Enhancing mitochondrial pyruvate metabolism ameliorates ischemic reperfusion injury in the heart

JCI Insight. 2024 Jul 25;9(17):e180906. doi: 10.1172/jci.insight.180906.

Abstract

The clinical therapy for treating acute myocardial infarction is primary percutaneous coronary intervention (PPCI). PPCI is effective at reperfusing the heart; however, the rapid reintroduction of blood can cause ischemia-reperfusion (I/R). Reperfusion injury is responsible for up to half of the total myocardial damage, but there are no pharmacological interventions to reduce I/R. We previously demonstrated that inhibiting monocarboxylate transporter 4 (MCT4) and redirecting pyruvate toward oxidation can blunt hypertrophy. We hypothesized that this pathway might be important during I/R. Here, we establish that the pyruvate-lactate axis plays a role in determining myocardial salvage following injury. After I/R, the mitochondrial pyruvate carrier (MPC), required for pyruvate oxidation, is upregulated in the surviving myocardium. In cardiomyocytes lacking the MPC, there was increased cell death and less salvage after I/R, which was associated with an upregulation of MCT4. To determine the importance of pyruvate oxidation, we inhibited MCT4 with a small-molecule drug (VB124) at reperfusion. This strategy normalized reactive oxygen species (ROS), mitochondrial membrane potential (ΔΨ), and Ca2+, increased pyruvate entry to the TCA cycle, increased oxygen consumption, and improved myocardial salvage and functional outcomes following I/R. Our data suggest normalizing pyruvate-lactate metabolism by inhibiting MCT4 is a promising therapy to mitigate I/R injury.

Keywords: Carbohydrate metabolism; Cardiology; Cardiovascular disease; Metabolism; Mitochondria.

MeSH terms

  • Animals
  • Anion Transport Proteins
  • Disease Models, Animal
  • Lactic Acid / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / metabolism
  • Mitochondria, Heart / metabolism
  • Mitochondrial Membrane Transport Proteins* / metabolism
  • Monocarboxylic Acid Transporters* / metabolism
  • Muscle Proteins / metabolism
  • Myocardial Infarction / metabolism
  • Myocardial Reperfusion Injury* / metabolism
  • Myocardium / metabolism
  • Myocardium / pathology
  • Myocytes, Cardiac* / metabolism
  • Oxidation-Reduction
  • Pyruvic Acid* / metabolism
  • Reactive Oxygen Species / metabolism

Substances

  • Monocarboxylic Acid Transporters
  • Pyruvic Acid
  • Mitochondrial Membrane Transport Proteins
  • Slc16a4 protein, mouse
  • Muscle Proteins
  • Lactic Acid
  • MPC1 pyruvate carrier protein, mouse
  • Reactive Oxygen Species
  • Anion Transport Proteins