Unique regulation of human Na+/H+ exchanger 3 (NHE3) by Nedd4-2 ligase that differs from non-primate NHE3s

J Biol Chem. 2014 Jun 27;289(26):18360-72. doi: 10.1074/jbc.M113.541706. Epub 2014 May 15.

Abstract

Na(+)/H(+) exchanger NHE3 expressed in the intestine and kidney plays a major role in NaCl and HCO3 (-) absorption that is closely linked to fluid absorption and blood pressure regulation. The Nedd4 family of E3 ubiquitin ligases interacts with a number of transporters and channels via PY motifs. A comparison of NHE3 sequences revealed the presence of PY motifs in NHE3s from human and several non-human primates but not in non-primate NHE3s. In this study we evaluated the differences between human and non-primate NHE3s in ubiquitination and interaction with Nedd4-2. We found that Nedd4-2 ubiquitinated human NHE3 (hNHE3) and altered its expression and activity. Surprisingly, rat NHE3 co-immunoprecipitated Nedd4-2, but its expression and activity were not altered by silencing of Nedd4-2. Ubiquitination by Nedd4-2 rendered hNHE3 to undergo internalization at a significantly greater rate than non-primate NHE3s without altering protein stability. Insertion of a PY motif in rabbit NHE3 recapitulated the interaction with Nedd4-2 and enhanced internalization. Thus, we propose a new model where disruption of Nedd4-2 interaction elevates hNHE3 expression and activity.

Keywords: Endocytosis; Hypertension; Protein-Protein Interaction; Sodium-Proton Exchange; Ubiquitin.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Endosomal Sorting Complexes Required for Transport / chemistry
  • Endosomal Sorting Complexes Required for Transport / genetics
  • Endosomal Sorting Complexes Required for Transport / metabolism*
  • Gene Expression Regulation
  • Humans
  • Mammals / classification
  • Mammals / genetics
  • Molecular Sequence Data
  • Nedd4 Ubiquitin Protein Ligases
  • Opossums
  • Phylogeny
  • Protein Binding
  • Rabbits
  • Rats
  • Sequence Alignment
  • Sodium-Hydrogen Exchanger 3
  • Sodium-Hydrogen Exchangers / chemistry
  • Sodium-Hydrogen Exchangers / genetics
  • Sodium-Hydrogen Exchangers / metabolism*
  • Ubiquitin-Protein Ligases / chemistry
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination

Substances

  • Endosomal Sorting Complexes Required for Transport
  • SLC9A3 protein, human
  • Slc9a3 protein, rat
  • Sodium-Hydrogen Exchanger 3
  • Sodium-Hydrogen Exchangers
  • NEDD4L protein, rat
  • Nedd4 Ubiquitin Protein Ligases
  • Nedd4 protein, human
  • Nedd4 protein, rat
  • Nedd4L protein, human
  • Ubiquitin-Protein Ligases