Effects of repetitive loading on the growth-induced changes in bone mass and cortical bone geometry: A 12-month study in pre/peri- and postmenarcheal tennis players

Ducher, Ga͏ële; Bass, Shona; Saxon, Leanne; Daly, Robin M.

doi:10.1002/jbmr.323

Cited by 61 publications

(60 citation statements)

References 31 publications

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“…There was no change in thickness, number, and separation of trabeculae in r-irisin-treated compared with control mice. Although it remains unclear why osteoblasts at cortical surfaces will behave differently from those synthesizing trabecular bone, our observation is in line with data indicating greater sensitivity of cortical bone to anabolic factors released by muscle (26,27,35). The selective action of r-irisin on cortical bone is likely to be related to the different functionalities of cortical and trabecular bone.…”

Section: Discussionsupporting

confidence: 89%

“…Specifically, by distributing bone mass away from the center, enlarged bone perimeter and cross-sectional area both contribute to increased pMOI and resistance to bending. The effect of r-irisin, essentially mimicking the effect of mechanotransduction (25)(26)(27), thus allows bone to become structurally more efficient for bending and torsion. Indeed, both mouse (28)(29)(30) and rat (31-34) models have collectively shown positive associations between exercise and increased bone size and bone mass.…”

Section: Discussionmentioning

confidence: 99%

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The myokine irisin increases cortical bone mass

Colaianni

Cuscito

Mongelli

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

415

399

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It is unclear how physical activity stimulates new bone synthesis. We explored whether irisin, a newly discovered myokine released upon physical activity, displays anabolic actions on the skeleton. Young male mice were injected with vehicle or recombinant irisin (r-irisin) at a low cumulative weekly dose of 100 µg kg(-1). We observed significant increases in cortical bone mass and strength, notably in cortical tissue mineral density, periosteal circumference, polar moment of inertia, and bending strength. This anabolic action was mediated primarily through the stimulation of bone formation, but with parallel notable reductions in osteoclast numbers. The trabecular compartment of the same bones was spared, as were vertebrae from the same mice. Higher irisin doses (3,500 µg kg(-1) per week) cause browning of adipose tissue; this was not seen with low-dose r-irisin. Expectedly, low-dose r-irisin modulated the skeletal genes, Opn and Sost, but not Ucp1 or Pparγ expression in white adipose tissue. In bone marrow stromal cell cultures, r-irisin rapidly phosphorylated Erk, and up-regulated Atf4, Runx2, Osx, Lrp5, β-catenin, Alp, and Col1a1; this is consistent with a direct receptor-mediated action to stimulate osteogenesis. We also noted that, although the irisin precursor Fndc5 was expressed abundantly in skeletal muscle, other sites, such as bone and brain, also expressed Fndc5, albeit at low levels. Furthermore, muscle fibers from r-irisin-injected mice displayed enhanced Fndc5 positivity, and irisin induced Fdnc5 mRNA expression in cultured myoblasts. Our data therefore highlight a previously unknown action of the myokine irisin, which may be the molecular entity responsible for muscle-bone connectivity

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Section: Discussionsupporting

confidence: 89%

Section: Discussionmentioning

confidence: 99%

The myokine irisin increases cortical bone mass

Colaianni

Cuscito

Mongelli

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

415

399

View full text Add to dashboard Cite

show abstract

“…Previous cross-sectional and unilateral studies in athletes (eg, tennis players) have reported that bone structural adaptations to loading during growth are maturity-dependent and sexspecific. (23)(24)(25) Prior to puberty, exercise appears to enhance periosteal apposition in both boys and girls, whereas exercise during or after puberty appears to promote periosteal expansion in boys and endocortical apposition (or reduced resorption) in girls. As indicated above, in our study in which the children were prepubertal at baseline we observed no effect of SPE on periosteal apposition (total bone area) in either sex, but there was evidence of reduced endocortical resorption at the mid-tibia in both sexes and the mid-radius in girls.…”

Section: Discussionmentioning

confidence: 99%

Effects of a Specialist-Led, School Physical Education Program on Bone Mass, Structure, and Strength in Primary School Children: A 4-Year Cluster Randomized Controlled Trial

Daly

Ducher

Hill

et al. 2015

Journal of Bone and Mineral Research

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This 4-year cluster randomized controlled trial of 365 boys and 362 girls (mean age 8.1 AE 0.3 years) from grade 2 in 29 primary schools investigated the effects of a specialist-taught physical education (PE) program on bone strength and body composition. All children received 150 min/week of common practice (CP) PE from general classroom teachers but in 13 schools 100 min/week of CP PE was replaced by specialized-led PE (SPE) by teachers who emphasized more vigorous exercise/games combined with static and dynamic postural activities involving muscle strength. Outcome measures assessed in grades 2, 4, and 6 included: total body bone mineral content (BMC), lean mass (LM), and fat mass (FM) by DXA, and radius and tibia (4% and 66% sites) bone structure, volumetric density and strength, and muscle cross-sectional area (CSA) by pQCT. After 4-years, gains in total body BMC, FM, and muscle CSA were similar between the groups in both sexes, but girls in the SPE group experienced a greater gain in total body LM (mean 1.0 kg; 95% CI, 0.2 to 1.9 kg). Compared to CP, girls in the SPE group also had greater gains in cortical area (CoA) and cortical thickness (CoTh) at the mid-tibia (CoA, 5.0% [95% CI, 0.2% to 1.9%]; CoTh, 7.5% [95% CI, 2.4% to 12.6%]) and mid-radius (CoA, 9.3% [95% CI, 3.5% to 15.1%]; CoTh, 14.4% [95% CI, 6.1% to 22.7%]), whereas SPE boys had a 5.2% (95% CI, 0.4% to 10.0%) greater gain in mid-tibia CoTh. These benefits were due to reduced endocortical expansion. There were no significant benefits of SPE on total bone area, cortical density or bone strength at the mid-shaft sites, nor any appreciable effects at the distal skeletal sites. This study indicates that a specialist-led school-based PE program improves cortical bone structure, due to reduced endocortical expansion. This finding challenges the notion that periosteal apposition is the predominant response of bone to loading during the prepubertal and early-pubertal period.

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“…However, this is also in line with previous literature data reporting that cortical bone is more sensitive to myokines or other anabolic factors released by muscle. [25][26][27] Notably, change in the expression myostatin, also released from skeletal muscle, undergoes opposite direction to Irisin release following exercise, as it has been shown that myostatin signaling is inhibited by acute resistance exercise. 28 In addition, myostatin knock out mice displayed BATexpansion, an effect mediated by the AMPK-PGC1a-FNDC5 pathway in skeletal muscle.…”

Section: Irisin the Messenger Of Healthy Bone-muscle Unitmentioning

confidence: 99%

Role of Irisin on the bone–muscle functional unit

Colaianni

Grano

2015

BoneKEy Reports

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Irisin was originally recognized as a hormone-like myokine secreted as a product of fibronectin type III domain containing 5 from skeletal muscle in response to exercise both in mice and humans. The first role attributed to Irisin was its ability to induce trans-differentiation of white adipose tissue into brown, but we recently demonstrated that Irisin also has a central role in the control of bone mass, even at lower concentration than required to induce the browning response. Considering how physical exercise is important for the development of an efficient load-bearing skeleton, we can now consider this myokine as one of the molecules responsible for the positive correlation between exercise and healthy bone, linking to the well-established relationship between muscle and bone. Recombinant Irisin (r-Irisin), administered at low dose in young mice, increases cortical bone mineral density and positively modifies bone geometry. Irisin exerts its effect prevalently on osteoblast lineage by enhancing differentiation and activity of bone-forming cells, through the increase in activating transcription factor 4 expression. Low-dose r-Irisin also increases osteopontin and decreases sclerostin synthesis but did not affect Uncoupling protein 1 expression in white adipose tissue, whose upregulation is known to cause browning of fat, when Irisin is administered at a higher dose. These findings offer an explanation to the positive outcome on the skeleton triggered by skeletal muscle during physical activity and prove that the bone tissue is more sensitive than the adipose tissue to the Irisin action.

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Effects of repetitive loading on the growth-induced changes in bone mass and cortical bone geometry: A 12-month study in pre/peri- and postmenarcheal tennis players

Cited by 61 publications

References 31 publications

The myokine irisin increases cortical bone mass

The myokine irisin increases cortical bone mass

Effects of a Specialist-Led, School Physical Education Program on Bone Mass, Structure, and Strength in Primary School Children: A 4-Year Cluster Randomized Controlled Trial

Role of Irisin on the bone–muscle functional unit

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