Contractile force is enhanced in Aortas from pendrin null mice due to stimulation of angiotensin II-dependent signaling

PLoS One. 2014 Aug 22;9(8):e105101. doi: 10.1371/journal.pone.0105101. eCollection 2014.

Abstract

Pendrin is a Cl-/HCO3- exchanger expressed in the apical regions of renal intercalated cells. Following pendrin gene ablation, blood pressure falls, in part, from reduced renal NaCl absorption. We asked if pendrin is expressed in vascular tissue and if the lower blood pressure observed in pendrin null mice is accompanied by reduced vascular reactivity. Thus, the contractile responses to KCl and phenylephrine (PE) were examined in isometrically mounted thoracic aortas from wild-type and pendrin null mice. Although pendrin expression was not detected in the aorta, pendrin gene ablation changed contractile protein abundance and increased the maximal contractile response to PE when normalized to cross sectional area (CSA). However, the contractile sensitivity to this agent was unchanged. The increase in contractile force/cross sectional area observed in pendrin null mice was due to reduced cross sectional area of the aorta and not from increased contractile force per vessel. The pendrin-dependent increase in maximal contractile response was endothelium- and nitric oxide-independent and did not occur from changes in Ca2+ sensitivity or chronic changes in catecholamine production. However, application of 100 nM angiotensin II increased force/CSA more in aortas from pendrin null than from wild type mice. Moreover, angiotensin type 1 receptor inhibitor (candesartan) treatment in vivo eliminated the pendrin-dependent changes contractile protein abundance and changes in the contractile force/cross sectional area in response to PE. In conclusion, pendrin gene ablation increases aorta contractile force per cross sectional area in response to angiotensin II and PE due to stimulation of angiotensin type 1 receptor-dependent signaling. The angiotensin type 1 receptor-dependent increase in vascular reactivity may mitigate the fall in blood pressure observed with pendrin gene ablation.

Publication types

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

MeSH terms

  • Angiotensin II / pharmacology*
  • Animals
  • Anion Transport Proteins / deficiency
  • Anion Transport Proteins / genetics*
  • Aorta / drug effects*
  • Aorta / metabolism*
  • Aorta / pathology
  • Calcium / metabolism
  • Catecholamines / biosynthesis
  • Dose-Response Relationship, Drug
  • Gene Expression
  • Kidney / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism
  • Nitric Oxide / metabolism
  • Phenylephrine / pharmacology
  • Potassium Chloride / pharmacology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptor, Angiotensin, Type 1 / metabolism
  • Signal Transduction / drug effects*
  • Sulfate Transporters
  • Vasoconstriction / drug effects*
  • Vasoconstriction / genetics*
  • Vasoconstrictor Agents / pharmacology

Substances

  • Anion Transport Proteins
  • Catecholamines
  • RNA, Messenger
  • Receptor, Angiotensin, Type 1
  • Slc26a4 protein, mouse
  • Sulfate Transporters
  • Vasoconstrictor Agents
  • Angiotensin II
  • Phenylephrine
  • Nitric Oxide
  • Potassium Chloride
  • Calcium

Grants and funding

Funding provided by National Institute of Diabetes, Digestive and Kidney Diseases grants 46493 (to S. M. Wall); 37963 (to D. C. Eaton); and National Heart, Lung and Blood Institute grant 070892 (to R. L. Sutliff). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.