Molecular basis for clinical heterogeneity in inherited cardiomyopathies due to myopalladin mutations

Hum Mol Genet. 2012 May 1;21(9):2039-53. doi: 10.1093/hmg/dds022. Epub 2012 Jan 27.

Abstract

Abnormalities in Z-disc proteins cause hypertrophic (HCM), dilated (DCM) and/or restrictive cardiomyopathy (RCM), but disease-causing mechanisms are not fully understood. Myopalladin (MYPN) is a Z-disc protein expressed in striated muscle and functions as a structural, signaling and gene expression regulating molecule in response to muscle stress. MYPN was genetically screened in 900 patients with HCM, DCM and RCM, and disease-causing mechanisms were investigated using comparative immunohistochemical analysis of the patient myocardium and neonatal rat cardiomyocytes expressing mutant MYPN. Cardiac-restricted transgenic (Tg) mice were generated and protein-protein interactions were evaluated. Two nonsense and 13 missense MYPN variants were identified in subjects with DCM, HCM and RCM with the average cardiomyopathy prevalence of 1.66%. Functional studies were performed on two variants (Q529X and Y20C) associated with variable clinical phenotypes. Humans carrying the Y20C-MYPN variant developed HCM or DCM, whereas Q529X-MYPN was found in familial RCM. Disturbed myofibrillogenesis with disruption of α-actinin2, desmin and cardiac ankyrin repeat protein (CARP) was evident in rat cardiomyocytes expressing MYPN(Q529X). Cardiac-restricted MYPN(Y20C) Tg mice developed HCM and disrupted intercalated discs, with disturbed expression of desmin, desmoplakin, connexin43 and vinculin being evident. Failed nuclear translocation and reduced binding of Y20C-MYPN to CARP were demonstrated using in vitro and in vivo systems. MYPN mutations cause various forms of cardiomyopathy via different protein-protein interactions. Q529X-MYPN causes RCM via disturbed myofibrillogenesis, whereas Y20C-MYPN perturbs MYPN nuclear shuttling and leads to abnormal assembly of terminal Z-disc within the cardiac transitional junction and intercalated disc.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Cardiomyopathy, Dilated / genetics*
  • Cardiomyopathy, Dilated / pathology
  • Cardiomyopathy, Dilated / physiopathology
  • Cardiomyopathy, Hypertrophic, Familial / genetics*
  • Cardiomyopathy, Hypertrophic, Familial / pathology
  • Cardiomyopathy, Hypertrophic, Familial / physiopathology
  • Case-Control Studies
  • Codon, Nonsense
  • Female
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microscopy, Electron, Transmission
  • Muscle Proteins / chemistry
  • Muscle Proteins / genetics*
  • Muscle Proteins / metabolism
  • Muscle Proteins / physiology
  • Mutant Proteins / chemistry
  • Mutant Proteins / genetics
  • Mutant Proteins / physiology
  • Mutation*
  • Mutation, Missense
  • Myocardium / pathology
  • Myocytes, Cardiac / ultrastructure
  • Nuclear Proteins / metabolism
  • Pedigree
  • Phenotype
  • Protein Binding
  • Rats
  • Rats, Mutant Strains
  • Rats, Sprague-Dawley
  • Repressor Proteins / metabolism

Substances

  • Ankrd1 protein, rat
  • Codon, Nonsense
  • MYPN protein, human
  • Muscle Proteins
  • Mutant Proteins
  • Nuclear Proteins
  • Repressor Proteins