Mechanisms underlying the neuronal calcium sensor-1-evoked enhancement of exocytosis in PC12 cells

J Biol Chem. 2002 Aug 16;277(33):30315-24. doi: 10.1074/jbc.M201132200. Epub 2002 May 28.

Abstract

Neuronal calcium sensor-1 (NCS-1) or the originally identified homologue frequenin belongs to a superfamily of EF-hand calcium binding proteins. Although NCS-1 is thought to enhance synaptic efficacy or exocytosis mainly by activating ion channel function, the detailed molecular basis for the enhancement is still a matter of debate. Here, mechanisms underlying the NCS-1-evoked enhancement of exocytosis were investigated using PC12 cells overexpressing NCS-1. NCS-1 was found to have a broad distribution in the cells being partially distributed in the cytosol and associated to vesicles and tubular-like structures. Biochemical and immunohistochemical studies indicated that NCS-1 partially colocalized with the light synaptic vesicle marker synaptophysin. When stimulated with UTP or bradykinin, agonists to phospholipase C-linked receptors, NCS-1 enhanced the agonist-mediated elementary and global Ca2+ signaling and increased the levels of downstream signals of phosphatidylinositol 4-kinase. NCS-1 enhanced the UTP-evoked exocytosis but not the depolarization-evoked Ca2+ responses or exocytosis, suggesting that the enhancement by NCS-1 should involve phospholipase C-linked receptor-mediated signals rather than the Ca2+ channels or exocytotic machinery per se. Taken together, NCS-1 enhances phosphoinositide turnover, resulting in enhancement of Ca2+ signaling and exocytosis. This is a novel regulatory mechanism of exocytosis that might involve the activation of phosphatidylinositol 4-kinase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bradykinin / pharmacology
  • Calcium / metabolism
  • Calcium-Binding Proteins / metabolism
  • Calcium-Binding Proteins / physiology*
  • Exocytosis / physiology*
  • Fluorescent Antibody Technique
  • Neuronal Calcium-Sensor Proteins
  • Neuropeptides / metabolism
  • Neuropeptides / physiology*
  • PC12 Cells
  • Phosphatidylinositols / metabolism
  • Potassium / pharmacology
  • Rats
  • Signal Transduction
  • Subcellular Fractions / metabolism
  • Uridine Triphosphate / pharmacology

Substances

  • Calcium-Binding Proteins
  • Neuronal Calcium-Sensor Proteins
  • Neuropeptides
  • Phosphatidylinositols
  • frequenin calcium sensor proteins
  • Potassium
  • Bradykinin
  • Calcium
  • Uridine Triphosphate