Essential Role of Smooth Muscle STIM1 in Hypertension and Cardiovascular Dysfunction

Arterioscler Thromb Vasc Biol. 2016 Sep;36(9):1900-9. doi: 10.1161/ATVBAHA.116.307869. Epub 2016 Jul 28.

Abstract

Objectives: Chronic hypertension is the most critical risk factor for cardiovascular disease, heart failure, and stroke.

Approach and results: Here we show that wild-type mice infused with angiotensin II develop hypertension, cardiac hypertrophy, perivascular fibrosis, and endothelial dysfunction with enhanced stromal interaction molecule 1 (STIM1) expression in heart and vessels. All these pathologies were significantly blunted in mice lacking STIM1 specifically in smooth muscle (Stim1(SMC-/-)). Mechanistically, STIM1 upregulation during angiotensin II-induced hypertension was associated with enhanced endoplasmic reticulum stress, and smooth muscle STIM1 was required for endoplasmic reticulum stress-induced vascular dysfunction through transforming growth factor-β and nicotinamide adenine dinucleotide phosphate oxidase-dependent pathways. Accordingly, knockout mice for the endoplasmic reticulum stress proapoptotic transcriptional factor, CCAAT-enhancer-binding protein homologous protein (CHOP(-/-)), were resistant to hypertension-induced cardiovascular pathologies. Wild-type mice infused with angiotensin II, but not Stim1(SMC-/-) or CHOP(-/-) mice showed elevated vascular nicotinamide adenine dinucleotide phosphate oxidase activity and reduced phosphorylated endothelial nitric oxide synthase, cGMP, and nitrite levels.

Conclusions: Thus, smooth muscle STIM1 plays a crucial role in the development of hypertension and associated cardiovascular pathologies and represents a promising target for cardiovascular therapy.

Keywords: ER stress; cardiac hypertrophy; endothelial nitric oxide synthase; hypertension; nicotinamide adenine dinucleotide phosphate; stromal interaction molecule 1; vascular reactivity.

Publication types

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

MeSH terms

  • Angiotensin II
  • Animals
  • Blood Pressure* / drug effects
  • Cardiomegaly / genetics
  • Cardiomegaly / metabolism*
  • Cardiomegaly / physiopathology
  • Cardiomegaly / prevention & control
  • Cyclic GMP / metabolism
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Endoplasmic Reticulum Stress
  • Fibrosis
  • Genetic Predisposition to Disease
  • Hypertension / genetics
  • Hypertension / metabolism*
  • Hypertension / physiopathology
  • Hypertension / prevention & control
  • Male
  • Mice, Knockout
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism*
  • Muscle, Smooth, Vascular / pathology
  • Muscle, Smooth, Vascular / physiopathology
  • Myocardium / metabolism
  • Myocardium / pathology
  • NADPH Oxidases / metabolism
  • Nitric Oxide Synthase Type III / metabolism
  • Nitrites / metabolism
  • Phenotype
  • Phosphorylation
  • Reactive Oxygen Species / metabolism
  • Signal Transduction
  • Stromal Interaction Molecule 1 / deficiency
  • Stromal Interaction Molecule 1 / genetics
  • Stromal Interaction Molecule 1 / metabolism*
  • Time Factors
  • Transcription Factor CHOP / deficiency
  • Transcription Factor CHOP / genetics
  • Transforming Growth Factor beta / metabolism
  • Vasodilation* / drug effects
  • Vasodilator Agents / pharmacology

Substances

  • Ddit3 protein, mouse
  • Nitrites
  • Reactive Oxygen Species
  • Stim1 protein, mouse
  • Stromal Interaction Molecule 1
  • Transforming Growth Factor beta
  • Vasodilator Agents
  • Angiotensin II
  • Transcription Factor CHOP
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • NADPH Oxidases
  • Cyclic GMP