Ceramide-Protein Interactions Modulate Ceramide-Associated Lipotoxic Cardiomyopathy

Cell Rep. 2018 Mar 6;22(10):2702-2715. doi: 10.1016/j.celrep.2018.02.034.

Abstract

Lipotoxic cardiomyopathy (LCM) is characterized by abnormal myocardial accumulation of lipids, including ceramide; however, the contribution of ceramide to the etiology of LCM is unclear. Here, we investigated the association of ceramide metabolism and ceramide-interacting proteins (CIPs) in LCM in the Drosophila heart model. We find that ceramide feeding or ceramide-elevating genetic manipulations are strongly associated with cardiac dilation and defects in contractility. High ceramide-associated LCM is prevented by inhibiting ceramide synthesis, establishing a robust model of direct ceramide-associated LCM, corroborating previous indirect evidence in mammals. We identified several CIPs from mouse heart and Drosophila extracts, including caspase activator Annexin-X, myosin chaperone Unc-45, and lipogenic enzyme FASN1, and remarkably, their cardiac-specific manipulation can prevent LCM. Collectively, these data suggest that high ceramide-associated lipotoxicity is mediated, in part, through altering caspase activation, sarcomeric maintenance, and lipogenesis, thus providing evidence for conserved mechanisms in LCM pathogenesis in mammals.

Keywords: Annexin; Drosophila; FASN; Unc-45; apoptosis; diabetic cardiac disease; heart; lipogenesis; myriocin; sphingolipids.

Publication types

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

MeSH terms

  • Adipose Tissue / metabolism
  • Animals
  • Cardiomyopathies / genetics
  • Cardiomyopathies / metabolism*
  • Cardiomyopathies / pathology
  • Caspases / metabolism
  • Ceramides / administration & dosage
  • Ceramides / biosynthesis
  • Ceramides / metabolism*
  • Diet
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / metabolism*
  • Enzyme Activation
  • Gene Knockdown Techniques
  • Lipids / chemistry
  • Lipids / toxicity*
  • Lipogenesis
  • Molecular Chaperones / metabolism
  • Myocardium / metabolism
  • Myocardium / pathology
  • Myosins / metabolism
  • Organ Specificity
  • Phenotype
  • Protein Binding
  • Sphingolipids / metabolism

Substances

  • Ceramides
  • Drosophila Proteins
  • Lipids
  • Molecular Chaperones
  • Sphingolipids
  • UNC-45 protein, Drosophila
  • Caspases
  • Myosins