Phosphoinositide 3-kinase (PI3K) signaling is an intracellular pathway activated by G protein-coupled and cytokine receptors. Bone formation can be stimulated by elevated PI3K signaling in response to mechanical loading and in some pathologies (e.g. CLOVES syndrome). Our aim was to determine whether PI3K activation specific to the osteoblast lineage could increase bone mass.
We generated a mouse (DPK) where PI3K signaling is activated in osteocytes and endocortical osteoblasts using dentin matrix protein-1 Cre (Dmp1Tg) and the Pik3caH1047R knock-in allele (PI3Kca). We confirmed PI3K activation in bone by Western blot. Micro-computed tomography identified no differences in femoral length between DPK (DMPTg.PI3Kca/+) mice and littermate controls. While there were no detectable changes in trabecular bone, DPK mice had ~50% greater cortical bone mass than age-matched controls at all ages assessed (6-, 12-, 18-, 24-weeks-old). Notably, while bone mass reached a peak and plateaud in control mice, DPK mice continued to accumulate bone in the mature skeleton. Three-point bend tests showed 12-week-old DPK bones had almost double the strength of controls (ultimate force before breaking was 82% greater), indicating that targeted PI3K activation can specifically increase cortical bone strength.
No differences in osteoclast parameters were observed by histomorphometry. Consistent with greater cross-sectional area, periosteal bone formation rate was doubled in DPK mice. This indicates that DMPTg-targeted PI3K activation specifically increases bone formation at the periosteum. However, by lineage tracing, DMPTg was not active in periosteal cells, but only in osteocytes and endocortical osteoblasts. Furthermore, RNAseq analysis of isolated cortical bone shafts did not identify any changes in known pathways that stimulate bone formation.
In conclusion, targeting PI3K activation to Dmp1cre+ cells promotes periosteal bone formation indirectly, and without stimulating known bone formation pathways. This suggests a novel mechanism that could inform approaches to stimulate periosteal bone formation and thereby increase cortical bone strength.