A novel Ca2+-induced Ca2+ release mechanism in A7r5 cells regulated by calmodulin-like proteins

J Biol Chem. 2003 Jul 25;278(30):27548-55. doi: 10.1074/jbc.M302026200. Epub 2003 May 13.

Abstract

Intracellular Ca2+ release is involved in setting up Ca2+ signals in all eukaryotic cells. Here we report that an increase in free Ca2+ concentration triggered the release of up to 41 +/- 3% of the intracellular Ca2+ stores in permeabilized A7r5 (embryonic rat aorta) cells with an EC50 of 700 nm. This type of Ca2+-induced Ca2+ release (CICR) was neither mediated by inositol 1,4,5-trisphosphate receptors nor by ryanodine receptors, because it was not blocked by heparin, 2-aminoethoxydiphenyl borate, xestospongin C, ruthenium red, or ryanodine. ATP dose-dependently stimulated the CICR mechanism, whereas 10 mm MgCl2 abolished it. CICR was not affected by exogenously added calmodulin (CaM), but CaM1234, a Ca2+-insensitive CaM mutant, strongly inhibited the CICR mechanism. Other proteins of the CaM-like neuronal Ca2+-sensor protein family such as Ca2+-binding protein 1 and neuronal Ca2+ sensor-1 were equally potent for inhibiting the CICR. Removal of endogenous CaM, using a CaM-binding peptide derived from the ryanodine receptor type-1 (amino acids 3614-3643) prevented subsequent activation of the CICR mechanism. A similar CICR mechanism was also found in 16HBE14o-(human bronchial mucosa) cells. We conclude that A7r5 and 16HBE14o-cells express a novel type of CICR mechanism that is silent in normal resting conditions due to inhibition by CaM but becomes activated by a Ca2+-dependent dissociation of CaM. This CICR mechanism, which may be regulated by members of the family of neuronal Ca2+-sensor proteins, may provide an additional route for Ca2+ release that could allow amplification of small Ca2+ signals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / pharmacology
  • Amino Acid Motifs
  • Animals
  • Calcium / metabolism*
  • Calmodulin / metabolism*
  • Cells, Cultured
  • Cloning, Molecular
  • Dose-Response Relationship, Drug
  • Humans
  • Magnesium / metabolism
  • Mice
  • Peptide Biosynthesis
  • Protein Structure, Tertiary
  • Rats
  • Ryanodine Receptor Calcium Release Channel / metabolism
  • Signal Transduction
  • Time Factors

Substances

  • Calmodulin
  • Ryanodine Receptor Calcium Release Channel
  • Adenosine Triphosphate
  • Magnesium
  • Calcium