Vascular smooth muscle cell-derived transforming growth factor-β promotes maturation of activated, neointima lesion-like macrophages

Arterioscler Thromb Vasc Biol. 2014 Apr;34(4):877-86. doi: 10.1161/ATVBAHA.114.303214. Epub 2014 Feb 13.

Abstract

Objective: To define the contribution of vascular smooth muscle cell (SMC)-derived factors to macrophage phenotypic modulation in the setting of vascular injury.

Approach and results: By flow cytometry, macrophages (M4) were the predominant myeloid cell type recruited to wire-injured femoral arteries, in mouse, compared with neutrophils or eosinophils. Recruited macrophages from injured vessels exhibited a distinct expression profile relative to circulating mononuclear cells (peripheral blood monocytes; increased: interleukin-6, interleukin-10, interleukin-12b, CC chemokine receptor [CCR]3, CCR7, tumor necrosis factor-α, inducible nitric oxide synthase, arginase 1; decreased: interleukin-12a, matrix metalloproteinase [MMP]9). This phenotype was recapitulated in vitro by maturing rat bone marrow cells in the presence of macrophage-colony stimulating factor and 20% conditioned media from cultured rat SMC (sMϕ) compared with maturation in macrophage-colony stimulating factor alone (M0). Recombinant transforming growth factor (TGF)-β1 recapitulated the effect of SMC conditioned media. Macrophage maturation studies performed in the presence of a pan-TGF-β neutralizing antibody, a TGF-β receptor inhibitor, or conditioned media from TGF-β-depleted SMCs confirmed that the SMC-derived factor responsible for macrophage activation was TGF-β. Finally, the effect of SMC-mediated macrophage activation on SMC biology was assessed. SMCs cocultured with sMϕ exhibited increased rates of proliferation relative to SMCs cultured alone or with M0 macrophages.

Conclusions: SMC-derived TGF-β modulates the phenotype of maturing macrophages in vitro, recapitulating the phenotype found in vascular lesions in vivo. SMC-modulated macrophages induce SMC activation to a greater extent than control macrophages.

Keywords: macrophages; muscle, smooth, vascular; neointima; transforming growth factor beta; vascular system injuries.

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Cell Proliferation
  • Cells, Cultured
  • Coculture Techniques
  • Culture Media, Conditioned / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Femoral Artery / injuries
  • Femoral Artery / metabolism
  • Femoral Artery / pathology
  • Humans
  • Macrophage Activation*
  • Macrophage Colony-Stimulating Factor / metabolism
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Mice
  • Mice, Inbred C57BL
  • Muscle, Smooth, Vascular / injuries
  • Muscle, Smooth, Vascular / metabolism*
  • Muscle, Smooth, Vascular / pathology
  • Myocytes, Smooth Muscle / metabolism*
  • Myocytes, Smooth Muscle / pathology
  • Neointima*
  • Paracrine Communication*
  • Phenotype
  • RNA Interference
  • Rats
  • Time Factors
  • Transfection
  • Transforming Growth Factor beta / genetics
  • Transforming Growth Factor beta / metabolism*
  • Transforming Growth Factor beta1 / metabolism
  • Vascular System Injuries / genetics
  • Vascular System Injuries / metabolism*
  • Vascular System Injuries / pathology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Biomarkers
  • Culture Media, Conditioned
  • Cytokines
  • TGFB1 protein, human
  • Transforming Growth Factor beta
  • Transforming Growth Factor beta1
  • Macrophage Colony-Stimulating Factor
  • p38 Mitogen-Activated Protein Kinases