Control of calcium signal propagation to the mitochondria by inositol 1,4,5-trisphosphate-binding proteins

J Biol Chem. 2005 Apr 1;280(13):12820-32. doi: 10.1074/jbc.M411591200. Epub 2005 Jan 11.

Abstract

Cytosolic Ca2+ ([Ca2+]c) signals triggered by many agonists are established through the inositol 1,4,5-trisphosphate (IP3) messenger pathway. This pathway is believed to use Ca2+-dependent local interactions among IP3 receptors (IP3R) and other Ca2+ channels leading to coordinated Ca2+ release from the endoplasmic reticulum throughout the cell and coupling Ca2+ entry and mitochondrial Ca2+ uptake to Ca2+ release. To evaluate the role of IP3 in the local control mechanisms that support the propagation of [Ca2+]c waves, store-operated Ca2+ entry, and mitochondrial Ca2+ uptake, we used two IP3-binding proteins (IP3BP): 1) the PH domain of the phospholipase C-like protein, p130 (p130PH); and 2) the ligand-binding domain of the human type-I IP3R (IP3R224-605). As expected, p130PH-GFP and GFP-IP3R224-605 behave as effective mobile cytosolic IP3 buffers. In COS-7 cells, the expression of IP3BPs had no effect on store-operated Ca2+ entry. However, the IP3-linked [Ca2+]c signal appeared as a regenerative wave and IP3BPs slowed down the wave propagation. Most importantly, IP3BPs largely inhibited the mitochondrial [Ca2+] signal and decreased the relationship between the [Ca2+]c and mitochondrial [Ca2+] signals, indicating disconnection of the mitochondria from the [Ca2+]c signal. These data suggest that IP3 elevations are important to regulate the local interactions among IP3Rs during propagation of [Ca2+]c waves and that the IP3-dependent synchronization of Ca2+ release events is crucial for the coupling between Ca2+ release and mitochondrial Ca2+ uptake.

Publication types

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

MeSH terms

  • Animals
  • COS Cells
  • Calcium / metabolism*
  • Carrier Proteins / metabolism
  • Cell Line, Tumor
  • Endoplasmic Reticulum / metabolism
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Ligands
  • Microscopy, Confocal
  • Microscopy, Fluorescence
  • Mitochondria / metabolism*
  • Protein Binding
  • Rats
  • Recombinant Proteins / chemistry
  • Signal Transduction
  • Spectrometry, Fluorescence
  • Time Factors
  • Transfection

Substances

  • Carrier Proteins
  • Ligands
  • Plcl1 protein, rat
  • Recombinant Proteins
  • Green Fluorescent Proteins
  • Inositol 1,4,5-Trisphosphate
  • Calcium