Modulation of heteromeric P2X1/5 receptors by phosphoinositides in astrocytes depends on the P2X1 subunit

J Neurochem. 2010 Jun;113(6):1676-84. doi: 10.1111/j.1471-4159.2010.06734.x. Epub 2010 Apr 3.

Abstract

Purinergic signaling is critical for neuron-glia communication. Glial cells participate in synaptic transmission and express metabotropic P2Y as well as ionotropic P2X ATP receptors. In astrocytes, endogenous ATP-evoked currents with kinetics and pharmacology characteristic of the heteromeric P2X1/5 receptor channel have recently been reported. We investigated the interaction of major phosphoinositides with heteromeric P2X1/5 channels. Using patch-clamp electrophysiology on enhanced green fluorescent protein-expressing astrocytes acutely isolated from cortical slices of transgenic mice, we report a strong modulation of P2X1/5-like currents by phosphoinositides. Wortmannin-induced depletion of phosphoinositides decreases the amplitude of both the fast and sustained component of the P2X1/5-like currents although recovery and kinetics remain intact. In transfected human embryonic kidney cells, we provide evidence that depleting phosphatidylinositol 4,5-bisphosphate [PI(4,5)P(2)] levels significantly decreases P2X1/5 currents while intracellular application of PI(4,5)P(2) completely rescued P2X1/5 currents, ruling out the involvement of phosphatidylinositol 3,4,5-trisphosphate. In contrast to P2X1, homomeric P2X5 current responses were found insensitive to phosphoinositides, and the C-terminus of P2X5 subunit lacked binding to phospholipids in an overlay assay. Our results suggest that the contribution of calcium-permeable heteromeric P2X1/5 receptor channels to the excitability of astrocytes is modulated by PI(4,5)P(2) through the P2X1 lipid-binding domain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / analogs & derivatives
  • Adenosine Triphosphate / pharmacology
  • Androstadienes / pharmacology
  • Animals
  • Animals, Newborn
  • Astrocytes
  • Brain / cytology
  • Cell Line, Transformed
  • Dose-Response Relationship, Drug
  • Electric Stimulation / methods
  • Enzyme Inhibitors / pharmacology
  • Glial Fibrillary Acidic Protein / genetics
  • Green Fluorescent Proteins / genetics
  • Humans
  • Membrane Lipids / metabolism
  • Membrane Potentials / drug effects
  • Membrane Potentials / genetics
  • Mice
  • Mice, Transgenic
  • Patch-Clamp Techniques / methods
  • Phosphatidylinositol 4,5-Diphosphate / pharmacology
  • Phosphatidylinositols / metabolism*
  • Rats
  • Receptors, Purinergic P2 / genetics
  • Receptors, Purinergic P2 / metabolism*
  • Receptors, Purinergic P2X
  • Receptors, Purinergic P2X5
  • Transfection / methods
  • Wortmannin

Substances

  • Androstadienes
  • Enzyme Inhibitors
  • Glial Fibrillary Acidic Protein
  • Membrane Lipids
  • P2RX5 protein, human
  • P2rx5 protein, mouse
  • Phosphatidylinositol 4,5-Diphosphate
  • Phosphatidylinositols
  • Receptors, Purinergic P2
  • Receptors, Purinergic P2X
  • Receptors, Purinergic P2X5
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins
  • Adenosine Triphosphate
  • alpha,beta-methyleneadenosine 5'-triphosphate
  • Wortmannin