Taurine inhibits K+-Cl- cotransporter KCC2 to regulate embryonic Cl- homeostasis via with-no-lysine (WNK) protein kinase signaling pathway

J Biol Chem. 2012 Jun 15;287(25):20839-50. doi: 10.1074/jbc.M111.319418. Epub 2012 Apr 27.

Abstract

GABA inhibits mature neurons and conversely excites immature neurons due to lower K(+)-Cl(-) cotransporter 2 (KCC2) expression. We observed that ectopically expressed KCC2 in embryonic cerebral cortices was not active; however, KCC2 functioned in newborns. In vitro studies revealed that taurine increased KCC2 inactivation in a phosphorylation-dependent manner. When Thr-906 and Thr-1007 residues in KCC2 were substituted with Ala (KCC2T906A/T1007A), KCC2 activity was facilitated, and the inhibitory effect of taurine was not observed. Exogenous taurine activated the with-no-lysine protein kinase 1 (WNK1) and downstream STE20/SPS1-related proline/alanine-rich kinase (SPAK)/oxidative stress response 1 (OSR1), and overexpression of active WNK1 resulted in KCC2 inhibition in the absence of taurine. Phosphorylation of SPAK was consistently higher in embryonic brains compared with that of neonatal brains and down-regulated by a taurine transporter inhibitor in vivo. Furthermore, cerebral radial migration was perturbed by a taurine-insensitive form of KCC2, KCC2T906A/T1007A, which may be regulated by WNK-SPAK/OSR1 signaling. Thus, taurine and WNK-SPAK/OSR1 signaling may contribute to embryonic neuronal Cl(-) homeostasis, which is required for normal brain development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Cell Line
  • Cerebral Cortex / cytology
  • Cerebral Cortex / embryology*
  • Embryo, Mammalian / cytology
  • Embryo, Mammalian / metabolism*
  • Homeostasis / drug effects
  • Homeostasis / physiology
  • K Cl- Cotransporters
  • Minor Histocompatibility Antigens
  • Mutation, Missense
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Neurons / cytology
  • Neurons / metabolism*
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Protein Kinases / genetics
  • Protein Kinases / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / immunology
  • Protein Serine-Threonine Kinases / metabolism
  • Rats
  • Rats, Wistar
  • Signal Transduction / drug effects*
  • Signal Transduction / physiology
  • Symporters / genetics
  • Symporters / metabolism*
  • Taurine / pharmacology*
  • WNK Lysine-Deficient Protein Kinase 1

Substances

  • Minor Histocompatibility Antigens
  • Nerve Tissue Proteins
  • Symporters
  • Taurine
  • Protein Kinases
  • PAS domain kinases
  • Oxsr1 protein, rat
  • Protein Serine-Threonine Kinases
  • WNK Lysine-Deficient Protein Kinase 1
  • Wnk1 protein, rat