Specific Palmitoyltransferases Associate with and Activate the Epithelial Sodium Channel

J Biol Chem. 2017 Mar 10;292(10):4152-4163. doi: 10.1074/jbc.M117.776146. Epub 2017 Jan 30.

Abstract

The epithelial sodium channel (ENaC) has an important role in regulating extracellular fluid volume and blood pressure, as well as airway surface liquid volume and mucociliary clearance. ENaC is a trimer of three homologous subunits (α, β, and γ). We previously reported that cytoplasmic residues on the β (βCys-43 and βCys-557) and γ (γCys-33 and γCys-41) subunits are palmitoylated. Mutation of Cys that blocked ENaC palmitoylation also reduced channel open probability. Furthermore, γ subunit palmitoylation had a dominant role over β subunit palmitoylation in regulating ENaC. To determine which palmitoyltransferases (termed DHHCs) regulate the channel, mouse ENaCs were co-expressed in Xenopus oocytes with each of the 23 mouse DHHCs. ENaC activity was significantly increased by DHHCs 1, 2, 3, 7, and 14. ENaC activation by DHHCs was lost when γ subunit palmitoylation sites were mutated, whereas DHHCs 1, 2, and 14 still activated ENaC lacking β subunit palmitoylation sites. β subunit palmitoylation was increased by ENaC co-expression with DHHC 7. Both wild type ENaC and channels lacking β and γ palmitoylation sites co-immunoprecipitated with the five activating DHHCs, suggesting that ENaC forms a complex with multiple DHHCs. RT-PCR revealed that transcripts for the five activating DHHCs were present in cultured mCCDcl1 cells, and DHHC 3 was expressed in aquaporin 2-positive principal cells of mouse aldosterone-sensitive distal nephron where ENaC is localized. Treatment of polarized mCCDcl1 cells with a general inhibitor of palmitoylation reduced ENaC-mediated Na+ currents within minutes. Our results indicate that specific DHHCs have a role in regulating ENaC.

Keywords: Cys palmitoylation; DHHC; epithelial sodium channel (ENaC); ion channel; post-translational modification (PTM); protein acylation; protein palmitoylation.

Publication types

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

MeSH terms

  • Acyltransferases / genetics
  • Acyltransferases / metabolism*
  • Animals
  • Cells, Cultured
  • Cytoplasm / metabolism
  • Epithelial Sodium Channels / genetics
  • Epithelial Sodium Channels / metabolism*
  • Female
  • HEK293 Cells
  • Humans
  • Immunoprecipitation
  • Ion Channel Gating / physiology*
  • Ion Transport
  • Kidney / cytology
  • Kidney / metabolism*
  • Lipoylation
  • Mice
  • Mice, Inbred C57BL
  • Oocytes / cytology
  • Oocytes / metabolism
  • Protein Processing, Post-Translational*
  • Protein Subunits
  • Serine C-Palmitoyltransferase / metabolism
  • Sodium / metabolism
  • Xenopus laevis

Substances

  • Epithelial Sodium Channels
  • Protein Subunits
  • Sodium
  • Acyltransferases
  • Serine C-Palmitoyltransferase