Large diameter of palytoxin-induced Na/K pump channels and modulation of palytoxin interaction by Na/K pump ligands

J Gen Physiol. 2004 Apr;123(4):357-76. doi: 10.1085/jgp.200308964. Epub 2004 Mar 15.

Abstract

Palytoxin binds to Na/K pumps to generate nonselective cation channels whose pore likely comprises at least part of the pump's ion translocation pathway. We systematically analyzed palytoxin's interactions with native human Na/K pumps in outside-out patches from HEK293 cells over a broad range of ionic and nucleotide conditions, and with or without cardiotonic steroids. With 5 mM internal (pipette) [MgATP], palytoxin activated the conductance with an apparent affinity that was highest for Na(+)-containing (K(+)-free) external and internal solutions, lowest for K(+)-containing (Na(+)-free) external and internal solutions, and intermediate for the mixed external Na(+)/internal K(+), and external K(+)/internal Na(+) conditions; with Na(+) solutions and MgATP, the mean dwell time of palytoxin on the Na/K pump was about one day. With Na(+) solutions, the apparent affinity for palytoxin action was low after equilibration of patches with nucleotide-free pipette solution. That apparent affinity was increased in two phases as the equilibrating [MgATP] was raised over the submicromolar, and submillimolar, ranges, but was increased by pipette MgAMPPNP in a single phase, over the submillimolar range; the apparent affinity at saturating [MgAMPPNP] remained approximately 30-fold lower than at saturating [MgATP]. After palytoxin washout, the conductance decay that reflects palytoxin unbinding was accelerated by cardiotonic steroid. When Na/K pumps were preincubated with cardiotonic steroid, subsequent activation of palytoxin-induced conductance was greatly slowed, even after washout of the cardiotonic steroid, but activation could still be accelerated by increasing palytoxin concentration. These results indicate that palytoxin and a cardiotonic steroid can simultaneously occupy the same Na/K pump, each destabilizing the other. The palytoxin-induced channels were permeable to several large organic cations, including N-methyl-d-glucamine(+), suggesting that the narrowest section of the pore must be approximately 7.5 A wide. Enhanced understanding of palytoxin action now allows its use for examining the structures and mechanisms of the gates that occlude/deocclude transported ions during the normal Na/K pump cycle.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Acrylamides / pharmacology*
  • Adenosine Triphosphate / pharmacology
  • Animals
  • Cardiotonic Agents / pharmacology
  • Cells, Cultured
  • Cnidarian Venoms
  • Drug Interactions
  • Electric Conductivity
  • Guinea Pigs
  • Humans
  • Ion Channel Gating / drug effects*
  • Kidney / cytology
  • Ligands
  • Myocytes, Cardiac / cytology
  • Myocytes, Cardiac / metabolism*
  • Ouabain / pharmacology
  • Patch-Clamp Techniques
  • Phosphorylation
  • Potassium / pharmacokinetics
  • Sodium / pharmacokinetics
  • Sodium-Potassium-Exchanging ATPase / metabolism*

Substances

  • Acrylamides
  • Cardiotonic Agents
  • Cnidarian Venoms
  • Ligands
  • Ouabain
  • Adenosine Triphosphate
  • Sodium
  • Sodium-Potassium-Exchanging ATPase
  • palytoxin
  • Potassium