Dystrophin-glycoprotein complex sequesters Yap to inhibit cardiomyocyte proliferation

Nature. 2017 Jul 13;547(7662):227-231. doi: 10.1038/nature22979. Epub 2017 Jun 5.

Abstract

The regenerative capacity of the adult mammalian heart is limited, because of the reduced ability of cardiomyocytes to progress through mitosis. Endogenous cardiomyocytes have regenerative capacity at birth but this capacity is lost postnatally, with subsequent organ growth occurring through cardiomyocyte hypertrophy. The Hippo pathway, a conserved kinase cascade, inhibits cardiomyocyte proliferation in the developing heart to control heart size and prevents regeneration in the adult heart. The dystrophin-glycoprotein complex (DGC), a multicomponent transmembrane complex linking the actin cytoskeleton to extracellular matrix, is essential for cardiomyocyte homeostasis. DGC deficiency in humans results in muscular dystrophy, including the lethal Duchenne muscular dystrophy. Here we show that the DGC component dystroglycan 1 (Dag1) directly binds to the Hippo pathway effector Yap to inhibit cardiomyocyte proliferation in mice. The Yap-Dag1 interaction was enhanced by Hippo-induced Yap phosphorylation, revealing a connection between Hippo pathway function and the DGC. After injury, Hippo-deficient postnatal mouse hearts maintained organ size control by repairing the defect with correct dimensions, whereas postnatal hearts deficient in both Hippo and the DGC showed cardiomyocyte overproliferation at the injury site. In the hearts of mature Mdx mice (which have a point mutation in Dmd)-a model of Duchenne muscular dystrophy-Hippo deficiency protected against overload-induced heart failure.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Cardiomyopathies
  • Cell Cycle Proteins
  • Cell Proliferation
  • Dystroglycans / metabolism
  • Dystrophin / deficiency
  • Dystrophin / genetics
  • Dystrophin / metabolism*
  • Glycoproteins / deficiency
  • Glycoproteins / metabolism*
  • Heart Failure / genetics
  • Heart Failure / prevention & control
  • Hippo Signaling Pathway
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred mdx
  • Multiprotein Complexes / chemistry*
  • Multiprotein Complexes / deficiency
  • Multiprotein Complexes / metabolism*
  • Muscular Dystrophy, Duchenne / genetics
  • Muscular Dystrophy, Duchenne / metabolism
  • Myocytes, Cardiac / cytology*
  • Myocytes, Cardiac / metabolism
  • Organ Size
  • Phosphoproteins / metabolism*
  • Phosphorylation
  • Pressure
  • Protein Binding
  • Protein Serine-Threonine Kinases / deficiency
  • Protein Serine-Threonine Kinases / metabolism
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • Cell Cycle Proteins
  • Dystrophin
  • Glycoproteins
  • Multiprotein Complexes
  • Phosphoproteins
  • YAP-Signaling Proteins
  • Yap1 protein, mouse
  • Dystroglycans
  • Protein Serine-Threonine Kinases