Na+/H+ exchanger 1 is regulated via its lipid-interacting domain, which functions as a molecular switch: a pharmacological approach using indolocarbazole compounds

Mol Pharmacol. 2014 Jan;85(1):18-28. doi: 10.1124/mol.113.089268. Epub 2013 Oct 17.

Abstract

The plasma membrane Na(+)/H(+) exchanger 1 (NHE1) is rapidly activated in response to various stimuli. The membrane-proximal cytoplasmic region (∼60 residues), termed the lipid-interacting domain (LID), is an important regulatory domain of NHE1. Here, we used a pharmacological approach to further characterize the role of LID in the regulation of NHE1. Pharmacological analysis using staurosporine-like indolocarbazole and bisindolylmaleimide compounds suggested that the phorbol ester- and receptor agonist-induced activation of NHE1 occurs through a protein kinase C-independent mechanism. In particular, only indolocarbazole compounds that inhibited NHE1 activation were able to interact with the LID, suggesting that the inhibition of NHE1 activation is achieved through the direct action of these compounds on the LID. Furthermore, in addition to phorbol esters and a receptor agonist, okadaic acid and hyperosmotic stress, which are known to activate NHE1 through unknown mechanisms, were found to promote membrane association of the LID concomitant with NHE1 activation; these effects were inhibited by staurosporine, as well as by a mutation in the LID. Binding experiments using the fluorescent ATP analog trinitrophenyl ATP revealed that ATP and the NHE1 activator phosphatidylinositol 4,5-bisphosphate bind competitively to the LID. These findings suggest that modulation of NHE1 activity by various activators and inhibitors occurs through the direct binding of these molecules to the LID, which alters the association of the LID with the plasma membrane.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenergic alpha-1 Receptor Agonists / pharmacology
  • Animals
  • Binding, Competitive
  • Carbazoles / chemistry
  • Carbazoles / pharmacology*
  • Cation Transport Proteins / antagonists & inhibitors
  • Cation Transport Proteins / chemistry
  • Cation Transport Proteins / genetics
  • Cation Transport Proteins / metabolism*
  • Cell Membrane
  • Cricetinae
  • Cricetulus
  • Databases, Chemical
  • Indoles / chemistry
  • Indoles / pharmacology*
  • Lipids / chemistry*
  • Maleimides / chemistry
  • Maleimides / pharmacology*
  • Mice
  • Mutation
  • Okadaic Acid / pharmacology
  • Osmotic Pressure
  • Phosphatidylinositol 4,5-Diphosphate / pharmacology
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / metabolism
  • Protein Kinase Inhibitors / chemistry
  • Protein Kinase Inhibitors / pharmacology*
  • Protein Structure, Tertiary
  • Protein Transport
  • Receptors, Adrenergic, alpha-1 / genetics
  • Receptors, Adrenergic, alpha-1 / metabolism
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers / antagonists & inhibitors
  • Sodium-Hydrogen Exchangers / chemistry
  • Sodium-Hydrogen Exchangers / genetics
  • Sodium-Hydrogen Exchangers / metabolism*
  • Staurosporine / chemistry
  • Staurosporine / pharmacology
  • Transfection

Substances

  • Adrenergic alpha-1 Receptor Agonists
  • Carbazoles
  • Cation Transport Proteins
  • Indoles
  • Lipids
  • Maleimides
  • Phosphatidylinositol 4,5-Diphosphate
  • Protein Kinase Inhibitors
  • Receptors, Adrenergic, alpha-1
  • SLC9A1 protein, human
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers
  • Okadaic Acid
  • Protein Kinase C
  • Staurosporine