Loss of Cardiac Ferritin H Facilitates Cardiomyopathy via Slc7a11-Mediated Ferroptosis

Circ Res. 2020 Jul 31;127(4):486-501. doi: 10.1161/CIRCRESAHA.120.316509. Epub 2020 Apr 30.

Abstract

Rationale: Maintaining iron homeostasis is essential for proper cardiac function. Both iron deficiency and iron overload are associated with cardiomyopathy and heart failure via complex mechanisms. Although ferritin plays a central role in iron metabolism by storing excess cellular iron, the molecular function of ferritin in cardiomyocytes remains unknown.

Objective: To characterize the functional role of Fth (ferritin H) in mediating cardiac iron homeostasis and heart disease.

Methods and results: Mice expressing a conditional Fth knockout allele were crossed with 2 distinct Cre recombinase-expressing mouse lines, resulting in offspring that lack Fth expression specifically in myocytes (MCK-Cre) or cardiomyocytes (Myh6-Cre). Mice lacking Fth in cardiomyocytes had decreased cardiac iron levels and increased oxidative stress, resulting in mild cardiac injury upon aging. However, feeding these mice a high-iron diet caused severe cardiac injury and hypertrophic cardiomyopathy, with molecular features typical of ferroptosis, including reduced glutathione (GSH) levels and increased lipid peroxidation. Ferrostatin-1, a specific inhibitor of ferroptosis, rescued this phenotype, supporting the notion that ferroptosis plays a pathophysiological role in the heart. Finally, we found that Fth-deficient cardiomyocytes have reduced expression of the ferroptosis regulator Slc7a11, and overexpressing Slc7a11 selectively in cardiomyocytes increased GSH levels and prevented cardiac ferroptosis.

Conclusions: Our findings provide compelling evidence that ferritin plays a major role in protecting against cardiac ferroptosis and subsequent heart failure, thereby providing a possible new therapeutic target for patients at risk of developing cardiomyopathy.

Keywords: cardiomyopathies; ferritins; ferroptosis; heart failure; iron.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging
  • Alleles
  • Amino Acid Transport System y+ / metabolism*
  • Animals
  • Apoferritins / adverse effects
  • Apoferritins / deficiency*
  • Apoferritins / genetics
  • Cardiomyopathies / etiology*
  • Cardiomyopathies / metabolism
  • Cardiomyopathies / prevention & control
  • Cardiomyopathy, Hypertrophic / etiology
  • Cardiomyopathy, Hypertrophic / prevention & control
  • Crosses, Genetic
  • Cyclohexylamines / administration & dosage
  • Ferroptosis / physiology*
  • Glutathione / metabolism
  • Heart Failure / etiology
  • Homeostasis
  • Hypertrophy, Left Ventricular / etiology
  • Iron / metabolism*
  • Iron Deficiencies
  • Iron Overload
  • Iron, Dietary / adverse effects
  • Lipid Peroxidation
  • Male
  • Mice
  • Mice, Transgenic
  • Myocardium / metabolism*
  • Myocytes, Cardiac / metabolism
  • Oxidative Stress
  • Phenylenediamines / administration & dosage
  • Reactive Oxygen Species / metabolism

Substances

  • Amino Acid Transport System y+
  • Cyclohexylamines
  • Iron, Dietary
  • Phenylenediamines
  • Reactive Oxygen Species
  • Slc7a11 protein, mouse
  • ferrostatin-1
  • Apoferritins
  • Iron
  • Glutathione