Nedd4-2 modulates renal Na+-Cl- cotransporter via the aldosterone-SGK1-Nedd4-2 pathway

J Am Soc Nephrol. 2011 Sep;22(9):1707-19. doi: 10.1681/ASN.2011020132. Epub 2011 Aug 18.

Abstract

Regulation of renal Na(+) transport is essential for controlling blood pressure, as well as Na(+) and K(+) homeostasis. Aldosterone stimulates Na(+) reabsorption by the Na(+)-Cl(-) cotransporter (NCC) in the distal convoluted tubule (DCT) and by the epithelial Na(+) channel (ENaC) in the late DCT, connecting tubule, and collecting duct. Aldosterone increases ENaC expression by inhibiting the channel's ubiquitylation and degradation; aldosterone promotes serum-glucocorticoid-regulated kinase SGK1-mediated phosphorylation of the ubiquitin-protein ligase Nedd4-2 on serine 328, which prevents the Nedd4-2/ENaC interaction. It is important to note that aldosterone increases NCC protein expression by an unknown post-translational mechanism. Here, we present evidence that Nedd4-2 coimmunoprecipitated with NCC and stimulated NCC ubiquitylation at the surface of transfected HEK293 cells. In Xenopus laevis oocytes, coexpression of NCC with wild-type Nedd4-2, but not its catalytically inactive mutant, strongly decreased NCC activity and surface expression. SGK1 prevented this inhibition in a kinase-dependent manner. Furthermore, deficiency of Nedd4-2 in the renal tubules of mice and in cultured mDCT(15) cells upregulated NCC. In contrast to ENaC, Nedd4-2-mediated inhibition of NCC did not require the PY-like motif of NCC. Moreover, the mutation of Nedd4-2 at either serine 328 or 222 did not affect SGK1 action, and mutation at both sites enhanced Nedd4-2 activity and abolished SGK1-dependent inhibition. Taken together, these results suggest that aldosterone modulates NCC protein expression via a pathway involving SGK1 and Nedd4-2 and provides an explanation for the well-known aldosterone-induced increase in NCC protein expression.

Publication types

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

MeSH terms

  • 11-beta-Hydroxysteroid Dehydrogenase Type 2 / metabolism
  • Aldosterone / metabolism*
  • Animals
  • Down-Regulation
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • HEK293 Cells
  • Humans
  • Immediate-Early Proteins / metabolism*
  • Kidney Tubules, Distal / enzymology*
  • Mice
  • Mice, Knockout
  • Nedd4 Ubiquitin Protein Ligases
  • Phosphorylation
  • Protein Serine-Threonine Kinases / metabolism*
  • Signal Transduction
  • Sodium Chloride Symporters / metabolism*
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination
  • Xenopus Proteins
  • Xenopus laevis

Substances

  • Endosomal Sorting Complexes Required for Transport
  • Immediate-Early Proteins
  • Sodium Chloride Symporters
  • Xenopus Proteins
  • Aldosterone
  • 11-beta-Hydroxysteroid Dehydrogenase Type 2
  • Nedd4 Ubiquitin Protein Ligases
  • Nedd4 protein, Xenopus
  • Nedd4 protein, human
  • Nedd4L protein, human
  • Nedd4l protein, mouse
  • nedd4l protein, Xenopus
  • Ubiquitin-Protein Ligases
  • Protein Serine-Threonine Kinases
  • serum-glucocorticoid regulated kinase