Ca2+ dependence of flow-stimulated K secretion in the mammalian cortical collecting duct

Am J Physiol Renal Physiol. 2007 Jul;293(1):F227-35. doi: 10.1152/ajprenal.00057.2007. Epub 2007 Mar 27.

Abstract

Apical low-conductance SK and high-conductance Ca(2+)-activated BK channels are present in distal nephron, including the cortical collecting duct (CCD). Flow-stimulated net K secretion (J(K)) in the CCD is 1) blocked by iberiotoxin, an inhibitor of BK but not SK channels, and 2) associated with an increase in [Ca(2+)](i), leading us to conclude that BK channels mediate flow-stimulated J(K). To examine the Ca(2+) dependence and sources of Ca(2+) contributing to flow-stimulated J(K), J(K) and net Na absorption (J(Na)) were measured at slow (approximately 1) and fast (approximately 5 nl.min(-1).mm(-1)) flow rates in rabbit CCDs microperfused in the absence of luminal Ca(2+) or after pretreatment with BAPTA-AM to chelate intracellular Ca(2+), 2-aminoethoxydiphenyl borate (2-APB), to inhibit the inositol 1,4,5-trisphosphate (IP(3)) receptor or thapsigargin to deplete internal stores. These treatments, which do not affect flow-stimulated J(Na) (Morimoto et al. Am J Physiol Renal Physiol 291: F663-F669, 2006), inhibited flow-stimulated J(K). Increases in [Ca(2+)](i) stimulate exocytosis. To test whether flow induces exocytic insertion of preformed BK channels into the apical membrane, CCDs were pretreated with 10 microM colchicine (COL) to disrupt microtubule function or 5 microg/ml brefeldin-A (BFA) to inhibit delivery of channels from the intracellular pool to the plasma membrane. Both agents inhibited flow-stimulated J(K) but not J(Na) (Morimoto et al. Am J Physiol Renal Physiol 291: F663-F669, 2006), although COL but not BFA also blocked the flow-induced [Ca(2+)](i) transient. We thus speculate that BK channel-mediated, flow-stimulated J(K) requires an increase in [Ca(2+)](i) due, in part, to luminal Ca(2+) entry and ER Ca(2+) release, microtubule integrity, and exocytic insertion of preformed channels into the apical membrane.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Methyl-3-isobutylxanthine / pharmacology
  • Animals
  • Bicarbonates / metabolism
  • Biological Transport, Active / drug effects
  • Brefeldin A / pharmacology
  • Calcium / metabolism
  • Calcium / physiology*
  • Cations / metabolism
  • Chelating Agents / pharmacology
  • Colchicine / pharmacology
  • Egtazic Acid / analogs & derivatives
  • Egtazic Acid / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Female
  • Hydrogen / metabolism
  • In Vitro Techniques
  • Kidney Cortex / metabolism*
  • Kidney Tubules, Collecting / metabolism*
  • Kinetics
  • Large-Conductance Calcium-Activated Potassium Channels / drug effects
  • Large-Conductance Calcium-Activated Potassium Channels / metabolism
  • Patch-Clamp Techniques
  • Perfusion
  • Phosphodiesterase Inhibitors / pharmacology
  • Potassium / metabolism*
  • Protein Synthesis Inhibitors / pharmacology
  • Rabbits
  • Thapsigargin / pharmacology

Substances

  • Bicarbonates
  • Cations
  • Chelating Agents
  • Enzyme Inhibitors
  • Large-Conductance Calcium-Activated Potassium Channels
  • Phosphodiesterase Inhibitors
  • Protein Synthesis Inhibitors
  • Brefeldin A
  • Egtazic Acid
  • Thapsigargin
  • Hydrogen
  • 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid
  • Potassium
  • Colchicine
  • Calcium
  • 1-Methyl-3-isobutylxanthine