Macrophage-derived MMP-8 determines smooth muscle cell differentiation from adventitia stem/progenitor cells and promotes neointima hyperplasia

Cardiovasc Res. 2020 Jan 1;116(1):211-225. doi: 10.1093/cvr/cvz044.

Abstract

Aims: Emerging evidence has suggested that adventitia stem/progenitor cells (AdSPCs) migrate into the intima of arteries in response to injury, where they differentiate towards smooth muscle cells (SMCs) and participate in neointimal hyperplasia. We have previously identified matrix metalloproteinase-8 (MMP8) as a key player in atherogenesis. In this study, we aimed to investigate the functional roles of macrophage-derived MMP8 in AdSPC differentiation and injury-induced arterial remodelling.

Methods and results: We first observed an important role for MMP8 in SMC differentiation from embryonic stem cells, but this effect was not seen in AdSPCs. Instead, through macrophages/AdSPCs co-culture and macrophage conditional culture medium studies, we have demonstrated that the MMP8 protein secreted from macrophages promotes SMC differentiation from AdSPCs. Mechanistically, we showed that macrophage-derived MMP8 promotes SMC differentiation from AdSPCs through modulating transforming growth factor-β activity and a disintegrin and metalloproteinase domain-containing protein 10 (ADAM10)/Notch1 signalling. We further demonstrated that the binding site for CBF1, Suppressor of Hairless, and Lag-1 (CSL) within SMC gene promoters is responsible for Notch1 mediated SMC differentiation. Finally, we demonstrated that macrophage-derived MMP8 increased injury-induced neointimal SMC hyperplasia by activating ADAM10/Notch1 signalling.

Conclusions: We have identified macrophage-derived MMP8 as a regulator in SMC differentiation from AdSPCs and neointimal SMC hyperplasia in response to injury. Our data provide new insights into the roles of MMP8 in AdSPC differentiation and the pathogenesis of neointima formation in the context of angiographic restenosis, and therefore may aid in the development of novel therapeutic agents for the prevention of this disease.

Keywords: A disintegrin and metalloproteinase domain-containing protein 10; Adventitia stem cells; Arterial remodelling; Atherosclerosis; Matrix metalloproteinase-8; Neointima formation; Notch signalling; Progenitor cells; Smooth muscle cell differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM10 Protein / genetics
  • ADAM10 Protein / metabolism
  • Adventitia / enzymology*
  • Adventitia / pathology
  • Amyloid Precursor Protein Secretases / genetics
  • Amyloid Precursor Protein Secretases / metabolism
  • Animals
  • Carotid Artery Injuries / enzymology*
  • Carotid Artery Injuries / genetics
  • Carotid Artery Injuries / pathology
  • Cell Differentiation*
  • Cell Proliferation*
  • Cells, Cultured
  • Coculture Techniques
  • Disease Models, Animal
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / genetics
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / metabolism
  • Macrophages / enzymology*
  • Macrophages / pathology
  • Matrix Metalloproteinase 8 / deficiency
  • Matrix Metalloproteinase 8 / genetics
  • Matrix Metalloproteinase 8 / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout, ApoE
  • Muscle, Smooth, Vascular / enzymology*
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / enzymology*
  • Myocytes, Smooth Muscle / pathology
  • Neointima*
  • Paracrine Communication
  • Receptor, Notch1 / genetics
  • Receptor, Notch1 / metabolism
  • Signal Transduction
  • Stem Cells / enzymology*
  • Stem Cells / pathology
  • Vascular Remodeling

Substances

  • Immunoglobulin J Recombination Signal Sequence-Binding Protein
  • Membrane Proteins
  • Notch1 protein, mouse
  • Rbpj protein, mouse
  • Receptor, Notch1
  • Amyloid Precursor Protein Secretases
  • MMP8 protein, mouse
  • Matrix Metalloproteinase 8
  • ADAM10 Protein
  • Adam10 protein, mouse