Piezo1-mediated M2 macrophage mechanotransduction enhances bone formation through secretion and activation of transforming growth factor-β1

Cell Prolif. 2023 Sep;56(9):e13440. doi: 10.1111/cpr.13440. Epub 2023 Mar 7.

Abstract

Macrophages are multifunctional immune system cells that are essential for the mechanical stimulation-induced control of metabolism. Piezo1 is a non-selective calcium channel expressed in multifarious tissues to convey mechanical signals. Here, a cellular model of tension was used to study the effect of mechanical stretch on the phenotypic transformation of macrophages and its mechanism. An indirect co-culture system was used to explore the effect of macrophage activation on bone marrow mesenchymal stem cells (BMSCs), and a treadmill running model was used to validate the mechanism in vivo for in vitro studies. p53 was acetylated and deacetylated by macrophages as a result of mechanical strain being detected by Piezo1. This process is able to polarize macrophages towards M2 and secretes transforming growth factor-beta (TGF-β1), which subsequently stimulates BMSCs migration, proliferation and osteogenic differentiation. Knockdown of Piezo1 inhibits the conversion of macrophages to the reparative phenotype, thereby affecting bone remodelling. Blockade of TGF-β I, II receptors and Piezo1 significantly reduced exercise-increased bone mass in mice. In conclusion, we showed that mechanical tension causes calcium influx, p53 deacetylation, macrophage polarization towards M2 and TGF-β1 release through Piezo1. These events support BMSC osteogenesis.

MeSH terms

  • Animals
  • Cell Differentiation
  • Ion Channels
  • Macrophages / metabolism
  • Mechanotransduction, Cellular
  • Mice
  • Osteogenesis*
  • Transforming Growth Factor beta1* / metabolism
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Transforming Growth Factor beta1
  • Tumor Suppressor Protein p53
  • Piezo1 protein, mouse
  • Ion Channels