Mineralization and bone resorption are regulated by the androgen receptor in male mice

Journal of Bone and Mineral Research

Volumn 24, Issue 4, 2009, Pages 621-631

  Chiang, Cherie ^a   Chiu, Maria ^a   Moore, Alison J ^b   Anderson, Paul H ^b,c   Ghasem Zadeh, Ali ^a,d   McManus, Julie F ^a   Cathy, Ma ^a   Seeman, Ego ^a,d   Clemens, Thomas L ^e   Morris, Howard A ^b   Zajac, Jeffrey D ^a   Davey, Rachel A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

^d AUSTIN HEALTH   (Australia)

^e University of Alabama at Birmingham   (United States)

Author keywords

Androgens; Bone histomorphometry; Knock out in; Osteoblasts

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; OSTEOCALCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MATRIX; BONE MINERALIZATION; BONE REMODELING; BONE STRUCTURE; BONE TURNOVER; CELL ACTIVITY; CELL DIFFERENTIATION; COMPARATIVE STUDY; CONTROLLED STUDY; CORTICAL BONE; LOXP SITE; MALE; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOLYSIS; PROTEIN FUNCTION; TRABECULAR BONE;

ACID PHOSPHATASE; ANIMALS; BIOLOGICAL MARKERS; BONE DENSITY; BONE REMODELING; BONE RESORPTION; FEMUR; GENE DELETION; INTEGRASES; ISOENZYMES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOCALCIN; PHENOTYPE; RECEPTORS, ANDROGEN; SPINE; TOMOGRAPHY, X-RAY COMPUTED;

EID: 65549171025     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.081217     Document Type: Article

References (48)

1. Vanderschueren D, Vandenput L, Boonen S, Lindberg MK, Bouillon R, Ohlsson C 2004 Androgens and bone. Endocr Rev 25:389-425.
2. Basaria S, Dobs AS 2001 Hypogonadism and androgen replacement therapy in elderly men. Am J Med 110:563-572.
3. Colvard DS, Eriksen EF, Keeting PE, Wilson EM, Lubahn DB, French FS. Riggs BL, Spelsberg TC 1989 Identification of androgen receptors in normal human osteoblast-like cells. Proc Natl Acad Sci USA 86:854-857.
4. Bertelloni S, Baroncelli GI, Ferdeghini M, Perri G, Saggese G 1998 Normal volumetric bone mineral density and bone turnover in young men with histories of constitutional delay of puberty. J Clin Endocrinol Metab 83:4280-4283.
5. Anderson FH, Francis RM, Faulkner K 1996 Androgen supplementation in eugonadal men with osteoporosis-effects of 6 months of treatment on bone mineral density and cardiovascular risk factors. Bone 18:171-177.
6. Carani C. Qin K, Simoni M, Faustini-Fustini M, Serpente S, Boyd J, Korach KS, Simpson ER 1997 Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 337:91-95.
7. Smith EP. Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS 1994 Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 331:1056-1061.
8. Kasperk CH, Wergedal JE, Farley JR, Linkhart TA, Turner RT, Baylink DJ 1989 Androgens directly stimulate proliferation of bone cells in vitro. Endocrinology 124:1576-1578.
9. Masuyama A, Ouchi Y, Sato F, Hosoi T, Nakamura T, Orimo H 1992 Characteristics of steroid hormone receptors in cultured MC3T3-E1 osteoblastic cells and effect of steroid hormones on cell proliferation. Calcif Tissue Int 51:376-381.
10. Mantalaris A, Panoskaltsis N, Sakai Y, Bourne P, Chang C, Messing EM, Wu JH 2001 Localization of androgen receptor expression in human bone marrow. J Pathol 193:361-366.
11. Bertelloni S. Baroncelli GI, Federico G, Cappa M, Lala R, Saggese G 1998 Altered bone mineral density in patients with complete androgen insensitivity syndrome. Horm Res 50:309-314.
12. Vanderschueren D, Van Herck E, Suiker AM, Visser WJ. Schot LP, Bouillon R 1992 Bone and mineral metabolism in aged male rats: Short and long term effects of androgen deficiency. Endocrinology 130:2906-2916.
13. Wakley GK, Schutte HD Jr, Hannon KS, Turner RT 1991 Androgen treatment prevents loss of cancellous bone in the orchidectomized rat. J Bone Miner Res 6:325-330.
14. Vandenput L, Swinnen JV, Van Herck E, Vcrstuyf A, Boonen S, Bouillon R, Vanderschueren D 2002 The estrogen receptor ligand ICI 182,780 does not impair the bone-sparing effects of testosterone in the young orchidectomized rat model. Calcif Tissue Int 70:170-175.
15. Vandenput L, Ederveen AG, Erben RG, Stahr K, Swinnen JV. Van Herck E, Verstuyf A, Boonen S, Bouillon R, Vanderschueren D 2001 Testosterone prevents orchidectomy-induced bone loss in estrogen receptor-alpha knockout mice. Biochem Biophys Res Cotnmun 285:70-76.
16. Notini AJ, Davey RA, McManus JF, Bate KL, Zajac JD 2005 Genomic actions of the androgen receptor are required for normal male sexual differentiation in a mouse model. J Mol Endocrinol 35:547-555.
17. Sato T, Kawano H, Kato S 2002 Study of androgen action in bone by analysis of androgen-receptor deficient mice. J Bone Miner Metab 20:326-330.
18. Kawano H, Sato T, Yamada T, Matsumoto T, Sekine K, Watanabe T, Nakamura T, Fukuda T, Yoshimura K, Yoshizawa T, Aihara K, Yamamoto Y, Nakamichi Y, Metzger D, Chambon P, Nakamura K, Kawaguchi H, Kato S 2003 Suppressive function of androgen receptor in bone resorption. Proc Natl Acad Sci USA 100:9416-9421.
19. Owen TA, Aronow M, Shalhoub V, Barone LM, Wilming L, Tassinari MS, Kennedy MB, Pockwinse S, Lian JB, Stein GS 1990 Progressive development of the rat osteoblast phenotype in vitro: Reciprocal relationships in expression of genes associated with osteoblast proliferation and differentiation during formation of the bone extracellular matrix. J Cell Physiol 143:420-430.
20. Somjen D, Weisman Y, Mor Z, Harell A, Kaye AM 1991 Regulation of proliferation of rat cartilage and bone by sex steroid hormones. J Steroid Biochem Mol Biol 40:717-723.
21. Davey RA, Hahn CN, May BK, Morris HA 2000 Osteoblast gene expression in rat long bones: Effects of ovariectomy and dihydrotestosterone on raRNA levels. Calcif Tissue Int 67:75-79.
22. Notini AJ, McManus JF, Moore A, Bouxsein M, Jimenez M, Chiu WS, Glatt V, Kream BE, Handelsman DJ, Morris HA, Zajac JD, Davey RA 2007 Osteoblast deletion of exon 3 of the androgen receptor gene results in trabecular bone loss in adult male mice. J Bone Miner Res 22:347-356.
23. Zhang M, Xuan S, Bouxsein ML, von Stechow D, Akeno N, Faugere MC, Malluche H, Zhao G, Rosen CJ, Efstratiadis A, Clemens TL 2002 Osteoblast-specific knockout of the insulinlike growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem 277:44005-44012.
24. Richman C, Kutilek S, Miyakoshi N, Srivastava AK, Beamer WG, Donahue LR, Rosen CJ, Wergedal JE, Baylink DJ, Mohan S 2001 Postnatal and pubertal skeletal changes contribute predominantly to the differences in peak bone density between C3H/HeJ and C57BL/6J mice. J Bone Miner Res 16:386-397.
25. Ferguson VL, Ayers RA, Batcman TA, Simske SJ 2003 Bone development and age-related bone loss in male C57BL/6J mice. Bone 33:387-398.
26. 26.Baldock PA, Moore RJ, Durbridge TC, Morris HA 1999 Comparison of three methods for estimation of bone resorption following ovariectomy in the distal femur and the proximal tibia of the rat. Bone 24:597-602.
27. Page K 1997 Theory and practice of histological techniques. In: Bancroft JD, Stevens A (eds.) Bone and Preparation of Bone Sections. Churchill Livingstone, London, UK, pp. 223-248.
28. Davey RA, Moore AJ. Chiu MW, Notini AJ, Morris HA, Zajac JD 2006 Effects of amylin deficiency on trabecular bone in young mice are sex-dependent. Calcif Tissue Int 78:398-403.
29. Parfitt AM 2005 Vitamin D and the pathogenesis of rickest and osteomalacia. In: Feldman D, Pike JW, Glorieux FH (eds.) Vitamin D. 2nd ed., vol. 2. Elsevier Academic Press, San Diego, CA, USA, pp. 1029-1048.
30. Hildebrand T, Laib A, Muller R, Dequeker J, Ruegsegger P 1999 Direct three-dimensional morphometric analysis of human cancellous bone: Microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 14:1167-1174.
31. MacLean HE, Chiu WS, Ma C, McManus JF, Davey RA, Cameron R. Notini AJ, Zajac JD 2008 A tloxed allele of the androgen receptor gene causes hyperandrogenization in male mice. Physiol Genomics 33:133-137.
32. Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O'Brien CA, Bellido T, Parfitt AM. Weinstein RS. Jilka RL, Manolagas SC 2007 Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285-27297.
33. Kalajzic Z, Liu P, Kalajzic I, Du Z, Braut A, Mina M, Canalis E, Rowe DW 2002 Directing the expression of a green fluorescent protein transgene in differentiated osteoblasts: Comparison between rat type I collagen and rat osteocalcin promoters. Bone 31:654-660.
34. Kasperk C, Fitzsimmons R, Strong D, Mohan S, Jennings J, Wergedal J, Baylink D 1990 Studies of the mechanism by which androgens enhance mitogenesis and differentiation in bone cells. J Clin Endocrinol Metab 71:1322-1329.
35. Mohan S, Richman C, Guo R, Amaar Y. Donahue LR, Wergedal J, Baylink DJ 2003 Insulin-like growth factor regulates peak bone mineral density in mice by both growth hormone-dependent and-independent mechanisms. Endocrinology 144:929-936.
36. Thcyse LF, Oosterlaken-Dijksterhuis MA, van Doom J, Terlou M, Mol JA, Voorhout G, Hazewinkel HA 2006 Expression of osteotropic growth factors and growth hormone receptor in a canine distraction osteogenesis model. J Bone Miner Metab 24:266-273.
37. Bouletreau PJ, Warren SM, Spector JA, Steinbrech DS, Mehrara BJ, Longaker MT 2002 Factors in the fracture microenvironment induce primary osteoblast angiogenic cytokine production. Plast Reconstr Surg 110:139-148.
38. Penolazzi L. Lambertini E, Tavanti E, Torreggiani E, Vesce F, Gambari R, Piva R 2008 Evaluation of chemokine and cytokine profiles in osteoblast progenitors from umbilical cord blood stem cells by BIO-PLEX technology. Cell Biol Int 32:320-325.
39. Leder BZ, LeBlanc KM. Schoenfeld DA. Eastell R, Finkelstein JS 2003 Differential effects of androgens and estrogens on bone turnover in normal men. J Clin Endocrinol Metab 88:204-210.
40. Falahati-Nini A, Riggs BL, Atkinson EJ, O'Fallon WM. Eastell R, Khosla S 2000 Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest 106:1553-1560.
41. Wiren KM, Zhang X, Semirale A, Price C, Woo A, Jepsen KJ 2006 Targeted Androgen Action in Mature Versus Preosteo-blasts Eliminates Periosteal Stimulation and Reduces Bone Quality during Growth. J Bone Miner Res 21:S1;S5.
42. Wiren KM, Zhang XW, Toombs AR, Kasparcova V, Gentile MA, Harada S, Jepsen KJ 2004 Targeted overexpression of androgen receptor in osteoblasts: Unexpected complex bone phenotype in growing animals. Endocrinology 145:3507-3522.
43. Davey RA, MacLean HE, McManus JF, Findlay DM, Zajac JD 2004 Genetically modified animal models as tools for studying bone and mineral metabolism. J Bone Miner Res 19:882-892.
44. Davey RA, MacLean HE 2006 Current and future approaches using genetically modified mice in endocrine research. Am J Physiol Endocrinol Metab 291:E429-E438.
45. Bilic-Curcic I, Kronenberg M, Jiang X, Bellizzi J, Mina M, Marijanovic I, Gardiner EM, Rowe DW 2005 Visualizing levels of osteoblast differentiation by a two-color promoter-GFP strategy: Type I collagen-GFPcyan and osteocalcin-GFPtpz. Genesis 43:87-98.
46. van der Eerden BC, van Til NP, Brinkmann AO, Lowik CW, Wit JM, Karperien M 2002 Gender differences in expression of androgen receptor in tibial growth plate and metaphyseal bone of the rat. Bone 30:891-896.
47. Notelovitz M 2002 Androgen effects on bone and muscle. Fertil Steril 77(Suppl 4):S34-S41.
48. Wiren KM, Toombs AR. Semirale AA, Zhang X 2006 Osteoblast and osteocyte apoptosis associated with androgen action in bone: Requirement of increased Bax/Bcl-2 ratio. Bone 38:637-651.