Loss of collectrin, an angiotensin-converting enzyme 2 homolog, uncouples endothelial nitric oxide synthase and causes hypertension and vascular dysfunction

Circulation. 2013 Oct 15;128(16):1770-80. doi: 10.1161/CIRCULATIONAHA.113.003301. Epub 2013 Sep 18.

Abstract

Background: Collectrin is an orphan member of the renin-angiotensin system and is a homolog of angiotensin-converting enzyme 2, sharing ≈50% sequence identity. Unlike angiotensin-converting enzyme 2, collectrin lacks any catalytic domain. Collectrin has been shown to function as a chaperone of amino acid transporters. In rodents, the renal expression of collectrin is increased after subtotal nephrectomy and during high-salt feeding, raising the question of whether collectrin has any direct role in blood pressure regulation.

Methods and results: Using a susceptible genetic background, we demonstrate that deletion of collectrin results in hypertension, exaggerated salt sensitivity, and impaired pressure natriuresis. Collectrin knockout mice display impaired endothelium-dependent vasorelaxation that is associated with vascular remodeling, endothelial nitric oxide synthase uncoupling, decreased nitric oxide production, and increased superoxide generation. Treatment with Tempol, a superoxide scavenger, attenuates the augmented sodium sensitivity in collectrin knockout mice. We report for the first time that collectrin is expressed in endothelial cells. Furthermore, collectrin directly regulates l-arginine uptake and plasma membrane levels of CAT1 and y(+)LAT1 amino acid transporters in endothelial cells. Treatment with l-arginine modestly lowers blood pressure of collectrin knockout mice.

Conclusions: Collectrin is a consequential link between the transport of l-arginine and endothelial nitric oxide synthase uncoupling in hypertension.

Keywords: Tmem27 protein, mouse; arginine; hypertension; salt sensitivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin-Converting Enzyme 2
  • Animals
  • Arginine / metabolism
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Female
  • Hypertension, Renal / genetics
  • Hypertension, Renal / metabolism*
  • Hypertension, Renal / physiopathology
  • Kidney / metabolism
  • Kidney / physiopathology
  • Lung / cytology
  • Male
  • Membrane Glycoproteins / genetics*
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, 129 Strain
  • Mice, Knockout
  • Natriuresis / physiology
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type III / metabolism*
  • Peptidyl-Dipeptidase A / genetics*
  • Peptidyl-Dipeptidase A / metabolism
  • Primary Cell Culture
  • Sodium Chloride, Dietary / pharmacology
  • Superoxides / metabolism

Substances

  • Membrane Glycoproteins
  • Sodium Chloride, Dietary
  • Tmem27 protein, mouse
  • Superoxides
  • Nitric Oxide
  • Arginine
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Peptidyl-Dipeptidase A
  • Ace2 protein, mouse
  • Angiotensin-Converting Enzyme 2