Dual effect of insulin-like growth factor on the apical 70-pS K channel in the thick ascending limb of rat kidney

Am J Physiol Cell Physiol. 2004 Jun;286(6):C1258-63. doi: 10.1152/ajpcell.00441.2003.

Abstract

We used the patch-clamp technique to study the effect of insulin-like growth factor I (IGF-I) on the apical 70-pS K channel in the isolated thick ascending limb (TAL) of the rat kidney. The isolated TAL was cut open to gain access to the apical membrane. Addition of 25 nM IGF-I stimulates the apical 70-pS K channel and increases channel activity, defined by the product of channel open probability and channel number, from 0.31 to 1.21. The stimulatory effect of IGF-I is not mediated by nitric oxide- or protein tyrosine phosphatase-dependent mechanisms, because inhibition of nitric oxide synthase or blocking protein tyrosine phosphatase did not abolish the stimulatory effect of IGF-I on the 70-pS K channel. In contrast, inhibition of mitogen-activated protein (MAP) kinase with PD-98059 or U0126 abolished the stimulatory effect of IGF-I. This suggests that MAP kinase is responsible for mediating the effect of IGF-I on the apical K channels. Moreover, the effect of IGF-I on the apical 70-pS K channel is biphasic because high concentrations (>200 nM) inhibit apical 70-pS K channels. Application of 400 nM IGF-I decreased channel activity from 1.45 to 0.2. The inhibitory effect of IGF-I is not blocked by calphostin C (an inhibitor of PKC), but inhibition of protein tyrosine kinase with herbimycin A abolished the IGF-induced inhibition. We conclude that IGF-I has a dual effect on the apical 70-pS K channel in the TAL: low concentrations of IGF-I stimulate, whereas high concentrations inhibit the channel activity. The stimulatory effect of IGF-I is mediated by a MAP kinase-dependent pathway, whereas the inhibitory effect is the result of stimulation of protein tyrosine kinase.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism*
  • Cell Membrane Permeability / drug effects
  • Cell Membrane Permeability / physiology
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Insulin-Like Growth Factor I / metabolism
  • Insulin-Like Growth Factor I / pharmacology*
  • Loop of Henle / cytology
  • Loop of Henle / drug effects
  • Loop of Henle / metabolism*
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Patch-Clamp Techniques
  • Potassium / metabolism
  • Potassium Channels / drug effects
  • Potassium Channels / metabolism*
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Protein-Tyrosine Kinases / metabolism
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Enzyme Inhibitors
  • Potassium Channels
  • Insulin-Like Growth Factor I
  • Protein-Tyrosine Kinases
  • Protein Kinase C
  • Mitogen-Activated Protein Kinase 1
  • Potassium