was only rarely induced by oxygen-glucose deprivation. In contrast, with a reduced outward driving force for K(+) (reducing K(+)-Cl(-) cotransport), the transient [Cl(-)](i) decrease still occurred. These results suggest that the transient [Cl(-)](i) decrease was primarily mediated by a rapid inhibition of the inwardly directed Na(+),K(+)-2Cl(-) cotransporter. Reverse transcriptase-polymerase chain reaction (RT-PCR) experiments suggested that the isoform involved is NKCC1. We hypothesize that the initial rapid Cl(-) efflux might effectively delay the irreversible Cl(-) influx that mediates neuronal injury.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / drug effects
  • Carrier Proteins / metabolism*
  • Cell Hypoxia / physiology
  • Chlorides / metabolism*
  • Fluorescent Dyes / pharmacokinetics
  • Glucose / deficiency
  • Ion Transport / drug effects
  • Ion Transport / physiology
  • Potassium / metabolism*
  • Pyramidal Cells / drug effects
  • Pyramidal Cells / metabolism*
  • Quinolinium Compounds / pharmacokinetics
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Wistar
  • Sodium / metabolism*
  • Sodium-Potassium-Chloride Symporters*
  • Somatosensory Cortex / drug effects
  • Somatosensory Cortex / metabolism*

Substances

  • Carrier Proteins
  • Chlorides
  • Fluorescent Dyes
  • Quinolinium Compounds
  • RNA, Messenger
  • SLC12A9 protein, human
  • Sodium-Potassium-Chloride Symporters
  • 6-methoxy-N-ethylquinolinium
  • Sodium
  • Glucose
  • Potassium