Image: Runx2 in athersclerotic blood vessels. Arrows point to the Runx2 positive osteochondrogenic cells.

Abstract

Aims Vascular smooth muscle cells (SMCs) are major precursors contributing to osteochondrogenesis and calcification in atherosclerosis. Runt-related transcription factor-2 (Runx2) has been found essential for SMC differentiation to an osteochondrogenic phenotype and subsequent calcification in vitro. A recent study using a conditional targeting allele that produced a truncated Runx2 protein in SMCs of ApoE?/? mice showed reduced vascular calcification, likely occurring via reduction of receptor activator of nuclear factor-?B ligand (RANKL), macrophage infiltration, and atherosclerotic lesion formation. Using an improved conditional Runx2 knockout mouse model, we have elucidated new roles for SMC-specific Runx2 in arterial intimal calcification (AIC) without effects on atherosclerotic lesion size.

Methods and results We used an improved targeting construct to generate LDLr?/? mice with floxed-Runx2 alleles (LDLr?/?:Runx2f/f) such that Cre-mediated recombination (LDLr?/?:Runx2?SM) does not produce functional truncated Runx2 protein, thereby avoiding off-target effects. We found that both LDLr?/?:Runx2f/f and LDLr?/?:Runx2?SM mice fed with a high fat diet developed atherosclerosis. SMC-specific Runx2 deletion did not significantly reduce atherosclerotic lesion size, macrophage number, or expression of RANKL, MCP-1, and CCR2. However, it significantly reduced AIC by 50%. Mechanistically, Sox9 and type II collagen were unaltered in vessels of LDLr?/?:Runx2?SM mice compared to LDLr?/?:Runx2f/f counterparts, while type X collagen, MMP13 and the osteoblastic marker osteocalcin were significantly reduced.

Conclusions SMC autonomous Runx2 is required for SMC differentiation towards osteoblast-like cells, SMC-derived chondrocyte maturation and AIC in atherosclerotic mice. These effects were independent of systemic lipid metabolism, RANKL expression, macrophage infiltration, and atheromatous lesion progression.