J Bone Metab.  2016 Aug;23(3):157-164. 10.11005/jbm.2016.23.3.157.

The Influence of the Type of Continuous Exercise Stress Applied during Growth Periods on Bone Metabolism and Osteogenesis

• Lee S
• Suzuki T
• Izawa H
• Satoh A

• KMID: 2350812
• DOI: http://doi.org/10.11005/jbm.2016.23.3.157

Abstract

BACKGROUND
In this study, we examined the influence of exercise loading characteristics on bone metabolic responses and bone morphology in the growth phase and adulthood.
METHODS
Running exercise (RUN) and jumping exercise (JUM) were used for the exercise loading in 28-day-old male Wistar rats. Bone metabolism was measured by blood osteocalcin (OC) and tartrate-resistant acid phosphatase (TRACP) levels. For bone morphology, the maximum bone length, bone weight, and bone strength of the femur and tibia were measured.
RESULTS
A pre- and post-exercise loading comparison in the growth phase showed significantly increased OC levels in the RUN and JUM groups and significantly decreased TRACP levels in the JUM group. On the other hand, a pre- and post-exercise loading comparison in adulthood showed significantly decreased TRACP levels in the RUN and JUM groups. Femur lengths were significantly shorter in the RUN and JUM groups than in the control (CON) group, while bone weight was significantly greater in the JUM group than in the CON group.
CONCLUSIONS
Exercise loading activates OC levels in the growth phase and suppresses TRACP levels in adulthood. On the other hand, these results suggest that excessive exercise loading may suppress bone length.

Keyword

Exercise; Growth; Osteoblasts; Osteoclasts; Osteogenesis; Stress mechanical

MeSH Terms

Acid Phosphatase
Femur
Hand
Humans
Male
Metabolism*
Osteoblasts
Osteocalcin
Osteoclasts
Osteogenesis*
Rats, Wistar
Running
Tibia
Acid Phosphatase
Osteocalcin

Figure

• 

  Fig. 1 Pre- versus post-exercise loading changes in Osteocalcin (OC) and Tartrate Resistant Acid Phopshatate (TRACP) in the growth phase and adulthood: Transient moderate or intense mechanical stress in the growth phase enhanced OC, while intense mechanical stress markedly suppressed TRACP. In contrast, in adulthood, TRACP was suppressed by transient moderate or intense mechanical stress. TRACP responded most particularly to intense mechanical stress and exhibited a different pattern in adulthood than in the growth phase. CON, control; RUN, running exercise; JUM, jumping exercise.

• 

  Fig. 2 Adulthood bone morphology (12 weeks): Maximum bone length of both the femur and tibia exhibited values that were inversely proportional to exercise load quantity in the order of control (CON) group>running exercise (RUN) group>jumping exercise (JUM) group. On the other hand, bone weight and maximum bending load of both the femur and the tibia exhibited values proportional to exercise load quantity in the order of JUM group>RUN group>CON group.

Reference

1. Martin T, Gooi JH, Sims NA. Molecular mechanisms in coupling of bone formation to resorption. Crit Rev Eukaryot Gene Expr. 2009; 19:73–88.

2. Lee S, Kumagai T, Hashimoto J, et al. A change of osteocalcin (OC) and tartrate resistant acid phosphatase 5b (TRACP-5b) with the menstrual cycle. Horm Metab Res. 2012; 44:699–703.

3. Filaire E, Toumi H. Reactive oxygen species and exercise on bone metabolism: friend or enemy? Joint Bone Spine. 2012; 79:341–346.

4. Sindler AL, Reyes R, Chen B, et al. Age and exercise training alter signaling through reactive oxygen species in the endothelium of skeletal muscle arterioles. J Appl Physiol (1985). 2013; 114:681–693.

5. Ofek O, Attar-Namdar M, Kram V, et al. CB2 cannabinoid receptor targets mitogenic Gi protein-cyclin D1 axis in osteoblasts. J Bone Miner Res. 2011; 26:308–316.

6. Lee S, Hashimoto J, Suzuki T, et al. Concentrated bovine-milk whey active protein (CBP) supplement-combined dynamic flamingo therapy (DFT) activates bone metabolism and bone-related factors. J Diabetes Metab. 2013; 4:251.

7. Hayden JM, Mohan S, Baylink DJ. The insulin-like growth factor system and the coupling of formation to resorption. Bone. 1995; 17:93s–98s.

8. Matsuo K, Irie N. Osteoclast-osteoblast communication. Arch Biochem Biophys. 2008; 473:201–209.

9. Xiong J, O'Brien CA. Osteocyte RANKL: new insights into the control of bone remodeling. J Bone Miner Res. 2012; 27:499–505.

10. Nakashima T, Hayashi M, Fukunaga T, et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med. 2011; 17:1231–1234.

11. Fonseca H, Moreira-Gonçalves D, Esteves JL, et al. Voluntary exercise has long-term in vivo protective effects on osteocyte viability and bone strength following ovariectomy. Calcif Tissue Int. 2011; 88:443–454.

12. Robling AG, Niziolek PJ, Baldridge LA, et al. Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem. 2008; 283:5866–5875.

13. Kamel MA, Picconi JL, Lara-Castillo N, et al. Activation of beta-catenin signaling in MLO-Y4 osteocytic cells versus 2T3 osteoblastic cells by fluid flow shear stress and PGE2: Implications for the study of mechanosensation in bone. Bone. 2010; 47:872–881.

14. Price C, Zhou X, Li W, et al. Real-time measurement of solute transport within the lacunar-canalicular system of mechanically loaded bone: direct evidence for load-induced fluid flow. J Bone Miner Res. 2011; 26:277–285.

15. Hata M, Naruse K, Ozawa S, et al. Mechanical stretch increases the proliferation while inhibiting the osteogenic differentiation in dental pulp stem cells. Tissue Eng Part A. 2013; 19:625–633.

16. Gong H, Zhu D, Gao J, et al. An adaptation model for trabecular bone at different mechanical levels. Biomed Eng Online. 2010; 9:32.

17. McAteer ME, Niziolek PJ, Ellis SN, et al. Mechanical stimulation and intermittent parathyroid hormone treatment induce disproportional osteogenic, geometric, and biomechanical effects in growing mouse bone. Calcif Tissue Int. 2010; 86:389–396.

18. Frost HM. Muscle, bone, and the Utah paradigm: a 1999 overview. Med Sci Sports Exerc. 2000; 32:911–917.

19. Frost HM. Wolff's Law and bone's structural adaptations to mechanical usage: an overview for clinicians. Angle Orthod. 1994; 64:175–188.

20. Huang TH, Lin SC, Chang FL, et al. Effects of different exercise modes on mineralization, structure, and biomechanical properties of growing bone. J Appl Physiol (1985). 2003; 95:300–307.

21. Umemura Y, Sogo N, Honda A. Effects of intervals between jumps or bouts on osteogenic response to loading. J Appl Physiol (1985). 2002; 93:1345–1348.

22. Sueda K, Kitoh N, Zheng Y, et al. Changes in bone turnover by jump-training in immature female rats: comparison of short- and long-term training. J Nagoya Women's Univ. 2002; 48:43–49.

23. Chen H, Miller S, Shaw J, et al. Massage therapy during early postnatal life promotes greater lean mass and bone growth, mineralization, and strength in juvenile and young adult rats. J Musculoskelet Neuronal Interact. 2009; 9:278–287.

24. Komori T. Mechanism of bone mass regulation by mechanical stress. Clin Calcium. 2013; 23:1559–1567.

25. Bonewald LF. The amazing osteocyte. J Bone Miner Res. 2011; 26:229–238.

26. Moester MJ, Papapoulos SE, Löwik CW, et al. Sclerostin: current knowledge and future perspectives. Calcif Tissue Int. 2010; 87:99–107.

27. Turner CH. Functional determinants of bone structure: beyond Wolff's law of bone transformation. Bone. 1992; 13:403–409.

28. Burger EH, Klein-Nulend J. Mechanotransduction in bone-role of the lacuno-canalicular network. FASEB J. 1999; 13:Suppl. S101–S112.

29. Chapurlat RD, Delmas PD. Bone microdamage: a clinical perspective. Osteoporos Int. 2009; 20:1299–1308.

30. Parfitt AM. Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. J Cell Biochem. 1994; 55:273–286.

31. Yuki A, Yotani K, Tamaki H, et al. Upregulation of osteogenic factors induced by high-impact jumping suppresses adipogenesis in marrow but not adipogenic transcription factors in rat tibiae. Eur J Appl Physiol. 2010; 109:641–650.

32. Menuki K, Mori T, Sakai A, et al. Climbing exercise enhances osteoblast differentiation and inhibits adipogenic differentiation with high expression of PTH/PTHrP receptor in bone marrow cells. Bone. 2008; 43:613–620.

33. Morey ER, Baylink DJ. Inhibition of bone formation during space flight. Science. 1978; 201:1138–1141.

34. Aizawa K, Iemitsu M, Otsuki T, et al. Sex differences in steroidogenesis in skeletal muscle following a single bout of exercise in rats. J Appl Physiol (1985). 2008; 104:67–74.

35. Tromp AM, Bravenboer N, Tanck E, et al. Additional weight bearing during exercise and estrogen in the rat: the effect on bone mass, turnover, and structure. Calcif Tissue Int. 2006; 79:404–415.

36. Lau E, Al-Dujaili S, Guenther A, et al. Effect of low-magnitude, high-frequency vibration on osteocytes in the regulation of osteoclasts. Bone. 2010; 46:1508–1515.

37. Hiroyuki T. Effects of mechanical loading on bone formation and bone resorption. J Exerc Sports Physiol. 2012; 19:53–57.

38. Mori T, Okimoto N, Sakai A, et al. Climbing exercise increases bone mass and trabecular bone turnover through transient regulation of marrow osteogenic and osteoclastogenic potentials in mice. J Bone Miner Res. 2003; 18:2002–2009.

39. Shimamura C, Iwamoto J, Takeda T, et al. Effect of decreased physical activity on bone mass in exercise-trained young rats. J Orthop Sci. 2002; 7:358–363.

40. Nishioka T, Ikata T, Iwase A, et al. Influence of exercise on the longitudinal growth of lower limb and the tensile strength of tibial tuberosity. Cent Japan J Orthop Surg Traumatol. 1992; 35:157–158.

41. de Campos-Ferraz PL, Ribeiro SM, Luz Sdos S, et al. Exercise x BCAA supplementation in young trained rats: what are their effects on body growth? J Sports Sci Med. 2011; 10:483–490.