The spatial distribution of inositol 1,4,5-trisphosphate receptor isoforms shapes Ca2+ waves

J Biol Chem. 2007 Mar 30;282(13):10057-10067. doi: 10.1074/jbc.M700746200. Epub 2007 Feb 6.

Abstract

Cytosolic Ca(2+) is a versatile second messenger that can regulate multiple cellular processes simultaneously. This is accomplished in part through Ca(2+) waves and other spatial patterns of Ca(2+) signals. To investigate the mechanism responsible for the formation of Ca(2+) waves, we examined the role of inositol 1,4,5-trisphosphate receptor (InsP3R) isoforms in Ca(2+) wave formation. Ca(2+) signals were examined in hepatocytes, which express the type I and II InsP3R in a polarized fashion, and in AR4-2J cells, a nonpolarized cell line that expresses type I and II InsP3R in a ratio similar to what is found in hepatocytes but homogeneously throughout the cell. Expression of type I or II InsP3R was selectively suppressed by isoform-specific DNA antisense in an adenoviral delivery system, which was delivered to AR4-2J cells in culture and to hepatocytes in vivo. Loss of either isoform inhibited Ca(2+) signals to a similar extent in AR4-2J cells. In contrast, loss of the basolateral type I InsP3R decreased the sensitivity of hepatocytes to vasopressin but had little effect on the initiation or spread of Ca(2+) waves across hepatocytes. Loss of the apical type II isoform caused an even greater decrease in the sensitivity of hepatocytes to vasopressin and resulted in Ca(2+) waves that were much slower and delayed in onset. These findings provide evidence that the apical concentration of type II InsP3Rs is essential for the formation of Ca(2+) waves in hepatocytes. The subcellular distribution of InsP3R isoforms may critically determine the repertoire of spatial patterns of Ca(2+) signals.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Calcium Channels / chemistry*
  • Calcium Channels / genetics
  • Calcium Channels / physiology*
  • Calcium Signaling / physiology*
  • Cells, Cultured
  • Hepatocytes / metabolism
  • Inositol 1,4,5-Trisphosphate Receptors / chemistry*
  • Inositol 1,4,5-Trisphosphate Receptors / genetics
  • Inositol 1,4,5-Trisphosphate Receptors / physiology*
  • Membrane Glycoproteins / chemistry*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / physiology*
  • Molecular Sequence Data
  • Protein Isoforms / chemistry
  • Protein Isoforms / physiology
  • Rats
  • Receptors, Cytoplasmic and Nuclear / chemistry*
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / physiology*
  • Vasopressins / physiology

Substances

  • Calcium Channels
  • ITPR2 protein, rat
  • Inositol 1,4,5-Trisphosphate Receptors
  • Itpr1 protein, rat
  • Membrane Glycoproteins
  • Protein Isoforms
  • Receptors, Cytoplasmic and Nuclear
  • Vasopressins