Activation of inositol 1,4,5-trisphosphate receptor is essential for the opening of mouse TRP5 channels

Mol Pharmacol. 2001 Nov;60(5):989-98. doi: 10.1124/mol.60.5.989.

Abstract

We studied the opening mechanism of Ca(2+)-permeable channels formed with mouse transient receptor potential type 5 (mTRP5) using Xenopus oocytes. After stimulation of coexpressed muscarinic M(1) receptors with acetylcholine (ACh) in a Ca(2+)-free solution, switching to 2 mM Ca(2+)-containing solution evoked a large Cl(-) current, which reflects the opening of endogenous Ca(2+)-dependent Cl(-) channels following Ca(2+) entry through the expressed channels. The ACh-evoked response was not affected by a depletion of Ca(2+) store with thapsigargin but was inhibited by preinjection of antisense oligodeoxynucleotides (ODNs) to G(q), G(11), or both. The mTRP5 channel response was also induced by a direct activation of G proteins with injection of guanosine 5'-3-O-(thio)triphosphate (GTP gamma S). The ACh- and GTP gamma S-evoked responses were inhibited by either pretreatment with a phospholipase C inhibitor, U73122, or an inositol-1,4,5-trisphosphate (IP(3)) receptor inhibitor, xestospongin C (XeC). An activation of IP(3) receptors with injection of adenophostin A (AdA) evoked the mTRP5 channel response in a dose-dependent manner. The AdA-evoked response was not suppressed by preinjection of antisense ODNs to G(q/11) or U73122 but was suppressed by either preinjection of XeC or a peptide mimicking the IP(3) binding domain of Xenopus IP(3) receptor. These findings suggest that the activation of IP(3) receptor is essential for the opening of mTRP5 channels, and that neither G proteins, phosphoinositide metabolism, nor depletion of the Ca(2+) store directly modifies the IP(3) receptor-linked opening of mTRP5 channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / metabolism
  • Adenosine / analogs & derivatives*
  • Adenosine / pharmacology
  • Allosteric Regulation
  • Animals
  • Calcium / deficiency
  • Calcium / metabolism
  • Calcium Channel Agonists / pharmacology
  • Calcium Channels / drug effects
  • Calcium Channels / metabolism*
  • Calcium Channels / physiology
  • Cation Transport Proteins*
  • Electrophysiology
  • Estrenes / pharmacology
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • GTP-Binding Proteins / metabolism*
  • Guanosine 5'-O-(3-Thiotriphosphate) / metabolism
  • Heterotrimeric GTP-Binding Proteins / antagonists & inhibitors
  • Heterotrimeric GTP-Binding Proteins / genetics
  • Inositol 1,4,5-Trisphosphate / metabolism
  • Inositol 1,4,5-Trisphosphate Receptors
  • Macrocyclic Compounds
  • Mice
  • Nuclear Proteins / antagonists & inhibitors
  • Nuclear Proteins / genetics
  • Oligodeoxyribonucleotides, Antisense / pharmacology
  • Oocytes / drug effects
  • Oocytes / physiology
  • Oxazoles / pharmacology
  • Peptides / chemical synthesis
  • Peptides / chemistry
  • Peptides / pharmacology
  • Phosphodiesterase Inhibitors / pharmacology
  • Protein Serine-Threonine Kinases
  • Pyrrolidinones / pharmacology
  • Receptor, Muscarinic M1
  • Receptors, Cytoplasmic and Nuclear / antagonists & inhibitors
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Receptors, Muscarinic / metabolism
  • TRPC Cation Channels
  • Type C Phospholipases / antagonists & inhibitors
  • Type C Phospholipases / metabolism
  • Xenopus laevis

Substances

  • Calcium Channel Agonists
  • Calcium Channels
  • Cation Transport Proteins
  • Estrenes
  • ITPR1 protein, human
  • Inositol 1,4,5-Trisphosphate Receptors
  • Macrocyclic Compounds
  • Nuclear Proteins
  • Oligodeoxyribonucleotides, Antisense
  • Oxazoles
  • Peptides
  • Phosphodiesterase Inhibitors
  • Pyrrolidinones
  • Receptor, Muscarinic M1
  • Receptors, Cytoplasmic and Nuclear
  • Receptors, Muscarinic
  • TRPC Cation Channels
  • TRPC5 protein, human
  • Trpc5 protein, mouse
  • xestospongin A
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • adenophostin A
  • Guanosine 5'-O-(3-Thiotriphosphate)
  • Inositol 1,4,5-Trisphosphate
  • Protein Serine-Threonine Kinases
  • STK19 protein, human
  • Type C Phospholipases
  • GTP-Binding Proteins
  • GTP-Binding Protein alpha Subunits, Gq-G11
  • Heterotrimeric GTP-Binding Proteins
  • Adenosine
  • Acetylcholine
  • Calcium