ADP-ribosylation factor 1 protein regulates trypsinogen activation via organellar trafficking of procathepsin B protein and autophagic maturation in acute pancreatitis

J Biol Chem. 2012 Jul 13;287(29):24284-93. doi: 10.1074/jbc.M111.328815. Epub 2012 May 8.

Abstract

Several studies have suggested that autophagy might play a deleterious role in acute pancreatitis via intra-acinar activation of digestive enzymes. The prototype for this phenomenon is cathepsin B-mediated trypsin generation. To determine the organellar basis of this process, we investigated the subcellular distribution of the cathepsin B precursor, procathepsin B. We found that procathepsin B is enriched in Golgi-containing microsomes, suggesting a role for the ADP-ribosylation (ARF)-dependent trafficking of cathepsin B. Indeed, caerulein treatment increased processing of procathepsin B, whereas a known ARF inhibitor brefeldin A (BFA) prevented this. Similar treatment did not affect processing of procathepsin L. BFA-mediated ARF1 inhibition resulted in reduced cathepsin B activity and consequently reduced trypsinogen activation. However, formation of light chain 3 (LC3-II) was not affected, suggesting that BFA did not prevent autophagy induction. Instead, sucrose density gradient centrifugation and electron microscopy showed that BFA arrested caerulein-induced autophagosomal maturation. Therefore, ARF1-dependent trafficking of procathepsin B and the maturation of autophagosomes results in cathepsin B-mediated trypsinogen activation induced by caerulein.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-Ribosylation Factor 1 / antagonists & inhibitors
  • ADP-Ribosylation Factor 1 / metabolism*
  • Animals
  • Autophagy / drug effects*
  • Blotting, Western
  • Brefeldin A / pharmacology
  • Cathepsin B / metabolism*
  • Ceruletide / pharmacology
  • Enzyme Precursors / metabolism*
  • Golgi Apparatus / drug effects
  • Golgi Apparatus / metabolism
  • Mice
  • Microscopy, Electron
  • Microscopy, Fluorescence
  • Pancreatitis / metabolism*
  • Rats
  • Real-Time Polymerase Chain Reaction
  • Trypsinogen / metabolism*

Substances

  • Enzyme Precursors
  • Brefeldin A
  • Ceruletide
  • Trypsinogen
  • procathepsin B
  • Cathepsin B
  • ADP-Ribosylation Factor 1