Familial Left Ventricular Non-Compaction Is Associated With a Rare p.V407I Variant in Bone Morphogenetic Protein 10

Circ J. 2019 Jul 25;83(8):1737-1746. doi: 10.1253/circj.CJ-19-0116. Epub 2019 Jun 26.

Abstract

Background: Left ventricular non-compaction (LVNC) is a heritable cardiomyopathy characterized by hypertrabeculation, inter-trabecular recesses and thin compact myocardium, but the genetic basis and mechanisms remain unclear. This study identified novel LVNC-associated mutations inNOTCH-dependent genes and investigated their mutational effects.

Methods and results: High-resolution melting screening was performed in 230 individuals with LVNC, followed by whole exome and Sanger sequencing of available family members. Dimerization of bone morphogenetic protein 10 (BMP10) and its binding to BMP receptors (BMPRs) were evaluated. Cellular differentiation, proliferation and tolerance to mechanical stretch were assessed in H9C2 cardiomyoblasts, expressing wild-type (WT) or mutant BMP10 delivered by adenoviral vectors. Rare variants, p.W143*-NRG1and p.V407I-BMP10, were identified in 2 unrelated probands and their affected family members. Although dimerization of mutant V407I-BMP10 was preserved like WT-BMP10, V407I-BMP10 pulled BMPR1a and BMPR2 receptors more weakly compared with WT-BMP10. On comparative gene expression and siRNA analysis, expressed BMPR1a and BMPR2 receptors were responsive to BMP10 treatment in H9C2 cardiomyoblasts. Expression of V407I-BMP10 resulted in a significantly lower rate of proliferation in H9C2 cells compared with WT-BMP10. Cyclic stretch resulted in destruction and death of V407I-BMP10 cells.

Conclusions: The W143*-NRG1and V470I-BMP10variants are associated with LVNC. Impaired BMPR-binding ability, perturbed proliferation and differentiation processes and intolerance to stretch in V407I-BMP10 mutant cardiomyoblasts may underlie myocardial non-compaction.

Keywords: Bone morphogenetic protein 10 (BMP10); Cardiomyocyte differentiation; Left ventricular non-compaction; Proliferation; Stretch.

MeSH terms

  • Animals
  • Bone Morphogenetic Protein Receptors, Type I / genetics
  • Bone Morphogenetic Protein Receptors, Type I / metabolism
  • Bone Morphogenetic Protein Receptors, Type II / genetics
  • Bone Morphogenetic Protein Receptors, Type II / metabolism
  • Bone Morphogenetic Proteins / genetics*
  • Bone Morphogenetic Proteins / metabolism
  • Case-Control Studies
  • Cell Differentiation
  • Cell Proliferation
  • Female
  • Genetic Predisposition to Disease
  • HEK293 Cells
  • Humans
  • Isolated Noncompaction of the Ventricular Myocardium / genetics*
  • Isolated Noncompaction of the Ventricular Myocardium / metabolism
  • Isolated Noncompaction of the Ventricular Myocardium / pathology
  • Male
  • Mechanotransduction, Cellular
  • Mice
  • Mutation*
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Phenotype
  • Polymorphism, Single Nucleotide*
  • Protein Binding
  • Rats

Substances

  • BMP10 protein, human
  • BMP10 protein, rat
  • Bone Morphogenetic Proteins
  • Bmpr1a protein, rat
  • Bmpr2 protein, rat
  • Bone Morphogenetic Protein Receptors, Type I
  • Bone Morphogenetic Protein Receptors, Type II