Myocardial Lipin 1 knockout in mice approximates cardiac effects of human LPIN1 mutations

JCI Insight. 2021 May 10;6(9):e134340. doi: 10.1172/jci.insight.134340.

Abstract

Lipin 1 is a bifunctional protein that is a transcriptional regulator and has phosphatidic acid (PA) phosphohydrolase activity, which dephosphorylates PA to generate diacylglycerol. Human lipin 1 mutations lead to episodic rhabdomyolysis, and some affected patients exhibit cardiac abnormalities, including exercise-induced cardiac dysfunction and cardiac triglyceride accumulation. Furthermore, lipin 1 expression is deactivated in failing heart, but the effects of lipin 1 deactivation in myocardium are incompletely understood. We generated mice with cardiac-specific lipin 1 KO (cs-Lpin1-/-) to examine the intrinsic effects of lipin 1 in the myocardium. Cs-Lpin1-/- mice had normal systolic cardiac function but mild cardiac hypertrophy. Compared with littermate control mice, PA content was higher in cs-Lpin1-/- hearts, which also had an unexpected increase in diacylglycerol and triglyceride content. Cs-Lpin1-/- mice exhibited diminished cardiac cardiolipin content and impaired mitochondrial respiration rates when provided with pyruvate or succinate as metabolic substrates. After transverse aortic constriction-induced pressure overload, loss of lipin 1 did not exacerbate cardiac hypertrophy or dysfunction. However, loss of lipin 1 dampened the cardiac ionotropic response to dobutamine and exercise endurance in association with reduced protein kinase A signaling. These data suggest that loss of lipin 1 impairs cardiac functional reserve, likely due to effects on glycerolipid homeostasis, mitochondrial function, and protein kinase A signaling.

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

Publication types

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

MeSH terms

  • Animals
  • Cardiolipins / metabolism
  • Cardiomegaly / genetics*
  • Cardiomegaly / metabolism
  • Cardiotonic Agents / pharmacology
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Diglycerides / metabolism
  • Disease Models, Animal*
  • Dobutamine / pharmacology
  • Exercise Tolerance / drug effects
  • Exercise Tolerance / genetics*
  • Mice*
  • Mice, Knockout
  • Mitochondria, Heart / metabolism*
  • Myocardial Contraction / drug effects
  • Myocardial Contraction / genetics*
  • Myocardium / metabolism*
  • Phosphatidate Phosphatase / genetics*
  • Phosphatidic Acids / metabolism
  • Pyruvic Acid / metabolism
  • Succinic Acid / metabolism
  • Triglycerides / metabolism

Substances

  • Cardiolipins
  • Cardiotonic Agents
  • Diglycerides
  • Phosphatidic Acids
  • Triglycerides
  • Dobutamine
  • Pyruvic Acid
  • Succinic Acid
  • Cyclic AMP-Dependent Protein Kinases
  • Lpin1 protein, mouse
  • Phosphatidate Phosphatase