TRPP2 and TRPV4 form an EGF-activated calcium permeable channel at the apical membrane of renal collecting duct cells

PLoS One. 2013 Aug 16;8(8):e73424. doi: 10.1371/journal.pone.0073424. eCollection 2013.

Abstract

Objective: Regulation of apical calcium entry is important for the function of principal cells of the collecting duct. However, the molecular identity and the regulators of the transporter/channel, which is responsible for apical calcium entry and what factors regulate the calcium conduction remain unclear.

Methods and results: We report that endogenous TRPP2 and TRPV4 assemble to form a 23-pS divalent cation-permeable non-selective ion channel at the apical membrane of renal principal cells of the collecting duct. TRPP2\TRPV4 channel complex was identified by patch-clamp, immunofluorescence and co-immunprecipitation studies in both principal cells that either possess normal cilia (cilia (+)) or in which cilia are absent (cilia (-)). This channel has distinct biophysical and pharmacological and regulatory profiles compared to either TRPP2 or TRPV4 channels. The rate of occurrence detected by patch clamp was higher in cilia (-) compared to cilia (+) cells. In addition, shRNA knockdown of TRPP2 increased the prevalence of TRPV4 channel activity while knockdown of TRPV4 resulted in TRPP2 activity and knockdown of both proteins vastly decreased the 23-pS channel activity. Epidermal growth factor (EGF) stimulated TRPP2\TRPV4 channel through the EGF receptor (EGFR) tyrosine kinase-dependent signaling. With loss of cilia, apical EGF treatment resulted in 64-fold increase in channel activity in cilia (-) but not cilia (+) cells. In addition EGF increased cell proliferation in cilia (-) cell that was dependent upon TRPP2\TRPV4 channel mediated increase in intracellular calcium.

Conclusion: We conclude that in the absence of cilia, an EGF activated TRPP2\TRPV4 channel may play an important role in increased cell proliferation and cystogenesis.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Channel Agonists / pharmacology*
  • Cations, Divalent / metabolism
  • Cell Membrane Permeability / drug effects*
  • Cell Polarity / drug effects*
  • Cell Proliferation / drug effects
  • Cilia / metabolism
  • Epidermal Growth Factor / pharmacology*
  • ErbB Receptors / metabolism
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fluorescent Antibody Technique
  • Gene Silencing / drug effects
  • Immunoprecipitation
  • Ion Channel Gating / drug effects
  • Kidney Tubules, Collecting / cytology
  • Kidney Tubules, Collecting / drug effects
  • Kidney Tubules, Collecting / metabolism*
  • MAP Kinase Signaling System / drug effects
  • Mice
  • Phosphorylation / drug effects
  • TRPP Cation Channels / metabolism*
  • TRPV Cation Channels / metabolism*

Substances

  • Calcium Channel Agonists
  • Cations, Divalent
  • TRPP Cation Channels
  • TRPV Cation Channels
  • Trpv4 protein, mouse
  • polycystic kidney disease 2 protein
  • Epidermal Growth Factor
  • ErbB Receptors
  • Extracellular Signal-Regulated MAP Kinases
  • Calcium