Extracellular protease trypsin activates amiloride-insensitive sodium channels in human leukemia cells

J Cell Biochem. 2019 Jan;120(1):461-469. doi: 10.1002/jcb.27402. Epub 2018 Sep 11.

Abstract

Sodium influx is tightly regulated in the cells of blood origin. Amiloride-insensitive sodium channels were identified as one of the main sodium-transporting pathways in leukemia cells. To date, all known regulatory pathways of these channels are coupled with intracellular actin cytoskeleton dynamics. Here, to search for physiological mechanisms controlling epithelial Na+ channel (ENaC)-like channels, we utilized leukemia K562 cells as a unique model to examine single channel behavior in a whole-cell patch-clamp experiments. We have shown for the first time that extracellular serine protease trypsin directly activates sodium channels in plasma membrane of K562 cells. The whole-cell single current recordings clearly demonstrate no inhibition of trypsin-activated channels by amiloride or benzamil. Involvement of proteolytic cleavage in channel opening was confirmed in experiments with soybean trypsin inhibitor. More importantly, stabilization of F-actin with intracellular phalloidin did not prevent trypsin-induced channel activation indicating no implication of cytoskeleton rearrangements in stimulatory effect of extracellular protease. Our data reveals a novel mechanism modulating amiloride-insensitive ENaC-like channel activity and integral sodium permeability in leukemia cells.

Keywords: actin cytoskeleton; amiloride; human leukemia cell; plasma membrane; sodium channel; trypsin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism
  • Amiloride / analogs & derivatives
  • Amiloride / pharmacology*
  • Cell Membrane / metabolism
  • Cell Membrane Permeability / drug effects
  • Cytochalasin D / pharmacology
  • Epithelial Sodium Channel Blockers / pharmacology
  • Epithelial Sodium Channels / metabolism*
  • Humans
  • K562 Cells
  • Leukemia, Myeloid / metabolism*
  • Leukemia, Myeloid / pathology*
  • Membrane Potentials / drug effects
  • Microscopy, Fluorescence
  • Models, Biological
  • Patch-Clamp Techniques
  • Phalloidine / pharmacology
  • Sodium / metabolism
  • Trypsin / metabolism
  • Trypsin / pharmacology*
  • Trypsin Inhibitors / pharmacology

Substances

  • Actins
  • Epithelial Sodium Channel Blockers
  • Epithelial Sodium Channels
  • Trypsin Inhibitors
  • benzamil
  • Phalloidine
  • Cytochalasin D
  • Amiloride
  • Sodium
  • Trypsin