Munc18-1 phosphorylation by protein kinase C potentiates vesicle pool replenishment in bovine chromaffin cells

Neuroscience. 2006 Dec 1;143(2):487-500. doi: 10.1016/j.neuroscience.2006.08.014. Epub 2006 Sep 25.

Abstract

Activation of protein kinase C (PKC) after robust stimulation is necessary for vesicle pool replenishment in secretory cells. Here we studied the contribution of a prominent downstream PKC target, Munc18-1, to this process in bovine chromaffin cells. In these cells, both activation of endogenous PKC and overexpressing of Munc18-1 promote vesicle pool replenishment after an extensive stimulation. In order to study the physiological relevance of PKC-dependent Munc18-1 phosphorylation, we generated two Munc18-1 phospho-mutants; one that mimics a constitutively PKC-phosphorylated Munc18-1 (i.e. a phosphomimetic mutant; Munc18-1(S313D)) and a second that cannot be PKC-phosphorylated (Munc18-1(3A)). Overexpression of Munc18-1(3A) caused a significant decrease in vesicle pool replenishment following a depleting stimulation, while Munc18-1(S313D) caused a significant increase in vesicle pool replenishment. These findings suggested that the phosphorylation of Munc18-1 by PKC potentiates vesicle pool replenishment. This hypothesis was further strengthened by the finding that overexpression of wild type Munc18-1 in the presence of a PKC inhibitor caused a significant reduction in vesicle pool replenishment, similar to that observed with Munc18-1(3A). Moreover, overexpression of Munc18-1(S313D) in the presence of the PKC inhibitor partly alleviated this attenuation, elucidating Munc18-1's unique contribution to vesicle pool replenishment. Finally, we demonstrate that Munc18-1 promotes vesicle docking in a phosphorylation-independent manner. This is deduced from the findings that both the wild type and the two Munc18-1 phospho-mutants enhanced docking to the same extent in bovine chromaffin cells. We conclude that Munc18-1 facilitates docking in a PKC phosphorylation-independent manner, and that its phosphorylation by PKC potentiates vesicle pool replenishment following a depleting stimulation, at a post-docking stage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adrenal Medulla / cytology
  • Animals
  • Aspartic Acid / genetics
  • Calcium / metabolism
  • Carbazoles / pharmacology
  • Cattle
  • Chromaffin Cells / drug effects
  • Chromaffin Cells / physiology*
  • Chromaffin Cells / ultrastructure
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology
  • Exocytosis / drug effects
  • Exocytosis / physiology
  • Green Fluorescent Proteins / metabolism
  • Immunohistochemistry / methods
  • Indoles / pharmacology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Microscopy, Electron, Transmission / methods
  • Munc18 Proteins / genetics
  • Munc18 Proteins / metabolism*
  • Mutagenesis / physiology
  • Patch-Clamp Techniques / methods
  • Phorbol 12,13-Dibutyrate
  • Phosphorylation / drug effects
  • Protein Kinase C / genetics
  • Protein Kinase C / metabolism*
  • Secretory Vesicles / drug effects
  • Secretory Vesicles / physiology*
  • Secretory Vesicles / ultrastructure
  • Serine / genetics
  • Transfection / methods

Substances

  • Carbazoles
  • Enzyme Inhibitors
  • Indoles
  • Munc18 Proteins
  • Go 6976
  • Green Fluorescent Proteins
  • Aspartic Acid
  • Phorbol 12,13-Dibutyrate
  • Serine
  • Protein Kinase C
  • Calcium