Skeletal muscle and bone are connected anatomically and physiologically, and play a crucial role in human locomotion and metabolism. Historically, the coupling between muscle and bone has been viewed in light of mechanotransduction, which dictates that the mechanical forces applied to muscle are transmitted to the skeleton to initiate bone formation. However, these organs also communicate through the endocrine system, orchestrated by a family of cytokines namely myokines (derived from myocytes) and osteokines (derived from bone cells). A third player in this biochemical crosstalk is adipose tissue and the secretion of adipokines (derived from adipocytes). In this review, we discuss the bidirectional effects of myokines and osteokines on muscle and bone metabolism, and the impact of adipokines on both of these secretory organs. Several myokines, notably, IL6, irisin, IGF-1, BDNF, myostatin, and FGF2 exert anabolic/catabolic effects on bone, while the osteokines osteocalcin and sclerostin have shown to induce muscle anabolism and catabolism, respectively. Adipokines, such as leptin, resistin, adiponectin, and TNFα (released from adipose tissue), can also modulate muscle and bone metabolism. Contrarily, exercise-mediated release of lipolytic myokines (IL6, irisin, and LIF) stimulates thermogenesis by promoting the browning of adipocytes. Myokines, osteokines, and adipokines exert autocrine/paracrine effects locally as well as through the endocrine system, to regulate muscle, bone, and fat metabolism. Reductions in physical activity and increases in energy intake, both linked with aging, leads to adipocyte hypertrophy and the recruitment of immunological cells (macrophages). In turn, this releases pro-inflammatory adipokines which induces chronic low-grade inflammation (LGI), a key player in the pathology of several diseases. However, exercise-induced stimulation of bioactive cytokines, through muscle-bone-fat crosstalk, increases muscle anabolism, bone formation, mitochondrial biogenesis, glucose utilization, and fatty acid oxidation, and attenuates chronic LGI.

Muscle, Bone, and Fat Crosstalk: the Biological Role of Myokines, Osteokines, and Adipokines

Bone has long been regarded as a static organ, simply providing protection and support. However, this mindset has changed radically in recent years and bone is becoming increasingly recognized for its endocrine function of secreting several hormones, thereby controlling various physiological pathways. One of the factors released by the skeleton is osteocalcin. Importantly, osteocalcin is secreted solely by osteoblasts but only has minor effects on bone mineralization and density. Instead, it has been reported to control several physiological processes in an endocrine manner, such as glucose homeostasis and exercise capacity, brain development, cognition, and male fertility. The aim of this review is to provide an overview of the currently known roles of osteocalcin and their underlying mechanisms. At present, one of the major goals in this field is translating basic research into therapeutic applications, therefore ongoing efforts to bring these findings to the clinics will also be discussed.

Osteocalcin-A Versatile Bone-Derived Hormone.

Recent advances have indicated that osteocalcin, and in particular its undercarboxylated form (ucOC), is not only a nutritional biomarker reflective of vitamin K status and an indicator of bone health but also an active hormone that mediates glucose metabolism in experimental studies. This work has been supported by the putative identification of G protein-coupled receptor, class C, group 6, member A (GPRC6A) as a cell surface receptor for ucOC. Of note, ucOC has been associated with diabetes and with cardiovascular risk in epidemiological studies, consistent with a pathophysiological role for ucOC in vivo. Limitations of existing knowledge include uncertainty regarding the underlying mechanisms by which ucOC interacts with GPRC6A to modulate metabolic and cardiovascular outcomes, technical issues with commonly used assays for ucOC in serum, and a paucity of clinical trials to prove causation and illuminate the scope for novel health interventions. A key emerging area of research is the role of ucOC in relation to expression of GPRC6A in muscle, and whether exercise interventions may modulate metabolic outcomes favorably in part via ucOC. Further research is warranted to clarify potential direct and indirect roles for ucOC in human health and cardiometabolic diseases.

Undercarboxylated Osteocalcin: Experimental and Human Evidence for a Role in Glucose Homeostasis and Muscle Regulation of Insulin Sensitivity

The acute exercise effects on bone markers in adults are unclear, while in children, there are no such data.
 To investigate the acute response of biochemical markers of bone turnover to a high-impact exercise session consisting of high-mechanical loading in boys and young men. Twelve boys (10.2 ± 0.4 years) and 14 men (22.0 ± 0.8 years) underwent a protocol of plyometric jumping exercises (total 144 jumps). Venous blood samples were collected pre-, 5 min, 1 and 24 h post-exercise, and analyzed for markers of bone formation and resorption: bone-specific alkaline phosphatase (bone ALP), osteoprotegerin (OPG), amino-terminal cross-linking telopeptide (NTx), and receptor activator of nuclear factor kappa beta ligand (RANKL). Boys had higher resting bone ALP (111.9 ± 29.2 vs. 30.6 ± 11.2 µg/L, p < 0.05) and NTx levels (49.8 ± 13.2 vs. 21.7 ± 5.9 nM BCE, p < 0.05) than men but no group differences were observed in resting OPG or RANKL. Following exercise (24 h), bone ALP and NTx increased in both boys and men (bone ALP: 24.1 vs. 9.9 %, respectively; NTx: 23.5 vs. −5 %, respectively), although the group-by-time interaction was not statistically significant. OPG increased significantly (p < 0.05) in both groups (5.7 and 16.1 %, respectively). Even one session of plyometric exercises appear to stimulate bone formation in boys and men, as reflected by the increase in bone ALP and OPG. The boys’ response appears more pronounced than the men’s, suggesting that during growth, cellular bone activities respond with greater magnitude to mechanical stimuli.

Effects of plyometric exercise session on markers of bone turnover in boys and young men.

Gonzalez de Aguero, A., Vicente-Rodriguez, G., Gomez-Cabello, A., Ara, I., Moreno, L. A., Casajus, J. A. (2012). A 21-week bone deposition promoting exercise programme increases bone mass in young people with Down syndrome. Developmental medicine and child neurology, 54 (6), 552-556. © The Authors. Developmental Medicine & Child Neurology © 2012 Mac Keith Press.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-8749.2012.04262.x

A 21-week bone deposition promoting exercise programme increases bone mass in young people with Down syndrome.

The purpose of this study was to investigate whether different modes of single-bout exercise would cause different responses in short-term bone metabolism. 24 untrained male college students (19.1 ± 0.1 years old) were recruited and randomly assigned to three groups: (1) a single-bout plyometric exercise group (the PL group, n = 8), (2) a 200-meter × 10 intermittent running group (the IR group, n = 8) and (3) a sedentary control group, which followed the same time schedule of experimentation without performing any exercise (the CON group, n = 8). Serial blood samples were collected before (baseline) and 5 min, 15 min, 1 h, 3 h, 6 h, 24 h, 48 h, and 72 h after exercise trials. Within 15 min of exercise, the PL and IR groups showed significantly higher serum phosphorus than did the control group (P < 0.05). Osteocalcin levels were significantly higher in the PL group at 5 min and 1 h after exercise (P < 0.05), while serum tartrate-resistant acid phosphatase (TRAP) showed no differences among groups. Exercises with different mechanical impact levels responded differently in serum bone formation markers as shown by osteocalcin. Because the increase in osteocalcin in the PL group was revealed shortly after the exercise bout, the changes might due to an exercise-induced mechanical impact rather than bone cellular activities.

Acute effects of plyometric jumping and intermittent running on serum bone markers in young males

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Acute effects of plyometric jumping and intermittent running on serum bone markers in young males