Desmin Knock-Out Cardiomyopathy: A Heart on the Verge of Metabolic Crisis

Int J Mol Sci. 2022 Oct 10;23(19):12020. doi: 10.3390/ijms231912020.

Abstract

Desmin mutations cause familial and sporadic cardiomyopathies. In addition to perturbing the contractile apparatus, both desmin deficiency and mutated desmin negatively impact mitochondria. Impaired myocardial metabolism secondary to mitochondrial defects could conceivably exacerbate cardiac contractile dysfunction. We performed metabolic myocardial phenotyping in left ventricular cardiac muscle tissue in desmin knock-out mice. Our analyses revealed decreased mitochondrial number, ultrastructural mitochondrial defects, and impaired mitochondria-related metabolic pathways including fatty acid transport, activation, and catabolism. Glucose transporter 1 and hexokinase-1 expression and hexokinase activity were increased. While mitochondrial creatine kinase expression was reduced, fetal creatine kinase expression was increased. Proteomic analysis revealed reduced expression of proteins involved in electron transport mainly of complexes I and II, oxidative phosphorylation, citrate cycle, beta-oxidation including auxiliary pathways, amino acid catabolism, and redox reactions and oxidative stress. Thus, desmin deficiency elicits a secondary cardiac mitochondriopathy with severely impaired oxidative phosphorylation and fatty and amino acid metabolism. Increased glucose utilization and fetal creatine kinase upregulation likely portray attempts to maintain myocardial energy supply. It may be prudent to avoid medications worsening mitochondrial function and other metabolic stressors. Therapeutic interventions for mitochondriopathies might also improve the metabolic condition in desmin deficient hearts.

Keywords: amino acid; cardiomyopathy; creatine kinase; desmin; desmin knock-out metabolism; desminopathy; fatty acid; glucose; mitochondria; mitochondriopathy.

MeSH terms

  • Amino Acids / metabolism
  • Animals
  • Cardiomyopathies* / genetics
  • Cardiomyopathies* / metabolism
  • Citrates / metabolism
  • Creatine Kinase, Mitochondrial Form / metabolism
  • Desmin* / genetics
  • Desmin* / metabolism
  • Fatty Acids / metabolism
  • Glucose / metabolism
  • Glucose Transporter Type 1 / metabolism
  • Hexokinase* / genetics
  • Hexokinase* / metabolism
  • Mice
  • Mice, Knockout
  • Myocardium / metabolism
  • Oxidative Phosphorylation
  • Proteomics

Substances

  • Amino Acids
  • Citrates
  • Desmin
  • Fatty Acids
  • Glucose Transporter Type 1
  • Hexokinase
  • Creatine Kinase, Mitochondrial Form
  • Glucose

Grants and funding

B.E. (Britta Eggers), K.S., and K.M. were supported by P.U.R.E. (Protein Research Unit Ruhr within Europe) and Center for Protein Diagnostics (ProDi) grants, and K.S. by de.NBI, a project of the German Federal Ministry of Education and Research (BMBF) (grant number FKZ 031 A 534A), both from the Ministry of Innovation, Science and Research of North Rhine-Westphalia, Germany. V.P. was supported by BONFOR. J.M.Z. received funding from the Ministry of Education, Youth and Sport of the Czech Republic (SVV-260571/2020). Fluorescence microscopy performed by members of the Faculty of Science, Charles University, Prague, was conducted in the Laboratory of Confocal and Fluorescence Microscopy co-financed by the European Regional Development Fund and the state budget of the Czech Republic, project numbers CZ.1.05/4.1.00/16.0347 and CZ.2.16/3.1.00/21515. The Optical Imaging Center Erlangen (OICE) facility was funded by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG, reference number 52732026).