Dietary restriction (DR) improves whole-body metabolism, extends lifespan and reduces reproductive function. While the mechanisms leading to these profound physiological changes remain to be elucidated, suppression of mammalian target of rapamycin complex 1 (mTORC1) is thought to play a critical role. The skeleton has recently emerged as a critical endocrine tissue that regulates glucose and energy metabolism and male reproductive function, via release of the bone-specific hormone osteocalcin (OCN), suggesting that suppression of mTORC1 in the skeleton could play a crucial role in the physiological responses to DR.
To investigate the role of skeletal-mTORC1 in modulating glucose metabolism and male fertility, we generated mice in which raptor, an essential component of mTORC1, is specifically deleted in osteoblasts (RaptorOB-/-). RaptorOB-/- mice are significantly smaller than controls, are osteopenic, have increased bone marrow adipose tissue (MAT) and reduced serum OCN levels. Compared to controls, serum adiponectin levels are significantly elevated in RaptorOB-/- animals, while leptin levels are reduced. Serum triglyceride levels are also significantly reduced in RaptorOB-/-, while free fatty acid levels are elevated. Importantly, despite being hypoinsulinemic, RaptorOB-/- have significantly lower fasting glucose levels, suggestive of insulin hypersensitivity. Consistent with this, insulin and glucose tolerance tests have revealed that RaptorOB-/- mice have improved glucose tolerance, enhanced insulin sensitivity and elevated insulin secretion. Furthermore, the reproductive function of RaptorOB-/- mice is significantly impaired, as evidenced by reduced circulating testosterone levels and sperm counts. Collectively, our results demonstrate that physiological changes associated with DR (e.g. elevated MAT and circulating adiponectin levels, reduced leptin and triglyceride levels, improved glucose metabolism and impaired male reproductive function) are mirrored in RaptorOB-/-mice, which suggests that skeletal-mTORC1 signalling is critical in mediating cellular responses to DR. These data highlight an essential role for the skeleton in monitoring global nutritional status.