Combined deficiency of dystrophin and beta1 integrin in the cardiac myocyte causes myocardial dysfunction, fibrosis and calcification

Circ Res. 2008 May 9;102(9):1109-17. doi: 10.1161/CIRCRESAHA.108.173153. Epub 2008 Mar 13.

Abstract

The dystrophin-glycoprotein complex is a large complex of membrane-associated proteins linking the cytoskeleton to the extracellular matrix in muscle. Transmembrane heterodimeric (alphabeta) integrins serve also as cellular adhesion molecules and mechanotransducers. In the animal model for Duchenne muscular dystrophy, the mdx mouse, loss of dystrophin causes more severe abnormalities in skeletal than in cardiac muscle. We hypothesized that ablation of cardiac myocyte integrins in the mdx background would lead to a severe cardiomyopathic phenotype. Mdx mice were crossed to ones with cardiac myocyte-specific deletion of beta1 integrin (beta1KO) to generate beta1KOmdx. Unstressed beta1KOmdx mice were viable and had normal cardiac function; however, high mortality was seen in peri- and postpartum females by 6 months of age, when severe myocardial necrosis and fibrosis and extensive dystrophic calcification was seen. Decreased ventricular function and blunted adrenergic responsiveness was found in the beta1KOmdx mice compared with control (Lox/Lox, no Cre), beta1KO, and mdx. Similarly, adult beta1KOmdx males were more prone to isoproterenol-induced heart failure and death compared with control groups. Given the extensive calcification, we analyzed transcript levels of genes linked to fibrosis and calcification and found matrix gamma-carboxyglutamic acid protein, decorin, periostin, and the osteoblast transcription factor Runx2/Cbfa1 significantly increased in beta1KOmdx cardiac muscle. Our data show that combined deficiency of dystrophin and integrins in murine cardiac myocytes results in more severe cardiomyopathic changes in the stressed myocardium than reduction of either dystrophin or integrins alone and predisposes to myocardial calcification.

Publication types

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

MeSH terms

  • Adrenergic beta-Agonists / administration & dosage
  • Animals
  • Calcinosis / genetics
  • Calcinosis / metabolism*
  • Calcinosis / physiopathology
  • Calcium-Binding Proteins / metabolism
  • Cardiomyopathies / genetics
  • Cardiomyopathies / metabolism*
  • Cardiomyopathies / pathology
  • Cardiomyopathies / physiopathology
  • Cell Adhesion Molecules / metabolism
  • Core Binding Factor Alpha 1 Subunit / metabolism
  • Decorin
  • Disease Models, Animal
  • Dobutamine / administration & dosage
  • Dystrophin / deficiency
  • Dystrophin / genetics
  • Dystrophin / metabolism*
  • Extracellular Matrix Proteins / metabolism
  • Female
  • Fibrosis
  • Heart Failure / chemically induced
  • Heart Failure / genetics
  • Heart Failure / metabolism
  • Heart Failure / physiopathology
  • Integrin beta1 / genetics
  • Integrin beta1 / metabolism*
  • Isoproterenol / administration & dosage
  • Male
  • Matrix Gla Protein
  • Mice
  • Mice, Inbred mdx
  • Mice, Knockout
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism*
  • Myocytes, Cardiac / pathology
  • Necrosis
  • Phenotype
  • Pregnancy
  • Proteoglycans / metabolism
  • RNA, Messenger / metabolism
  • Severity of Illness Index
  • Time Factors
  • Up-Regulation
  • Ventricular Function* / drug effects

Substances

  • Adrenergic beta-Agonists
  • Calcium-Binding Proteins
  • Cell Adhesion Molecules
  • Core Binding Factor Alpha 1 Subunit
  • Dcn protein, mouse
  • Decorin
  • Dystrophin
  • Extracellular Matrix Proteins
  • Integrin beta1
  • Postn protein, mouse
  • Proteoglycans
  • RNA, Messenger
  • Runx2 protein, mouse
  • apo-dystrophin 1
  • Dobutamine
  • Isoproterenol