Mechanisms of Lipid Accumulation in the Bone Morphogenetic Protein Receptor Type 2 Mutant Right Ventricle

Am J Respir Crit Care Med. 2016 Sep 15;194(6):719-28. doi: 10.1164/rccm.201507-1444OC.

Abstract

Rationale: In heritable pulmonary arterial hypertension with germline mutation in the bone morphogenetic protein receptor type 2 (BMPR2) gene, right ventricle (RV) dysfunction is associated with RV lipotoxicity; however, the underlying mechanism for lipid accumulation is not known.

Objectives: We hypothesized that lipid accumulation in cardiomyocytes with BMPR2 mutation occurs owing to alterations in lipid transport and impaired fatty acid oxidation (FAO), which is exacerbated by a high-lipid (Western) diet (WD).

Methods: We used a transgenic mouse model of pulmonary arterial hypertension with mutant BMPR2 and generated a cardiomyocyte cell line with BMPR2 mutation. Electron microscopy and metabolomic analysis were performed on mouse RVs.

Measurements and main results: By metabolomics analysis, we found an increase in long-chain fatty acids in BMPR2 mutant mouse RVs compared with controls, which correlated with cardiac index. BMPR2-mutant cardiomyocytes had increased lipid compared with controls. Direct measurement of FAO in the WD-fed BMPR2-mutant RV showed impaired palmitate-linked oxygen consumption, and metabolomics analysis showed reduced indices of FAO. Using both mutant BMPR2 mouse RVs and cardiomyocytes, we found an increase in the uptake of (14)C-palmitate and fatty acid transporter CD36 that was further exacerbated by WD.

Conclusions: Taken together, our data suggest that impaired FAO and increased expression of the lipid transporter CD36 are key mechanisms underlying lipid deposition in the BMPR2-mutant RV, which are exacerbated in the presence of dietary lipids. These findings suggest important features leading to RV lipotoxicity in pulmonary arterial hypertension and may point to novel areas of therapeutic intervention.

Keywords: fatty acid oxidation; fatty acid transporter (CD36); lipotoxic cardiomyopathy; pulmonary arterial hypertension; right ventricular lipotoxicity.

Publication types

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

MeSH terms

  • Animals
  • Bone Morphogenetic Protein Receptors, Type II / genetics*
  • Bone Morphogenetic Protein Receptors, Type II / physiology
  • Cell Line
  • Disease Models, Animal
  • Fatty Acids / metabolism
  • Heart Ventricles / chemistry*
  • Heart Ventricles / metabolism
  • Heart Ventricles / ultrastructure
  • Hypertension, Pulmonary / genetics
  • Hypertension, Pulmonary / metabolism
  • Lipid Metabolism / genetics
  • Lipids / analysis*
  • Metabolomics
  • Mice
  • Mice, Transgenic
  • Microscopy, Electron
  • Myocytes, Cardiac / metabolism

Substances

  • Fatty Acids
  • Lipids
  • BMPR2 protein, human
  • Bone Morphogenetic Protein Receptors, Type II