Discoidin domain receptor 2 is an important modulator of BMP signaling during heterotopic bone formation

Bone Res. 2025 Jan 2;13(1):7. doi: 10.1038/s41413-024-00391-z.

Abstract

Bone morphogenetic proteins are essential for bone regeneration/fracture healing but can also induce heterotopic ossification (HO). Understanding accessory factors modulating BMP signaling would provide both a means of enhancing BMP-dependent regeneration while preventing HO. This study focuses on the ability of the collagen receptor, discoidin domain receptor 2 (DDR2), to regulate BMP activity. As will be shown, induction of bone formation by subcutaneous BMP2 implants is severely compromised in Ddr2-deficient mice. In addition, Ddr2 deficiency attenuates HO in mice expressing the ACVR1 mutation associated with human fibrodysplasia ossificans progressiva. In cells migrating into BMP2 implants, DDR2 is co-expressed with GLI1, a skeletal stem cell marker, and DDR2/GLI1-positive cells participate in BMP2-induced bone formation where they contribute to chondrogenic and osteogenic lineages. Consistent with this distribution, conditional knockout of Ddr2 in Gli1-expressing cells inhibited bone formation to the same extent seen in globally Ddr2-deficient animals. This response was explained by selective inhibition of Gli1+ cell proliferation without changes in apoptosis. The basis for this DDR2 requirement was explored further using bone marrow stromal cells. Although Ddr2 deficiency inhibited BMP2-dependent chondrocyte and osteoblast differentiation and in vivo, bone formation, early BMP responses including SMAD phosphorylation remained largely intact. Instead, Ddr2 deficiency reduced the nuclear/cytoplasmic ratio of the Hippo pathway intermediates, YAP and TAZ. This suggests that DDR2 regulates Hippo pathway-mediated responses to the collagen matrix, which subsequently affect BMP responsiveness. In summary, DDR2 is an important modulator of BMP signaling and a potential therapeutic target both for enhancing regeneration and treating HO.

MeSH terms

  • Activin Receptors, Type I / genetics
  • Activin Receptors, Type I / metabolism
  • Animals
  • Bone Morphogenetic Protein 2* / genetics
  • Bone Morphogenetic Protein 2* / metabolism
  • Bone Morphogenetic Proteins / metabolism
  • Cell Proliferation
  • Discoidin Domain Receptor 2* / genetics
  • Discoidin Domain Receptor 2* / metabolism
  • Humans
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Mice, Knockout
  • Ossification, Heterotopic* / genetics
  • Ossification, Heterotopic* / metabolism
  • Ossification, Heterotopic* / pathology
  • Osteogenesis* / drug effects
  • Signal Transduction*
  • Zinc Finger Protein GLI1 / genetics
  • Zinc Finger Protein GLI1 / metabolism

Substances

  • Discoidin Domain Receptor 2
  • Bone Morphogenetic Protein 2
  • Zinc Finger Protein GLI1
  • Acvr1 protein, mouse
  • Activin Receptors, Type I
  • Gli1 protein, mouse
  • Bone Morphogenetic Proteins