cAMP-dependent activation of the renal-specific Na+-K+-2Cl- cotransporter is mediated by regulation of cotransporter trafficking

Am J Physiol Renal Physiol. 2003 Jun;284(6):F1145-54. doi: 10.1152/ajprenal.00421.2002. Epub 2003 Feb 25.

Abstract

The murine apical bumetanide-sensitive Na(+)-K(+)-2Cl(-) cotransporter gene (mBSC1) exhibits two spliced isoform products that differ at the COOH-terminal domain. A long COOH-terminal isoform (L-mBSC1) encodes the Na(+)-K(+)-2Cl(-) cotransporter, and a short isoform (S-mBSC1) exerts a dominant-negative effect on L-mBSC1 cotransporter activity that is abrogated by cAMP. However, the mechanism of this dominant-negative effect was not clear. In this study, we used confocal microscopic analysis of an enhanced green fluorescent protein (EGFP) fusion construct (L-mBSC1-EGFP) expressed to characterize the surface expression of the L-BSC1 isoform in Xenopus laevis oocytes. Functional expression was also assessed in L-mBSC1-injected oocytes by measuring the bumetanide-sensitive (86)Rb(+) uptake. Oocytes injected with L-mBSC1-EGFP cRNA developed a distinct plasma membrane-associated fluorescence that colocalized with the fluorescent membrane dye FM 4-64. The fluorescence intensity in L-mBSC1-EGFP oocytes did not change after cAMP was added to the extracellular medium. In contrast, L-mBSC1-EGFP fluorescence intensity was reduced in a dose-dependent manner, with coexpression of S-mBSC1. The inhibitory effect of S-mBSC1 was abrogated by cAMP. Finally, the exocytosis inhibitor colchicine blocked the effect of cAMP on the L-mBSC1-EGFP/S-mBSC1-coinjected oocytes. All changes in L-mBSC1 surface expression correlated with modification of bumetanide-sensitive (86)Rb(+) uptake. Our data suggest that the dominant-negative effect of S-mBSC1 on L-mBSC1 transport function is due to the effects of the cotransporter on trafficking.

Publication types

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

MeSH terms

  • 1-Methyl-3-isobutylxanthine / pharmacology
  • Animals
  • Bucladesine / antagonists & inhibitors
  • Bucladesine / pharmacology
  • Cell Membrane / enzymology
  • Cell Membrane / metabolism
  • Colchicine / pharmacology
  • Cyclic AMP / physiology*
  • DNA, Complementary / biosynthesis
  • Enzyme Activation
  • Exocytosis / physiology
  • Green Fluorescent Proteins
  • In Vitro Techniques
  • Isoenzymes / biosynthesis
  • Isoenzymes / metabolism
  • Kidney / enzymology*
  • Kidney / physiology*
  • Luminescent Proteins
  • Membrane Proteins / biosynthesis
  • Mice
  • Oocytes
  • Phosphodiesterase Inhibitors / pharmacology
  • Phosphorylation
  • Sodium-Potassium-Chloride Symporters / biosynthesis
  • Sodium-Potassium-Chloride Symporters / metabolism*
  • Xenopus

Substances

  • DNA, Complementary
  • Isoenzymes
  • Luminescent Proteins
  • Membrane Proteins
  • Phosphodiesterase Inhibitors
  • Sodium-Potassium-Chloride Symporters
  • Green Fluorescent Proteins
  • Bucladesine
  • Cyclic AMP
  • Colchicine
  • 1-Methyl-3-isobutylxanthine