Dissociation of spectrin-ankyrin complex as a basis for loss of Na-K-ATPase polarity after ischemia

Am J Physiol Renal Physiol. 2003 Feb;284(2):F358-64. doi: 10.1152/ajprenal.00100.2002. Epub 2002 Oct 29.

Abstract

The polarized distribution of Na-K-ATPase at the basolateral membranes of renal tubule epithelial cells is maintained via a tethering interaction with the underlying spectrin-ankyrin cytoskeleton. In this study, we have explored the mechanism underlying the loss of Na-K-ATPase polarity after ischemic injury in Madin-Darby canine kidney (MDCK) cells, utilizing a novel antibody raised against a recently described kidney-specific isoform of ankyrin. In control MDCK cells, ankyrin was colocalized with Na-K-ATPase at the basolateral membrane. ATP depletion resulted in a duration-dependent mislocation of Na-K-ATPase and ankyrin throughout the cytoplasm. Colocalization studies showed a partial overlap between the distribution of ankyrin and Na-K-ATPase at all periods after ATP depletion. By immunoprecipitation with anti-ankyrin antibody, the mislocated Na-K-ATPase remained bound to ankyrin at all time points after ATP depletion. However, the interaction between ankyrin and spectrin was markedly diminished within 3 h of ATP depletion and was completely lost after 6 h. In solution binding assays using a fusion peptide of glutathione S-transferase with the ankyrin binding domain of Na-K-ATPase, a complex with ankyrin was detected at all time points after ATP depletion, but spectrin was lost from the complex in a duration-dependent manner. The loss of spectrin binding was not attributable to spectrin degradation but was associated with hyperphosphorylation of ankyrin. The results suggest that a dissociation of the membrane-cytoskeleton complex at the spectrin-ankyrin interface may contribute to the loss of Na-K-ATPase polarity after ischemic injury and reaffirm a critical adapter role for ankyrin in the normal maintenance of Na-K-ATPase polarity.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / deficiency
  • Animals
  • Ankyrins / metabolism*
  • Cell Line
  • Dogs
  • Ischemia / metabolism*
  • Kidney Tubules / metabolism
  • Phosphorylation
  • Rats
  • Renal Circulation*
  • Sodium-Potassium-Exchanging ATPase / metabolism*
  • Spectrin / metabolism*
  • Time Factors
  • Tissue Distribution

Substances

  • Ankyrins
  • Spectrin
  • Adenosine Triphosphate
  • Sodium-Potassium-Exchanging ATPase