Androgen receptor disruption increases the osteogenic response to mechanical loading in male mice

Journal of Bone and Mineral Research

Volumn 25, Issue 1, 2010, Pages 124-131

  Callewaert, Filip ^a   Bakker, Astrid ^b   Schrooten, Jan ^a   Van Meerbeek, Bart ^c   Verhoeven, Guido ^a   Boonen, Steven ^a   Vanderschueren, Dirk ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c CATHOLIC UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Adaptive response of bone to mechanical loading; Bone formation; Pulsating fluid flow; Sex steroid receptors; Sost sclerostin

Indexed keywords

ANDROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; NITRIC OXIDE; SCLEROSTIN; TESTOSTERONE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; BONE CELL; BONE DEVELOPMENT; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; PERIOSTEUM; PROTEIN EXPRESSION; PULSATILE FLOW; REAL TIME POLYMERASE CHAIN REACTION; ULNA; WILD TYPE;

ANIMALS; BONE AND BONES; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; CYCLOOXYGENASE 2; FEMALE; GENETIC MARKERS; MALE; MICE; MICE, KNOCKOUT; NITRIC OXIDE; OSTEOGENESIS; PERIOSTEUM; RECEPTORS, ANDROGEN; STRESS, MECHANICAL; TESTOSTERONE; WEIGHT-BEARING;

EID: 77953383151     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.091001     Document Type: Article

References (49)

1. Boonen S, Kaufman JM, Goemaere S, Bouillon R, Vanderschueren D. The diagnosis and treatment of male osteoporosis: defining, assessing, and preventing skeletal fragility in men. Eur J Intern Med. 2007;18:6-17.
2. Khosla S, Amin S, Orwoll E. Osteoporosis in men. Endocr Rev. 2008;29:441-464.
3. Seeman E. Periosteal bone formation: a neglected determinant of bone strength. N Engl J Med. 2003;349:320-323.
4. Frost HM. Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol. 2003;275:1081-1101.
5. Frost HM. Bone "mass" and the "mechanostat": a proposal. Anat Rec. 1987;219:1-9.
6. Lanyon LE. Control of bone architecture by functional load bearing. J Bone Miner Res. 1992;7:S369-375.
7. Bass SL, Saxon L, Daly RM, et al. The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: a study in tennis players. J Bone Miner Res. 2002;17:2274-2280.
8. Lang T, LeBlanc A, Evans H, Lu Y, Genant H, Yu A. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res. 2004;19:1006-1012.
9. Lee KC, Maxwell A, Lanyon LE. Validation of a technique for studying functional adaptation of the mouse ulna in response to mechanical loading. Bone. 2002; 31:407-412.
10. Ehrlich PJ, Lanyon LE. Mechanical strain and bone cell function: a review. Osteoporos Int. 2002;13:688-700.
11. Santos A, Bakker AD, Klein-Nulend J. The role of osteocytes in bone mechanotransduction. Osteoporos Int. 2009;20:1686-1692.
12. Bonewald LF, Johnson ML. Osteocytes, mechanosensing and WNT signaling. Bone. 2008;42:606-615.
13. Klein-Nulend J, van der Plas A, Semeins CM, et al. Sensitivity of osteocytes to biomechanical stress in vitro. FASEB J. 1995;9:441-445.
14. Tatsumi S, Ishii K, Amizuka N, et al. Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab. 2007;5:464-475.
15. 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.
16. ten Dijke P, Krause C, de Gorter DJ, Lowik CW, van Bezooijen RL. Osteocyte-derived sclerostin inhibits bone formation: its role in bone morphogenetic protein and WNT signaling. J Bone Joint Surg. 2008;90A:S31-35.
17. Poole KE, van Bezooijen RL, Loveridge N, et al. Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J. 2005;19:1842-1844.
18. van Bezooijen RL, ten Dijke P, Papapoulos SE, Lowik CW. SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev. 2005;16:319-327.
19. Lin C, Jiang X, Dai Z, et al. Sclerostin mediates bone response to mechanical unloading via antagonizing WNT/beta-catenin signaling. J Bone Miner Res. 2009;24:1651-1661.
20. Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, et al. WNT/beta-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem. 2006;281:31720-31728.
21. Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C. Androgens and bone. Endocr Rev. 2004;25:389-425.
22. Rauch F, Bailey DA, Baxter-Jones A, Mirwald R, Faulkner R. The "muscle-bone unit" during the pubertal growth spurt. Bone. 2004;34:771-775.
23. Callewaert F, Venken K, Ophoff J, et al. Differential regulation of bone and body composition in male mice with combined inactivation of androgen and estrogen receptor-alpha. FASEB J. 2009;23:232-240.
24. Lee K, Jessop H, Suswillo R, Zaman G, Lanyon L. Endocrinology: bone adaptation requires oestrogen receptor-alpha. Nature. 2003;424:389.
25. Lee KC, Jessop H, Suswillo R, Zaman G, Lanyon LE. The adaptive response of bone to mechanical loading in female transgenic mice is deficient in the absence of oestrogen receptor-alpha and -beta. J Endocrinol. 2004;182:193-201.
26. Jessop HL, Suswillo RF, Rawlinson SC, et al. Osteoblast-like cells from estrogen receptor-alpha knockout mice have deficient responses to mechanical strain. J Bone Miner Res. 2004;19:938-946.
27. De Gendt K, Swinnen JV, Saunders PT, et al. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA. 2004;101:1327-1332.
28. Parfitt AM, Drezner MK, Glorieux FH, et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 1987;2:595-610.
29. 15N]nitrate in biological fluids. Anal Biochem. 1982;126:131-138.
30. Ducher G, Daly R, Bass S. The effects of repetitive loading on bone mass and geometry in young male tennis players: a quantitative study using magnetic resonance imaging. J Bone Miner Res. 2009;24:1686-1692.
31. Fritton JC, Myers ER, Wright TM, van der Meulen MC. Bone mass is preserved and cancellous architecture altered due to cyclic loading of the mouse tibia after orchidectomy. J Bone Miner Res. 2008;23:663-671.
32. Venken K, De Gendt K, Boonen S, et al. Relative impact of androgen and estrogen receptor activation in the effects of androgens on trabecular and cortical bone in growing male mice: a study in the androgen receptor knockout mouse model. J Bone Miner Res. 2006;21:576-585.
33. Marcus R, Leary D, Schneider DL, Shane E, Favus M, Quigley CA. The contribution of testosterone to skeletal development and maintenance: lessons from the androgen insensitivity syndrome. J Clin Endocrinol Metab. 2000;85:1032-1037.
34. Bhasin S, Woodhouse L, Casaburi R, et al. Testosterone dose-response relationships in healthy young men. Am J Physiol Endocrinol Metab. 2001;281:E1172-1181.
35. Saxon LK, Turner CH. Estrogen receptor beta: the antimechanostat? Bone. 2005; 36:185-192.
36. Saxon LK, Robling AG, Castillo AB, Mohan S, Turner CH. The skeletal responsiveness to mechanical loading is enhanced in mice with a null mutation in estrogen receptor-beta. Am J Physiol Endocrinol Metab. 2007;293:E484-491.
37. Lapauw BM, Taes Y, Bogaert V, et al. Serum estradiol is associated with volumetric BMD and modulates the impact of physical activity on bone size at the age of peak bone mass: a study in healthy male siblings. J Bone Miner Res. 2009;24:1075-1085.
38. Armstrong VJ, Muzylak M, Sunters A, et al. WNT/beta-catenin signaling is a component of osteoblastic bone cell early responses to load-bearing and requires estrogen receptor-alpha. J Biol Chem. 2007;282:20715-20727.
39. Fritton SP, McLeod KJ, Rubin CT. Quantifying the strain history of bone: spatial uniformity and self-similarity of low-magnitude strains. J Biomech. 2000;33:317-325.
40. Weinbaum S, Cowin SC, Zeng Y. A model for the excitation of osteocytes by mechanical loading-induced bone fluid shear stresses. J Biomech. 1994;27:339-360.
41. Fox SW, Chambers TJ, Chow JW. Nitric oxide is an earlymediator of the increase in bone formation by mechanical stimulation. Am J Physiol. 1996;270:E955-960.
42. Forwood MR. Inducible cyclooxygenase (COX-2) mediates the induction of bone formation by mechanical loading in vivo. J Bone Miner Res. 1996;11:1688-1693.
43. Klein-Nulend J, Burger EH, Semeins CM, Raisz LG, Pilbeam CC. Pulsating fluid flow stimulates prostaglandin release and inducible prostaglandin G/H synthase mRNA expression in primary mouse bone cells. J Bone Miner Res. 1997;12:45-51.
44. van't Hof RJ, Ralston SH. Nitric oxide and bone. Immunology. 2001;103:255-261.
45. Klein-Nulend J, Semeins CM, Ajubi NE, Nijweide PJ, Burger EH. Pulsating fluid flow increases nitric oxide (NO) synthesis by osteocytes but not periosteal fibroblasts: correlation with prostaglandin upregulation. Biochem Biophys Res Commun. 1995;217:640-648.
46. Pitsillides AA, Rawlinson SC, Suswillo RF, Bourrin S, Zaman G, Lanyon LE. Mechanical strain-induced NO production by bone cells: a possible role in adaptive bone (re)modeling? FASEB J. 1995;9:1614-1622.
47. Chow JW, Fox SW, Lean JM, Chambers TJ. Role of nitric oxide and prostaglandins in mechanically induced bone formation. J Bone Miner Res. 1998;13:1039-1044.
48. Smith WL, Garavito RM, DeWitt DL. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J Biol Chem. 1996;271:33157-33160.
49. Bakker AD, Klein-Nulend J, Burger EH. Mechanotransduction in bone cells proceeds via activation of COX-2, but not COX-1. Biochem Biophys Res Commun. 2003;305:677-683.