Chronically Elevating Circulating Ketones Can Reduce Cardiac Inflammation and Blunt the Development of Heart Failure

Circ Heart Fail. 2020 Jun;13(6):e006573. doi: 10.1161/CIRCHEARTFAILURE.119.006573. Epub 2020 Jun 4.

Abstract

Background: Previous studies have shown beneficial effects of acute infusion of the primary ketone body, β-hydroxybutyrate, in heart failure (HF). However, whether chronic elevations in circulating ketones are beneficial remains unknown.

Methods: To chronically elevate circulating ketones in mice, we deleted the expression of the ketolytic, rate-limiting-enzyme, SCOT (succinyl-CoA:3-ketoacid-CoA transferase 1; encoded by Oxct1), in skeletal muscle. Tamoxifen-inducible skeletal muscle-specific Oxct1Muscle-/- knockout (n=32) mice and littermate controls (wild type; WT; n=35) were subjected to transverse aortic constriction (TAC) surgery to induce HF.

Results: Deletion of SCOT in skeletal, but not cardiac muscle resulted in elevated concentrations of fasted circulating β-hydroxybutyrate in knockout mice compared with WT mice (P=0.030). Five weeks following TAC, WT mice progressed to HF, whereas knockout mice with elevated fasting circulating ketones were largely protected from the TAC-induced effects observed in WT mice (ejection fraction, P=0.011; mitral E/A, P=0.012). Furthermore, knockout mice with TAC had attenuated expression of markers of sterile inflammation and macrophage infiltration, which were otherwise elevated in WT mice subjected to TAC. Lastly, addition of β-hydroxybutyrate to isolated hearts was associated with reduced NLRP3 (nucleotide-binding domain-like receptor protein 3)-inflammasome activation, which has been previously shown to play a role in contributing to HF-induced cardiac inflammation.

Conclusions: These data show that chronic elevation of circulating ketones protects against the development of HF that is associated with the ability of β-hydroxybutyrate to directly reduce inflammation. These beneficial effects of ketones were associated with reduced cardiac NLRP3 inflammasome activation, suggesting that ketones may modulate cardiac inflammation via this mechanism.

Keywords: cytokines; heart failure; inflammasome; inflammation; ketone bodies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3-Hydroxybutyric Acid / blood*
  • Animals
  • Coenzyme A-Transferases / deficiency*
  • Coenzyme A-Transferases / genetics
  • Disease Models, Animal
  • Fibrosis
  • Heart Failure / blood
  • Heart Failure / enzymology
  • Heart Failure / physiopathology
  • Heart Failure / prevention & control*
  • Hypertrophy, Left Ventricular / blood
  • Hypertrophy, Left Ventricular / physiopathology
  • Hypertrophy, Left Ventricular / prevention & control
  • Inflammasomes / metabolism
  • Isolated Heart Preparation
  • Male
  • Mice, Knockout
  • Myocarditis / blood
  • Myocarditis / enzymology
  • Myocarditis / physiopathology
  • Myocarditis / prevention & control*
  • Myocardium / enzymology*
  • Myocardium / pathology
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Up-Regulation
  • Ventricular Dysfunction, Left / blood
  • Ventricular Dysfunction, Left / physiopathology
  • Ventricular Dysfunction, Left / prevention & control
  • Ventricular Function, Left
  • Ventricular Remodeling

Substances

  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Coenzyme A-Transferases
  • 3-ketoacid CoA-transferase
  • 3-Hydroxybutyric Acid

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