BMP promotes motility and represses growth of smooth muscle cells by activation of tandem Wnt pathways

J Cell Biol. 2011 Jan 10;192(1):171-88. doi: 10.1083/jcb.201008060.

Abstract

We present a novel cell-signaling paradigm in which bone morphogenetic protein 2 (BMP-2) consecutively and interdependently activates the wingless (Wnt)-β-catenin (βC) and Wnt-planar cell polarity (PCP) signaling pathways to facilitate vascular smooth muscle motility while simultaneously suppressing growth. We show that BMP-2, in a phospho-Akt-dependent manner, induces βC transcriptional activity to produce fibronectin, which then activates integrin-linked kinase 1 (ILK-1) via α4-integrins. ILK-1 then induces the Wnt-PCP pathway by binding a proline-rich motif in disheveled (Dvl) and consequently activating RhoA-Rac1-mediated motility. Transfection of a Dvl mutant that binds βC without activating RhoA-Rac1 not only prevents BMP-2-mediated vascular smooth muscle cell motility but promotes proliferation in association with persistent βC activity. Interfering with the Dvl-dependent Wnt-PCP activation in a murine stented aortic graft injury model promotes extensive neointima formation, as shown by optical coherence tomography and histopathology. We speculate that, in response to injury, factors that subvert BMP-2-mediated tandem activation of Wnt-βC and Wnt-PCP pathways contribute to obliterative vascular disease in both the systemic and pulmonary circulations.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Aorta / drug effects
  • Aorta / transplantation
  • Axin Protein
  • Becaplermin
  • Bone Morphogenetic Protein 2 / pharmacology*
  • Bone Morphogenetic Protein Receptors, Type II / metabolism
  • Cell Movement / drug effects*
  • Cell Proliferation / drug effects
  • Dishevelled Proteins
  • Enzyme Activation / drug effects
  • Fibronectins / metabolism
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • Humans
  • Mice
  • Models, Biological
  • Mutant Proteins / metabolism
  • Myocytes, Smooth Muscle / cytology*
  • Myocytes, Smooth Muscle / drug effects*
  • Myocytes, Smooth Muscle / enzymology
  • Neointima / pathology
  • Phosphoproteins / metabolism
  • Platelet-Derived Growth Factor / pharmacology
  • Protein Binding / drug effects
  • Protein Serine-Threonine Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-sis
  • Repressor Proteins / metabolism
  • Signal Transduction / drug effects*
  • Wnt Proteins / metabolism*
  • beta Catenin / metabolism
  • rac1 GTP-Binding Protein / metabolism
  • rhoA GTP-Binding Protein / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Axin Protein
  • Bone Morphogenetic Protein 2
  • Dishevelled Proteins
  • Fibronectins
  • Mutant Proteins
  • Phosphoproteins
  • Platelet-Derived Growth Factor
  • Proto-Oncogene Proteins c-sis
  • Repressor Proteins
  • Wnt Proteins
  • beta Catenin
  • Becaplermin
  • integrin-linked kinase
  • Glycogen Synthase Kinase 3 beta
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Glycogen Synthase Kinase 3
  • BMPR2 protein, human
  • Bone Morphogenetic Protein Receptors, Type II
  • rac1 GTP-Binding Protein
  • rhoA GTP-Binding Protein