N-linked glycans are required on epithelial Na+ channel subunits for maturation and surface expression

Am J Physiol Renal Physiol. 2018 Mar 1;314(3):F483-F492. doi: 10.1152/ajprenal.00195.2017. Epub 2017 Nov 29.

Abstract

Epithelial Na+ channel (ENaC) subunits undergo N-linked glycosylation in the endoplasmic reticulum where they assemble into an αβγ complex. Six, 13, and 5 consensus sites (Asn-X-Ser/Thr) for N-glycosylation reside in the extracellular domains of the mouse α-, β-, and γ-subunits, respectively. Because the importance of ENaC N-linked glycans has not been fully addressed, we examined the effect of preventing N-glycosylation of specific subunits on channel function, expression, maturation, and folding. Heterologous expression in Xenopus oocytes or Fischer rat thyroid cells with αβγ-ENaC lacking N-linked glycans on a single subunit reduced ENaC activity as well as the inhibitory response to extracellular Na+. The lack of N-linked glycans on the β-subunit also precluded channel activation by trypsin. However, channel activation by shear stress was N-linked glycan independent, regardless of which subunit was modified. We also discovered that the lack of N-linked glycans on any one subunit reduced the total and surface levels of cognate subunits. The lack of N-linked glycans on the β-subunit had the largest effect on total levels, with the lack of N-linked glycans on the γ- and α-subunits having intermediate and modest effects, respectively. Finally, channels with wild-type β-subunits were more sensitive to limited trypsin proteolysis than channels lacking N-linked glycans on the β-subunit. Our results indicate that N-linked glycans on each subunit are required for proper folding, maturation, surface expression, and function of the channel.

Keywords: N-linked glycan; epithelial sodium channel; maturation; mechanosensation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Epithelial Sodium Channels / chemistry
  • Epithelial Sodium Channels / genetics
  • Epithelial Sodium Channels / metabolism*
  • Glycosylation
  • Mechanotransduction, Cellular
  • Membrane Potentials
  • Mutation
  • Protein Conformation
  • Protein Folding
  • Protein Processing, Post-Translational*
  • Protein Transport
  • Rats, Inbred F344
  • Sodium / metabolism*
  • Structure-Activity Relationship
  • Trypsin / metabolism
  • Xenopus laevis

Substances

  • Epithelial Sodium Channels
  • Scnn1a protein, mouse
  • Scnn1b protein, mouse
  • Scnn1g protein, mouse
  • Sodium
  • Trypsin