MFG-E8 Regulates Vascular Smooth Muscle Cell Migration Through Dose-Dependent Mediation of Actin Polymerization

J Am Heart Assoc. 2021 Jun;10(11):e020870. doi: 10.1161/JAHA.121.020870. Epub 2021 May 27.

Abstract

Background Migration of vascular smooth muscle cells (VSMCs) is the main contributor to neointimal formation. The Arp2/3 (actin-related proteins 2 and 3) complex activates actin polymerization and is involved in lamellipodia formation during VSMC migration. Milk fat globule-epidermal growth factor 8 (MFG-E8) is a glycoprotein expressed in VSMCs. We hypothesized that MFG-E8 regulates VSMC migration through modulation of Arp2/3-mediated actin polymerization. Methods and Results To determine whether MFG-E8 is essential for VSMC migration, a model of neointimal hyperplasia was induced in the common carotid artery of wild-type and MFG-E8 knockout mice, and the extent of neointimal formation was evaluated. Genetic deletion of MFG-E8 in mice attenuated injury-induced neointimal hyperplasia. Cultured VSMCs deficient in MFG-E8 exhibited decreased cell migration. Immunofluorescence and immunoblotting revealed decreased Arp2 but not Arp3 expression in the common carotid arteries and VSMCs deficient in MFG-E8. Exogenous administration of recombinant MFG-E8 biphasically and dose-dependently regulated the cultured VSMCs. At a low concentration, MFG-E8 upregulated Arp2 expression. By contrast, MFG-E8 at a high concentration reduced the Arp2 level and significantly attenuated actin assembly. Arp2 upregulation mediated by low-dose MFG-E8 was abolished by treating cultured VSMCs with β1 integrin function-blocking antibody and Rac1 inhibitors. Moreover, treatment of the artery with a high dose of recombinant MFG-E8 diminished injury-induced neointimal hyperplasia and reduced VSMC migration. Conclusions MFG-E8 plays a critical role in VSMC migration through dose-dependent regulation of Arp2-mediated actin polymerization. These findings suggest that high doses of MFG-E8 may have therapeutic potential for treating vascular occlusive diseases.

Keywords: Arp2/3 complex; MFG‐E8; migration; neointimal formation; vascular smooth muscle cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism*
  • Animals
  • Antigens, Surface / genetics*
  • Antigens, Surface / metabolism
  • Antigens, Surface / therapeutic use
  • Apoptosis
  • Arterial Occlusive Diseases / drug therapy*
  • Arterial Occlusive Diseases / genetics
  • Arterial Occlusive Diseases / pathology
  • Carotid Artery, Common / metabolism*
  • Carotid Artery, Common / pathology
  • Cell Movement / genetics
  • Cell Proliferation
  • Cells, Cultured
  • DNA / genetics*
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation*
  • Male
  • Mice
  • Mice, Knockout
  • Microscopy, Confocal
  • Milk Proteins / genetics*
  • Milk Proteins / metabolism
  • Milk Proteins / therapeutic use
  • Muscle, Smooth, Vascular / pathology
  • Polymerization

Substances

  • Actins
  • Antigens, Surface
  • Mfge8 protein, mouse
  • Milk Proteins
  • DNA