Glycosylation-dependent activation of epithelial sodium channel by solnatide

Biochem Pharmacol. 2015 Dec 15;98(4):740-53. doi: 10.1016/j.bcp.2015.08.003. Epub 2015 Aug 5.

Abstract

Dysfunction of the epithelial sodium channel (ENaC), which regulates salt and water homeostasis in epithelia, causes several human pathological conditions, including pulmonary oedema. This is a potentially lethal complication of acute lung injury at least partially caused by dysfunctional alveolar liquid clearance, which in turn impairs alveolar gas exchange. Solnatide (named TIP-peptide, AP301), a 17 residue peptide mimicking the lectin-like domain of TNF has been shown to activate ENaC in several experimental animal models of acute lung injury and is being evaluated as a potential therapy for pulmonary oedema. The peptide has recently completed phase 1 and 2a clinical trials. In this study, we identify a glycosylation-dependent mechanism that preserves ENaC function and expression. Since our previous data suggested that the pore-forming subunits of ENaC are essential for maximal current activation by solnatide, we performed single- and multi-N-glycosylation site mutations in αN232,293,312,397,511Q- and δN166,211,384Q-subunits, in order to identify crucial residues for interaction with solnatide within the extracellular loop of the channel. Additionally, we generated αL576X and αN232,293,312,397,511Q,L576X deletion mutants of ENaC-α, since we have previously demonstrated that the carboxy terminal domain of this subunit is also involved in its interaction with solnatide. In cells expressing αN232,293,312,397,511Q,L576Xβγ-hENaC or δN166,311,384Q,D552Xβγ-hENaC activation by solnatide, as measured in whole cell patch clamp mode, was completely abolished, whereas it was attenuated in αL576Xβγ-hENaC- and δD552Xβγ-hENaC-expressing cells. Taken together, our findings delineate an N-glycan dependent interaction between the TIP-peptide and ENaC leading to normalization of both sodium and fluid absorption in oedematous alveoli to non-oedematous levels.

Keywords: Epithelial sodium channel (ENaC); Glycosylation; Patch-clamp; Western blot.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Epithelial Sodium Channels / metabolism*
  • Glycosylation
  • HEK293 Cells
  • Humans
  • Peptides, Cyclic / chemistry*
  • Peptides, Cyclic / metabolism*

Substances

  • Epithelial Sodium Channels
  • Peptides, Cyclic
  • AP301 peptide