Cross-talk between macrophages and smooth muscle cells impairs collagen and metalloprotease synthesis and promotes angiogenesis

Biochim Biophys Acta. 2016 Jul;1863(7 Pt A):1568-78. doi: 10.1016/j.bbamcr.2016.04.001. Epub 2016 Apr 7.

Abstract

Coronary atherosclerosis complicated by plaque disruption and thrombosis is a critical event in myocardial infarction and stroke, the major causes of cardiovascular death. In atherogenesis, macrophages (MAC) and smooth muscle cells (SMC) are key actors; they synthesize matrix components and numerous factors involved in the process. Here, we design experiments to investigate whether SMC-MAC communication induces changes in ECM protein composition and/or neo-angiogenesis. Cell to cell communication was achieved using trans-well chambers, where SMCs were grown in the upper chamber and differentiated MAC in the bottom chamber for 24 or 72h. We found that cross-talk between MAC and SMC during co-culture: (i) significantly decreased the expression of ECM proteins (collagen I, III, elastin) in SMC; (ii) increased the expression and activity of metalloprotease MMP-9 and expression of collagenase MMP-1, in both MAC and SMC; (iii) augmented the secretion of soluble VEGF in the conditioned media of cell co-culture and VEGF gene expression in both cell types, compared with control cells. Moreover, the conditioned media collected from MAC-SMC co-culture promoted endothelial cell tube formation in Matrigel, signifying an increased angiogenic effect. In addition, the MAC-SMC communication led to an increase in inflammatory IL-1β and TLR-2, which could be responsible for cellular signaling. In conclusion, MAC-SMC communication affects factors and molecules that could alter ECM composition and neo-angiogenesis, features that could directly dictate the progression of atheroma towards the vulnerable plaque. Targeting the MAC-SMC cross-talk may represent a novel therapeutic strategy to slow-down or retard the plaque progression.

Keywords: Angiogenesis; Atherosclerosis; Extracellular matrix proteins; Macrophage–SMC cross-talk; Matrix metalloproteinases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Atherosclerosis / enzymology*
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Atherosclerosis / physiopathology
  • Cell Communication*
  • Cell Line
  • Coculture Techniques
  • Collagen / metabolism*
  • Culture Media, Conditioned / metabolism
  • Humans
  • Inflammation Mediators / metabolism
  • Interleukin-1beta / metabolism
  • Macrophages / enzymology*
  • Macrophages / pathology
  • Matrix Metalloproteinase 1 / metabolism*
  • Matrix Metalloproteinase 9 / metabolism*
  • Muscle, Smooth, Vascular / enzymology*
  • Muscle, Smooth, Vascular / pathology
  • Muscle, Smooth, Vascular / physiopathology
  • Myocytes, Smooth Muscle / enzymology*
  • Myocytes, Smooth Muscle / pathology
  • Neovascularization, Physiologic*
  • RNA Interference
  • Signal Transduction
  • Time Factors
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / metabolism
  • Transfection
  • Vascular Endothelial Growth Factor A / metabolism

Substances

  • Culture Media, Conditioned
  • IL1B protein, human
  • Inflammation Mediators
  • Interleukin-1beta
  • TLR2 protein, human
  • Toll-Like Receptor 2
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Collagen
  • MMP9 protein, human
  • Matrix Metalloproteinase 9
  • MMP1 protein, human
  • Matrix Metalloproteinase 1