Hormone-induced calcium oscillations depend on cross-coupling with inositol 1,4,5-trisphosphate oscillations

Cell Rep. 2014 Nov 20;9(4):1209-18. doi: 10.1016/j.celrep.2014.10.033. Epub 2014 Nov 13.

Abstract

Receptor-mediated oscillations in cytosolic Ca(2+) concentration ([Ca(2+)]i) could originate either directly from an autonomous Ca(2+) feedback oscillator at the inositol 1,4,5-trisphosphate (IP3) receptor or as a secondary consequence of IP3 oscillations driven by Ca(2+) feedback on IP3 metabolism. It is challenging to discriminate these alternatives, because IP3 fluctuations could drive Ca(2+) oscillations or could just be a secondary response to the [Ca(2+)]i spikes. To investigate this problem, we constructed a recombinant IP3 buffer using type-I IP3 receptor ligand-binding domain fused to GFP (GFP-LBD), which buffers IP3 in the physiological range. This IP3 buffer slows hormone-induced [IP3] dynamics without changing steady-state [IP3]. GFP-LBD perturbed [Ca(2+)]i oscillations in a dose-dependent manner: it decreased both the rate of [Ca(2+)]i rise and the speed of Ca(2+) wave propagation and, at high levels, abolished [Ca(2+)]i oscillations completely. These data, together with computational modeling, demonstrate that IP3 dynamics play a fundamental role in generating [Ca(2+)]i oscillations and waves.

Publication types

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

MeSH terms

  • Animals
  • COS Cells
  • Calcium / pharmacology
  • Calcium Signaling / drug effects*
  • Chlorocebus aethiops
  • Computer Simulation
  • Green Fluorescent Proteins / metabolism
  • Hepatocytes / drug effects
  • Hepatocytes / metabolism
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Inositol 1,4,5-Trisphosphate Receptors / chemistry
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism
  • Ligands
  • Models, Biological
  • Protein Structure, Tertiary
  • Rats
  • Vasopressins / pharmacology*

Substances

  • Inositol 1,4,5-Trisphosphate Receptors
  • Ligands
  • Vasopressins
  • Green Fluorescent Proteins
  • Inositol 1,4,5-Trisphosphate
  • Calcium