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Karla J Suchacki The Queen’s Medical Research Institute, The University of Edinburgh, Edinburgh, UK

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Fiona Roberts The Roslin Institute, The University of Edinburgh, Easter Bush, Midltohian

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Andrea Lovdel The Queen’s Medical Research Institute, The University of Edinburgh, Edinburgh, UK

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Colin Farquharson The Roslin Institute, The University of Edinburgh, Easter Bush, Midltohian

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Nik M Morton The Queen’s Medical Research Institute, The University of Edinburgh, Edinburgh, UK

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Vicky E MacRae The Roslin Institute, The University of Edinburgh, Easter Bush, Midltohian

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William P Cawthorn The Queen’s Medical Research Institute, The University of Edinburgh, Edinburgh, UK

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Throughout the last decade, significant developments in cellular, molecular and mouse models have revealed major endocrine functions of the skeleton. More recent studies have evolved the interplay between bone-specific hormones, the skeleton, marrow adipose tissue, muscle and the brain. This review focuses on literature from the last decade, addressing the endocrine regulation of global energy metabolism via the skeleton. In addition, we will highlight several recent studies that further our knowledge of new endocrine functions of some organs; explore remaining unanswered questions; and, finally, we will discuss future directions for this more complex era of bone biology research.

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Andrea Lovdel University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Karla J Suchacki University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Fiona Roberts University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Richard J Sulston University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Robert J Wallace Department of Orthopaedics, The University of Edinburgh, Edinburgh, UK

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Benjamin J Thomas University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Rachel M B Bell University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Iris Pruñonosa Cervera University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Gavin J Macpherson Department of Orthopaedic Surgery, Royal Infirmary of Edinburgh, Edinburgh, UK

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Nicholas M Morton University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK
Centre for Systems Health and Integrated Metabolic Research, Department of Biosciences, School of Science and Technology, Nottingham Trent University, Nottingham, UK

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Natalie Z M Homer University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Karen E Chapman University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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William P Cawthorn University/BHF Centre for Cardiovascular Science, The University of Edinburgh, The Queen’s Medical Research Institute, Edinburgh BioQuarter, Edinburgh, UK

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Bone marrow adipose tissue (BMAT) comprises >10% of total adipose mass in healthy humans. It increases in diverse conditions, including ageing, obesity, osteoporosis, glucocorticoid therapy, and notably, during caloric restriction (CR). BMAT potentially influences skeletal, metabolic, and immune functions, but the mechanisms of BMAT expansion remain poorly understood. Our hypothesis is that, during CR, excessive glucocorticoid activity drives BMAT expansion. The enzyme 11β-hydroxysteroid dehydrogenase type 1 (11β-HSD1) amplifies glucocorticoid activity by catalysing intracellular regeneration of active glucocorticoids from inert 11-keto forms. Mice lacking 11β-HSD1 resist metabolic dysregulation and bone loss during exogenous glucocorticoid excess; thus, we hypothesised that 11β-HSD1 knockout mice would also resist excessive glucocorticoid action during CR, thereby restrining BMAT expansion and bone loss. To test this, we first confirmed that 11β-HSD1 is expressed in mouse and human bone marrow. We then investigated the effects of CR in male and female control and 11β-HSD1 knockout mice from 9 to 15 weeks of age. CR increased Hsd11b1 mRNA in adipose tissue and bone marrow. Deletion of Hsd11b1 did not alter bone or BMAT characteristics in mice fed a control diet and had little effect on tibial bone microarchitecture during CR. Notably, Hsd11b1 deletion attenuated the CR-induced increases in BMAT and prevented increases in bone marrow corticosterone in males but not females. This was not associated with suppression of glucocorticoid target genes in bone marrow. Instead, knockout males had increased progesterone in plasma and bone marrow. Together, our findings show that knockout of 11β-HSD1 prevents CR-induced BMAT expansion in a sex-specific manner and highlights progesterone as a potential new regulator of bone marrow adiposity.

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