Osteocalcin

Michael Scally MD

Doctor of Medicine
10+ Year Member
De Toni L, Di Nisio A, Rocca MS, De Rocco Ponce M, Ferlin A, Foresta C. Osteocalcin, a bone-derived hormone with important andrological implications. Andrology. http://onlinelibrary.wiley.com/doi/10.1111/andr.12359/abstract

Increasing evidence disclosed the existence of a novel multi-organ endocrine pathway, involving bone, pancreas and testis, of high penetrance in energy metabolism and male fertility.

The main mediator of this axis is undercarboxylated osteocalcin (ucOC), a bone-derived protein-exerting systemic effects on tissues expressing the metabotropic receptor GPRC6A.

The recognized effects of ucOC are the improvement of insulin secretion from the pancreas, the amelioration of systemic insulin sensitivity, in particular in skeletal muscle, and the stimulation of the global endocrine activity of the Leydig cell, including vitamin D 25-hydroxylation and testosterone production.

The supporting evidence of this circuit in both animal and human models is here reviewed, with particular emphasis on the role of ucOC on testis function. The possible pharmacological modulation of this hormonal circuit for therapeutic aims is also discussed.



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The multi-organ hormonal circuit, involving bone, testis and pancreas, suggested to regulate energy metabolism and male fertility.

According to this model, carboxylated osteocalcin (OC) in the bone extracellular matrix is decarboxylated into undercarboxylated OC (ucOC) and released in the bloodstream where it exerts systemic effects on tissues-expressing GPRC6A, the recognized receptor of ucOC.

On pancreas, ucOC stimulates Langerhans b-cells (b-Cells) proliferation and improves insulin (Ins) secretion. In turn Ins, acting through the insulin receptor (InsR), promotes the decarboxylation of OC in the bone, by enhancing the acidification of extracellular matrix in resorption lacunae operated by osteoblasts.

This effect is ascribed to the InsR-dependent inhibition of osteoprotegerin (Opg) release by osteoblasts. The consequent reduction in the Opg/Receptor activator of nuclear factor kappa-B ligand (RANKL) ratio triggers the bone-remodelling activity of osteoblasts.

On adipose tissue, ucOC stimulates the production of adiponectin that ameliorates systemic insulin sensitivity, in particular, in skeletal muscle. Skeletal muscle itself is a target tissue of ucOC, being stimulated for mass maintenance and metabolic proficiency.

Together with the luteinizing hormone (LH)/LH-receptor (LHR) axis, ucOC stimulates the global endocrine activity of the Leydig cell, including Vit D 25-hydroxylation (25OHVitD) and testosterone (T) production.

The possible role of ucOC on INSL3 production by Leydig cells has not been investigated yet. In turn T, and likely INSL3, stimulates spermatogenesis within the seminiferous tubule, whereas 25OHVitD, T and INSL3 display a recognized positive effect on bone formation.

The known effects of Leydig cell hormones on adipocytes and skeletal muscle metabolism have not been indicated.

Discontinuous arrows indicate the hormone release. Continuous arrows indicate an overall effect on the whole tissue.
 
Can the positive association of osteocalcin with testosterone be unmasked when the preeminent hypothalamic-pituitary regulation of testosterone production is impaired?

PURPOSE: Osteocalcin (OCN), released from the bone matrix during the resorption phase, in its undercarboxylated form, stimulates testosterone (T) biosynthesis in mouse and a loss-of-function mutation of its receptor was associated with hypergonadotropic hypogonadism in humans. Nevertheless, when population-based studies have explored the OCN-T association, conflicting results have been reported.

Hypothesizing that the evidence of a positive association between OCN and T could have been hindered by the preeminent role of a well-functioning hypothalamus-pituitary axis in promoting T biosynthesis, we explored this association in men with chronic spinal cord injury (SCI), exhibiting high prevalence of non-hypergonadotropic androgen deficiency.


METHODS: Fifty-five consecutive men with chronic SCI underwent clinical/biochemical evaluations, including measurements of total T (TT), OCN and 25(OH)D levels. Free T (FT) levels were calculated by the Vermeulen formula. Comorbidity was scored by Charlson comorbidity index (CCI).

RESULTS: A biochemical androgen deficiency (TT < 300 ng/dL) was observed in 15 patients (27.3%). TT was positively correlated with OCN, 25(OH)D and leisure time physical activity and negatively correlated with age, BMI and CCI. OCN was also positively correlated with calculated FT and negatively correlated with BMI and HOMA-IR. At the multiple linear regression analyses, a positive association of OCN with TT and calculated FT persisted after adjustment for confounders.

CONCLUSIONS: The positive association here found between OCN and T levels in men with chronic SCI reinforces the notion that a bone-testis axis is also functioning in humans and suggests that it can be unmasked when the preeminent hypothalamic-pituitary regulation of T production is impaired.

Barbonetti A, D'Andrea S, Samavat J, et al. Can the positive association of osteocalcin with testosterone be unmasked when the preeminent hypothalamic-pituitary regulation of testosterone production is impaired? The model of spinal cord injury. Journal of endocrinological investigation 2018. https://link.springer.com/article/10.1007%2Fs40618-018-0897-x
 
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[OA] Osteocalcin Levels in Male Idiopathic Hypogonadotropic Hypogonadism: Relationship With the Testosterone Secretion and Metabolic Profiles

Idiopathic hypogonadotropic hypogonadism (IHH) patients are characterized by the absence of puberty and varying degrees of deteriorated metabolic conditions. Osteocalcin (OC) could regulate testosterone secretion and energy metabolism, but it remains unknown whether such an effect exists in IHH patients. Our study is aimed to examine the relationship between serum OC levels with testosterone and its responsiveness to gonadotropin stimulation and metabolic profiles in male IHH patients.

A total of 99 male patients aged 18-37 years and diagnosed with IHH were enrolled in the current study, and the relationships between OC and testicular volume, baseline total testosterone (TT), free testosterone (FT), and peak TT (Tmax) levels after human chorionic gonadotropin (hCG) stimulation, gonadotropin responsiveness index (GRI), which is calculated by dividing Tmax by testicular volume, as well as metabolic profiles, such as 2-h post-challenge glucose (2hPG) and fat percentage (fat%), were analyzed.

The results showed that OC had an independent negative relationship with testicular volume (r = -0.253, P = 0.012) and a positive association with Tmax (r = 0.262, P = 0.014) after adjusting for confounders. In addition, OC was a major determinant of GRI (adjusted R (2) for the model = 0.164, P = 0.012), fat% (adjusted R (2) for the model = 0.100, P = 0.004), and 2hPG (adjusted R (2) for the model = 0.054, P = 0.013) in IHH patients.

In conclusion, OC is associated with testosterone secretion upon gonadotropin stimulation, glucose metabolism, and fat mass variations in IHH. This study was registered at clinicaltrials.gov (NCT02310074).

Yang YY, Zheng SC, Wang WC, et al. Osteocalcin Levels in Male Idiopathic Hypogonadotropic Hypogonadism: Relationship With the Testosterone Secretion and Metabolic Profiles. Front Endocrinol (Lausanne) 2019;10:687. Osteocalcin Levels in Male Idiopathic Hypogonadotropic Hypogonadism: Relationship With the Testosterone Secretion and Metabolic Profiles
 
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What is the function of osteocalcin?

Highlights
· Osteocalcin is not involved in the regulation of bone quantity.
· Osteocalcin is essential for the alignment of apatite crystals.
· Osteocalcin is required for optimal bone strength.
· Osteocalcin does not function as a hormone.

Background - Osteocalcin is the most abundant non-collagenous protein in bone and is specifically expressed in osteoblasts. Previous studies using osteocalcin-deficient (Ocn–/–) mice demonstrated that osteocalcin inhibits bone formation, and serum uncarboxylated osteocalcin functions as a hormone that improves glucose metabolism, induces testosterone synthesis in the testes, and maintains muscle mass. Furthermore, the relationship between serum osteocalcin and glucose metabolism or cardiovascular risk in humans has been reported. However, new Ocn–/– mice exhibited different phenotypes.

Highlight - Bone volume, formation, and resorption were normal in the new Ocn–/– mice. The orientation of collagen fibers was parallel to the bone longitudinal direction and the size of apatite crystals was normal, but the c-axis of apatite crystals was random and bone strength was reduced in new Ocn–/– mice. Glucose metabolism, testosterone synthesis, and muscle mass were normal in new Ocn–/– mice. Exercise improved glucose metabolism and increased bone formation, leading to an increase in the serum osteocalcin level, which is a marker for bone formation.

Conclusion - Contrary to previous findings, new Ocn–/– mice revealed that osteocalcin has no function in the regulation of bone quantity, but instead, functions to direct the parallel alignment of the c-axis of apatite crystals with collagen fibrils. Moreover, it has no physiological function as a hormone that regulates glucose metabolism, testosterone synthesis, or muscle mass. These controversial phenotypes require further investigation. The relationship of serum osteocalcin with glucose metabolism or cardiovascular risk suggests the importance of exercise for their improvement.

Komori T. What is the function of osteocalcin? [published online ahead of print, 2020 Jun 11]. J Oral Biosci. 2020;S1349-0079(20)30054-2. doi:10.1016/j.job.2020.05.004 What is the function of osteocalcin? - ScienceDirect
 
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