Nitrosative stress drives heart failure with preserved ejection fraction

Nature. 2019 Apr;568(7752):351-356. doi: 10.1038/s41586-019-1100-z. Epub 2019 Apr 10.

Abstract

Heart failure with preserved ejection fraction (HFpEF) is a common syndrome with high morbidity and mortality for which there are no evidence-based therapies. Here we report that concomitant metabolic and hypertensive stress in mice-elicited by a combination of high-fat diet and inhibition of constitutive nitric oxide synthase using Nω-nitro-L-arginine methyl ester (L-NAME)-recapitulates the numerous systemic and cardiovascular features of HFpEF in humans. Expression of one of the unfolded protein response effectors, the spliced form of X-box-binding protein 1 (XBP1s), was reduced in the myocardium of our rodent model and in humans with HFpEF. Mechanistically, the decrease in XBP1s resulted from increased activity of inducible nitric oxide synthase (iNOS) and S-nitrosylation of the endonuclease inositol-requiring protein 1α (IRE1α), culminating in defective XBP1 splicing. Pharmacological or genetic suppression of iNOS, or cardiomyocyte-restricted overexpression of XBP1s, each ameliorated the HFpEF phenotype. We report that iNOS-driven dysregulation of the IRE1α-XBP1 pathway is a crucial mechanism of cardiomyocyte dysfunction in HFpEF.

MeSH terms

  • Animals
  • Diet, High-Fat / adverse effects
  • Disease Models, Animal
  • Endoribonucleases / metabolism
  • Heart Failure / metabolism*
  • Heart Failure / physiopathology*
  • Heart Failure / prevention & control
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Myocytes, Cardiac / enzymology
  • Myocytes, Cardiac / metabolism
  • Myocytes, Cardiac / pathology
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide Synthase Type II / antagonists & inhibitors
  • Nitric Oxide Synthase Type II / deficiency
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism
  • Nitrosative Stress*
  • Phenotype
  • Protein Serine-Threonine Kinases / metabolism
  • Signal Transduction
  • Stroke Volume*
  • X-Box Binding Protein 1 / genetics
  • X-Box Binding Protein 1 / metabolism

Substances

  • X-Box Binding Protein 1
  • XBP1 protein, human
  • Nitric Oxide Synthase Type II
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • Endoribonucleases
  • NG-Nitroarginine Methyl Ester