Age-related impairment of bones' adaptive response to loading in mice is associated with sex-related deficiencies in osteoblasts but no change in osteocytes

Journal of Bone and Mineral Research

Volumn 29, Issue 8, 2014, Pages 1859-1871

  Meakin, Lee B ^a   Galea, Gabriel L ^a   Sugiyama, Toshihiro ^a,b   Lanyon, Lance E ^a   Price, Joanna S ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b YAMAGUCHI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Aging; Mechanical Loading; Osteoblasts

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; KI 67 ANTIGEN; SCLEROSTIN;

ADULT; AGED; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DISEASE; BONE MASS; BONE STRUCTURE; CELL COUNT; CELL CYCLE G2 PHASE; CONTROLLED STUDY; CORTICAL BONE; DISEASE ASSOCIATION; FEMALE; IMMUNOFLUORESCENCE; IN VITRO STUDY; MALE; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PERIOSTEUM; PRIMARY CULTURE; PROTEIN EXPRESSION; SEXUAL DYSFUNCTION; TIBIA; TRABECULAR BONE; YOUNG ADULT; AGE; ANIMAL; BODY WEIGHT; BONE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; MECHANICAL STRESS; MOUSE;

AGE FACTORS; ANIMALS; BODY WEIGHT; BONE AND BONES; CELL PROLIFERATION; FEMALE; MALE; MICE; OSTEOBLASTS; OSTEOCYTES; STRESS, MECHANICAL; TIBIA;

EID: 84904696920     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2222     Document Type: Article

References (47)

1. Frost HM., The Utah paradigm of skeletal physiology. ISMNI; 1960.
2. Lanyon L, Skerry T., Postmenopausal osteoporosis as a failure of bone's adaptation to functional loading: a hypothesis. J Bone Miner Res. 2001; 16 (11): 1937-47.
3. Srinivasan S, Gross TS, Bain SD., Bone mechanotransduction may require augmentation in order to strengthen the senescent skeleton. Aging Res Rev. 2012; 11 (3): 353-60.
4. Kerr D, Morton A, Dick I, Prince R., Exercise effects on bone mass in postmenopausal women are site-specific and load-dependent. J Bone Miner Res. 1996; 11 (2): 218-25.
5. Whiteford J, Ackland TR, Dhaliwal SS, et al. Effects of a 1-year randomized controlled trial of resistance training on lower limb bone and muscle structure and function in older men. Osteoporos Int. 2010; 21 (9): 1529-36.
6. Turner CH, Takano Y, Owan I., Aging changes mechanical loading thresholds for bone formation in rats. J Bone Miner Res. 1995; 10 (10): 1544-9.
7. Srinivasan S, Agans SC, King KA, Moy NY, Poliachik SL, Gross TS., Enabling bone formation in the aged skeleton via rest-inserted mechanical loading. Bone. 2003; 33 (6): 946-55.
8. Brodt MD, Silva MJ., Aged mice have enhanced endocortical response and normal periosteal response compared with young-adult mice following 1 week of axial tibial compression. J Bone Miner Res. 2010; 25 (9): 2006-15.
9. Moustafa A, Sugiyama T, Prasad J, et al. Mechanical loading-related changes in osteocyte sclerostin expression in mice are more closely associated with the subsequent osteogenic response than the peak strains engendered. Osteoporos Int. 2012; 23 (4): 1225-34.
10. 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 (9): 5866-75.
11. Tu X, Rhee Y, Condon KW, et al. Sost downregulation and local Wnt signaling are required for the osteogenic response to mechanical loading. Bone. 2012; 50 (1): 209-17.
12. Ardawi M-SM, Rouzi AA, Al-Sibiani SA, Al-Senani NS, Qari MH, Mousa SA., High serum sclerostin predicts the occurrence of osteoporotic fractures in postmenopausal women: the Center of Excellence for Osteoporosis Research Study. J Bone Miner Res. 2012; 27 (12): 2592-602.
13. Galea GL, Meakin LB, Sugiyama T, et al. Estrogen receptor α mediates proliferation of osteoblastic cells stimulated by estrogen and mechanical strain, but their acute down regulation of the Wnt antagonist Sost is mediated by Estrogen Receptor β. J Biol Chem. 2013; 288 (13): 9035-48.
14. Pead MJ, Skerry TM, Lanyon LE., Direct transformation from quiescence to bone formation in the adult periosteum following a single brief period of bone loading. J Bone Miner Res. 1988; 3 (6): 647-56.
15. Turner CH, Owan I, Alvey T, Hulman J, Hock JM., Recruitment and proliferative responses of osteoblasts after mechanical loading in vivo determined using sustained-release bromodeoxyuridine. Bone. 1998; 22 (5): 463-9.
16. Neidlinger-Wilke C, Stalla I, Claes L, et al. Human osteoblasts from younger normal and osteoporotic donors show differences in proliferation and TGF beta-release in response to cyclic strain. J Biomech. 1995; 28 (12): 1411-8.
17. Zaman G, Sunters A, Galea GL, et al. Loading-related regulation of transcription factor EGR2/Krox-20 in bone cells is ERK1/2 protein-mediated and prostaglandin, Wnt signaling pathway-, and insulin-like growth factor-I axis-dependent. J Biol Chem. 2012; 287 (6): 3946-62.
18. Zaman G, Saxon LK, Sunters A, et al. Loading-related regulation of gene expression in bone in the contexts of estrogen deficiency, lack of estrogen receptor alpha and disuse. Bone. 2010; 46 (3): 628-42.
19. Meakin LB, Sugiyama T, Galea GL, Browne WJ, Lanyon LE, Price JS., Male mice housed in groups engage in frequent fighting and show a lower response to additional bone loading than females or individually housed males that do not fight. Bone. 2013; 54 (1): 113-7.
20. Sugiyama T, Meakin LB, Browne WJ, Galea GL, Price JS, Lanyon LE., Bones' adaptive response to mechanical loading is essentially linear between the low strains associated with disuse and the high strains associated with the lamellar/woven bone transition. J Bone Miner Res. 2012; 27 (8): 1784-93.
21. Sugiyama T, Price JS, Lanyon LE., Functional adaptation to mechanical loading in both cortical and cancellous bone is controlled locally and is confined to the loaded bones. Bone. 2010; 46 (2): 314-21.
22. Sugiyama T, Saxon LK, Zaman G, et al. Mechanical loading enhances the anabolic effects of intermittent parathyroid hormone (1-34) on trabecular and cortical bone in mice. Bone. 2008; 43 (2): 238-48.
23. Patel TK, Brodt MD, Silva MJ., Experimental and finite element analysis of strains induced by axial tibial compression in young-adult and old female C57Bl/6 mice. J Biomech. 2014; 47 (2): 451-7.
24. McKenzie JA, Silva MJ., Comparing histological, vascular and molecular responses associated with woven and lamellar bone formation induced by mechanical loading in the rat ulna. Bone. 2011; 48 (2): 250-8.
25. De Souza RL, Matsuura M, Eckstein F, Rawlinson SCF, Lanyon LE, Pitsillides AA., Non-invasive axial loading of mouse tibiae increases cortical bone formation and modifies trabecular organization: a new model to study cortical and cancellous compartments in a single loaded element. Bone. 2005; 37 (6): 810-8.
26. Sugiyama T, Meakin LB, Galea GL, et al. Risedronate does not reduce mechanical loading-related increases in cortical and trabecular bone mass in mice. Bone. 2011; 49 (1): 133-9.
27. Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R., Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010; 25 (7): 1468-86.
28. Hahn M, Vogel M, Pompesius-Kempa M, Delling G., Trabecular bone pattern factor-a new parameter for simple quantification of bone microarchitecture. Bone. 1992; 13 (4): 327-30.
29. Bonnet N, Standley KN, Bianchi EN, et al. The matricellular protein periostin is required for sost inhibition and the anabolic response to mechanical loading and physical activity. J Biol Chem. 2009; 284 (51): 35939-50.
30. Windahl S, Saxon L, Börjesson A, et al. Estrogen receptor-α is required for the osteogenic response to mechanical loading in a ligand-independent manner involving its activation function 1 but not 2. J Bone Miner Res. 2013; 28 (2): 291-301.
31. Javaheri B, Sunters A, Zaman G, et al. Lrp5 is not required for the proliferative response of osteoblasts to strain but regulates proliferation and apoptosis in a cell autonomous manner. PLoS ONE. 2012; 7 (5): e35726.
32. Sunters A, Armstrong VJ, Zaman G, et al. Mechano-transduction in osteoblastic cells involves strain-regulated estrogen receptor alpha-mediated control of insulin-like growth factor (IGF) I receptor sensitivity to Ambient IGF, leading to phosphatidylinositol 3-kinase/AKT-dependent Wnt/LRP5 receptor-independent activation of beta-catenin signaling. J Biol Chem. 2010; 285 (12): 8743-58.
33. Willinghamm MD, Brodt MD, Lee KL, Stephens AL, Ye J, Silva MJ., Age-related changes in bone structure and strength in female and male BALB/c mice. Calcif Tissue Int. 2010; 86 (6): 470-83.
34. Almeida M, Han L, Martin-Millan M, et al. Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem. 2007; 282 (37): 27285-97.
35. Ferguson VL, Ayers RA, Bateman TA, Simske SJ., Bone development and age-related bone loss in male C57BL/6J mice. Bone. 2003; 33 (3): 387-98.
36. Silva MJ, Tomlinson RE., Biomechanics and mechanobiology (ASBMR 2012). IBMS BoneKEy. 2013; 10 (282): 1-3.
37. Weinstein RS, Wan C, Liu Q, et al. Endogenous glucocorticoids decrease skeletal angiogenesis, vascularity, hydration, and strength in aged mice. Aging Cell. 2010; 9 (2): 147-61.
38. Sakai D, Kii I, Nakagawa K, et al. Remodeling of actin cytoskeleton in mouse periosteal cells under mechanical loading induces periosteal cell proliferation during bone formation. PLoS ONE. 2011; 6 (9): e24847.
39. Ghule PN, Medina R, Lengner CJ, et al. Reprogramming the pluripotent cell cycle: restoration of an abbreviated G1 phase in human induced pluripotent stem (iPS) cells. J Cell Physiol. 2011; 226 (5): 1149-56.
40. Ghule PN, Becker KA, Harper JW, et al. Cell cycle dependent phosphorylation and subnuclear organization of the histone gene regulator p220(NPAT) in human embryonic stem cells. J Cell Physiol. 2007; 213 (1): 9-17.
41. Riggs BL, Melton LJ, Robb RA, et al. A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res. 2008; 23 (2): 205-14.
42. Khosla S., Pathogenesis of age-related bone loss in humans. J Gerontol A Biol Sci Med Sci. 2013; 68 (10): 1226-35.
43. Manolagas SC, Almeida M., Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol. 2007; 21 (11): 2605-14.
44. Almeida M, Han L, Martin-Millan M, O'Brien CA, Manolagas SC., Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor- to forkhead box O-mediated transcription. J Biol Chem. 2007; 282 (37): 27298-305.
45. Jullien L, Mestre M, Roux P, Gire V., Eroded human telomeres are more prone to remain uncapped and to trigger a G2 checkpoint response. Nucleic Acids Res. 2013; 41 (2): 900-11.
46. Mao Z, Ke Z, Gorbunova V, Seluanov A., Replicatively senescent cells are arrested in G1 and G2 phases. Aging (Albany NY). 2012; 4 (6): 431-5.
47. Kassem M, Marie PJ., Senescence-associated intrinsic mechanisms of osteoblast dysfunctions. Aging Cell. 2011; 10 (2): 191-7.