Flow regulation of endothelin-1 production in the inner medullary collecting duct

Am J Physiol Renal Physiol. 2015 Mar 15;308(6):F541-52. doi: 10.1152/ajprenal.00456.2014. Epub 2015 Jan 13.

Abstract

Collecting duct-derived endothelin (ET)-1 is an autocrine inhibitor of Na(+) and water reabsorption; its deficiency causes hypertension and water retention. Extracellular fluid volume expansion increases collecting duct ET-1, thereby promoting natriuresis and diuresis; however, how this coupling between volume expansion and collecting duct ET-1 occurs is incompletely understood. One possibility is that volume expansion increases tubular fluid flow. To investigate this, cultured IMCD3 cells were subjected to static or flow conditions. Exposure to a shear stress of 2 dyn/cm(2) for 2 h increased ET-1 mRNA content by ∼2.3-fold. Absence of perfusate Ca(2+), chelation of intracellular Ca(2+), or inhibition of Ca(2+) signaling (calmodulin, Ca(2+)/calmodulin-dependent kinase, calcineurin, PKC, or phospholipase C) prevented the flow response. Evaluation of possible flow-activated Ca(2+) entry pathways revealed no role for transient receptor potential (TRP)C3, TRPC6, and TRPV4; however, cells with TRPP2 (polycystin-2) knockdown had no ET-1 flow response. Flow increased intracellular Ca(2+) was blunted in TRPP2 knockdown cells. Nonspecific blockade of P2 receptors, as well as specific inhibition of P2X7 and P2Y2 receptors, prevented the ET-1 flow response. The ET-1 flow response was not affected by inhibition of either epithelial Na(+) channels or the mitochondrial Na(+)/Ca(2+) exchanger. Taken together, these findings provide evidence that in IMCD3 cells, flow, via polycystin-2 and P2 receptors, engages Ca(2+)-dependent signaling pathways that stimulate ET-1 synthesis.

Keywords: collecting duct; endothelin; flow; purinergic.

Publication types

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

MeSH terms

  • Animals
  • Calcium / metabolism
  • Calcium Signaling
  • Cell Line
  • Diuresis
  • Endothelin-1 / metabolism*
  • Epithelial Sodium Channels / metabolism
  • Kidney Medulla / metabolism*
  • Kidney Tubules, Collecting / metabolism*
  • Male
  • Mice
  • Natriuresis
  • RNA, Messenger / metabolism
  • Rats, Sprague-Dawley
  • Receptors, Purinergic / metabolism*
  • Sodium / metabolism
  • TRPP Cation Channels / metabolism*
  • Transient Receptor Potential Channels / metabolism
  • Water / metabolism

Substances

  • Endothelin-1
  • Epithelial Sodium Channels
  • RNA, Messenger
  • Receptors, Purinergic
  • TRPP Cation Channels
  • Transient Receptor Potential Channels
  • polycystic kidney disease 2 protein
  • Water
  • Sodium
  • Calcium