Controlled mineralisation of the collagen matrix is essential to maintain optimum bone strength. Previous work has shown that mice with EphrinB2 (Efnb2) knockdown in osteocytes develop brittle bones with a high level of mineralisation and abundant autophagosome numbers within osteocytes. In this study, we sought to determine mechanisms by which autophagy in osteocytes is regulated by EphrinB2 and restrains mineralisation.
To determine whether increased autophagy increases mineralisation, two osteocyte-like cell lines (OCY454 and Kusa 4b10) were treated under mineralising conditions with the autophagy inducer rapamycin. This increased mineral deposition in both cell lines, confirming that stimulation of autophagy in osteocytes promotes mineral deposition. In addition, EphrinB2-Fc treatment suppressed bafilomycinA1-induced accumulation of LC3 positive autophagosomes. This effect of EphrinB2-Fc was blocked by the RhoA/ROCK inhibitor H1152, indicating that EphrinB2 regulates autophagy, at least in part, through RhoA/ROCK signalling.
Autophagy is the natural intracellular recycling pathway used to degrade damaged organelles and proteins, and depends on fusion of autophagosomes with lysosomes. In addition to elevated autophagosome numbers, Efnb2-deficient osteocytes demonstrated a significant (>50%) decrease in both lysosomal markers Lamp-1 and LysoTracker by quantitative confocal microscopy. Furthermore, the cis-Golgi network marker GM130 was significantly (70%) lower in Efnb2-deficient osteocytes compared to vector control cells. This indicates that increased autophagosome numbers in the absence of EphrinB2 occurs due to insufficient lysosome biogenesis and a defect in at least the cis compartment of the Golgi apparatus.
Our data reveals a novel pathway by which mineralisation and bone strength are maintained. It suggests that autophagy increases mineralisation by osteocytes, and that in these cells Efnb2 knockdown leads to accumulation of autophagosomes because of impaired lysosome formation and disruption of the Golgi apparatus. These findings provide the first suggestion that increased bone mineralisation may result from a lysosomal storage disorder prevented by EphrinB2 in osteocytes.