Pre-receptorial regulation of steroid hormones in bone cells: Insights on glucocorticoid-induced osteoporosis

Journal of Steroid Biochemistry and Molecular Biology

Volumn 108, Issue 3-5, 2008, Pages 292-299

  Pierotti, Silvia ^a   Gandini, Loredana ^a   Lenzi, Andrea ^a   Isidori, Andrea M ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

11 HSD; Androgens; Glucocorticoids; Mesenchymal stem cell differentiation; Osteoporosis

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; 11BETA HYDROXYSTEROID DEHYDROGENASE 1; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ALKALINE PHOSPHATASE; CORTISONE; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PRASTERONE SULFATE; SEX HORMONE; SOMATOMEDIN; STEROID; TESTOSTERONE 17BETA DEHYDROGENASE; UNCLASSIFIED DRUG;

ARTICLE; BONE CELL; BONE DEVELOPMENT; BONE METABOLISM; BONE REMODELING; CELL DIFFERENTIATION; CELL LINEAGE; CELL METABOLISM; CELL PROLIFERATION; CUSHING SYNDROME; ENZYME ACTIVITY; HUMAN; MESENCHYMAL STEM CELL; NONHUMAN; OSTEOBLAST; OSTEOCYTE; OSTEOLYSIS; OSTEOPOROSIS; STEROID METABOLISM;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; 11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ADULT; BONE AND BONES; BONE REMODELING; GLUCOCORTICOIDS; HUMANS; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; OSTEOPOROSIS;

EID: 38749106539     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2007.09.018     Document Type: Article

References (64)

1. Cushing H.W. The basophil adenomas of the pituitary body and their clinical manifestations (pituitary basophilism). Bull. Johns Hopkins Hosp. 50 (1932) 137-195
2. Khosla S., Lufkin E.G., Hodgson S.F., Fitzpatrick L.A., and Melton III L.J. Epidemiology and clinical features of osteoporosis in young individuals. Bone 15 (1994) 551-555
3. van Staa T.P., Leufkens H.G., and Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos. Int. 13 (2002) 777-787
4. Cooper M.S., Syddall H.E., Fall C.H., Wood P.J., Stewart P.M., Cooper C., and Dennison E.M. Circulating cortisone levels are associated with biochemical markers of bone formation and lumbar spine BMD: the Hertfordshire Cohort Study. Clin. Endocrinol. (Oxf.) 62 (2005) 692-697
5. Taylor-Jones J.M., McGehee R.E., Rando T.A., Lecka-Czernik B., Lipschitz D.A., and Peterson C.A. Activation of an adipogenic program in adult myoblasts with age. Mech. Ageing Dev. 123 (2002) 649-661
6. Delany A.M., Jeffrey J.J., Rydziel S., and Canalis E. Cortisol increases interstitial collagenase expression in osteoblasts by post-transcriptional mechanisms. J. Biol. Chem. 270 (1995) 26607-26612
7. Delany A.M., Gabbitas B.Y., and Canalis E. Cortisol downregulates osteoblast alpha 1 (I) procollagen mRNA by transcriptional and posttranscriptional mechanisms. J. Cell Biochem. 57 (1995) 488-494
8. Stromstedt P.E., Poellinger L., Gustafsson J.A., and Carlstedt-Duke J. The glucocorticoid receptor binds to a sequence overlapping the TATA box of the human osteocalcin promoter: a potential mechanism for negative regulation. Mol. Cell Biol. 11 (1991) 3379-3383
9. Heinrichs A.A., Bortell R., Rahman S., Stein J.L., Alnemri E.S., Litwack G., Lian J.B., and Stein G.S. Identification of multiple glucocorticoid receptor binding sites in the rat osteocalcin gene promoter. Biochemistry 32 (1993) 11436-11444
10. O'Brien C.A., Jia D., Plotkin L.I., Bellido T., Powers C.C., Stewart S.A., Manolagas S.C., and Weinstein R.S. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 145 (2004) 1835-1841
11. Weinstein R.S., Jilka R.L., Parfitt A.M., and Manolagas S.C. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J. Clin. Invest. 102 (1998) 274-282
12. Beavan S., Horner A., Bord S., Ireland D., and Compston J. Colocalization of glucocorticoid and mineralocorticoid receptors in human bone. J. Bone Miner. Res. 16 (2001) 1496-1504
13. Hofbauer L.C., Gori F., Riggs B.L., Lacey D.L., Dunstan C.R., Spelsberg T.C., and Khosla S. Stimulation of osteoprotegerin ligand and inhibition of osteoprotegerin production by glucocorticoids in human osteoblastic lineage cells: potential paracrine mechanisms of glucocorticoid-induced osteoporosis. Endocrinology 140 (1999) 4382-4389
14. Takuma A., Kaneda T., Sato T., Ninomiya S., Kumegawa M., and Hakeda Y. Dexamethasone enhances osteoclast formation synergistically with transforming growth factor-beta by stimulating the priming of osteoclast progenitors for differentiation into osteoclasts. J. Biol. Chem. 278 (2003) 44667-44674
15. Defranco D.J., Lian J.B., and Glowacki J. Differential effects of glucocorticoid on recruitment and activity of osteoclasts induced by normal and osteocalcin-deficient bone implanted in rats. Endocrinology 131 (1992) 114-121
16. Delany A.M., Durant D., and Canalis E. Glucocorticoid suppression of IGF I transcription in osteoblasts. Mol. Endocrinol. 15 (2001) 1781-1789
17. Pereira R.C., Durant D., and Canalis E. Transcriptional regulation of connective tissue growth factor by cortisol in osteoblasts. Am. J. Physiol. Endocrinol. Metab. 279 (2000) E570-E576
18. Bennett A., Chen T., Feldman D., Hintz R.L., and Rosenfeld R.G. Characterization of insulin-like growth factor I receptors on cultured rat bone cells: regulation of receptor concentration by glucocorticoids. Endocrinology 115 (1984) 1577-1583
19. Rydziel S., and Canalis E. Cortisol represses insulin-like growth factor II receptor transcription in skeletal cell cultures. Endocrinology 136 (1995) 4254-4260
20. Eriksen E.F., Colvard D.S., Berg N.J., Graham M.L., Mann K.G., Spelsberg T.C., and Riggs B.L. Evidence of estrogen receptors in normal human osteoblast-like cells. Science 241 (1988) 84-86
21. Pensler J.M., Radosevich J.A., Higbee R., and Langman C.B. Osteoclasts isolated from membranous bone in children exhibit nuclear estrogen and progesterone receptors. J. Bone Miner. Res. 5 (1990) 797-802
22. Bellido T., Jilka R.L., Boyce B.F., Girasole G., Broxmeyer H., Dalrymple S.A., Murray R., and Manolagas S.C. Regulation of interleukin-6, osteoclastogenesis, and bone mass by androgens. The role of the androgen receptor. J. Clin. Invest. 95 (1995) 2886-2895
23. Benz D.J., Haussler M.R., Thomas M.A., Speelman B., and Komm B.S. High-affinity androgen binding and androgenic regulation of alpha 1(I)-procollagen and transforming growth factor-beta steady state messenger ribonucleic acid levels in human osteoblast-like osteosarcoma cells. Endocrinology 128 (1991) 2723-2730
24. Braidman I.P., Baris C., Selby P.L., Adams J.E., Freemont A.J., and Hoyland J.A. Preliminary report of impaired oestrogen receptor-alpha expression in bone, but no involvement of androgen receptor, in male idiopathic osteoporosis. J. Pathol. 192 (2000) 90-96
25. Kousteni S., Bellido T., Plotkin L.I., O'Brien C.A., Bodenner D.L., Han L., Han K., DiGregorio G.B., Katzenellenbogen J.A., Katzenellenbogen B.S., Roberson P.K., Weinstein R.S., Jilka R.L., and Manolagas S.C. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104 (2001) 719-730
26. Manolagas S.C. Role of cytokines in bone resorption. Bone 17 (1995) 63S-67S
27. Manolagas S.C., Kousteni S., and Jilka R.L. Sex steroids and bone. Recent Prog. Horm. Res. 57 (2002) 385-409
28. Okazaki R., Inoue D., Shibata M., Saika M., Kido S., Ooka H., Tomiyama H., Sakamoto Y., and Matsumoto T. Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Endocrinology 143 (2002) 2349-2356
29. Kenny A.M., and Raisz L.G. Mechanisms of bone remodeling: implications for clinical practice. J. Reprod. Med. 47 (2002) 63-70
30. Liegibel U.M., Sommer U., Tomakidi P., Hilscher U., Van Den H.L., Pirzer R., Hillmeier J., Nawroth P., and Kasperk C. Concerted action of androgens and mechanical strain shifts bone metabolism from high turnover into an osteoanabolic mode. J. Exp. Med. 196 (2002) 1387-1392
31. Isidori A.M., Giannetta E., Greco E.A., Gianfrilli D., Bonifacio V., Isidori A., Lenzi A., and Fabbri A. Effects of testosterone on body composition, bone metabolism and serum lipid profile in middle-aged men: a meta-analysis. Clin. Endocrinol. (Oxf.) 63 (2005) 280-293
32. 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., and Kato S. Suppressive function of androgen receptor in bone resorption. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 9416-9421
33. Venken K., De Gendt K., Boonen S., Ophoff J., Bouillon R., Swinnen J.V., Verhoeven G., and Vanderschueren D. 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. 21 (2006) 576-585
34. Minetto M., Reimondo G., Osella G., Ventura M., Angeli A., and Terzolo M. Bone loss is more severe in primary adrenal than in pituitary-dependent Cushing's syndrome. Osteoporos. Int. 15 (2004) 855-861
35. Moverare S., Venken K., Eriksson A.L., Andersson N., Skrtic S., Wergedal J., Mohan S., Salmon P., Bouillon R., Gustafsson J.A., Vanderschueren D., and Ohlsson C. Differential effects on bone of estrogen receptor alpha and androgen receptor activation in orchidectomized adult male mice. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13573-13578
36. Chang P.L., Blair H.C., Zhao X., Chien Y.W., Chen D., Tilden A.B., Chang Z., Cao X., Faye-Petersen O.M., and Hicks P. Comparison of fetal and adult marrow stromal cells in osteogenesis with and without glucocorticoids. Connect. Tissue Res. 47 (2006) 67-76
37. Akavia U.D., Shur I., Rechavi G., and Benayahu D. Transcriptional profiling of mesenchymal stromal cells from young and old rats in response to dexamethasone. BMC Genomics 7 (2006) 95
38. Shur I., Lokiec F., Bleiberg I., and Benayahu D. Differential gene expression of cultured human osteoblasts. J. Cell Biochem. 83 (2001) 547-553
39. Fried A., Benayahu D., and Wientroub S. Marrow stroma-derived osteogenic clonal cell lines: putative stages in osteoblastic differentiation. J. Cell Physiol. 155 (1993) 472-482
40. Fried A., and Benayahu D. Dexamethasone regulation of marrow stromal-derived osteoblastic cells. J. Cell Biochem. 62 (1996) 476-483
41. Kuznetsov S.A., Krebsbach P.H., Satomura K., Kerr J., Riminucci M., Benayahu D., and Robey P.G. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J. Bone Miner. Res. 12 (1997) 1335-1347
42. Beloti M.M., and Rosa A.L. Osteoblast differentiation of human bone marrow cells under continuous and discontinuous treatment with dexamethasone. Braz. Dent. J. 16 (2005) 156-161
43. Cooper M.S., Hewison M., and Stewart P.M. Glucocorticoid activity, inactivity and the osteoblast. J. Endocrinol. 163 (1999) 159-164
44. Moore S.G., and Dawson K.L. Red and yellow marrow in the femur: age-related changes in appearance at MR imaging. Radiology 175 (1990) 219-223
45. Bianco P., Riminucci M., Gronthos S., and Robey P.G. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19 (2001) 180-192
46. Isidori A.M., Giannetta E., Pozza C., Bonifacio V., and Isidori A. Androgens, cardiovascular disease and osteoporosis. J. Endocrinol. Invest. 28 (2005) 73-79
47. Wu Z., Xie Y., Bucher N.L., and Farmer S.R. Conditional ectopic expression of C/EBP beta in NIH-3T3 cells induces PPAR gamma and stimulates adipogenesis. Genes Dev. 9 (1995) 2350-2363
48. Ducy P., Zhang R., Geoffroy V., Ridall A.L., and Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89 (1997) 747-754
49. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., and Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 (1997) 755-764
50. Nakashima K., Zhou X., Kunkel G., Zhang Z., Deng J.M., Behringer R.R., and de Crombrugghe B. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108 (2002) 17-29
51. Gutierrez S., Javed A., Tennant D.K., van Rees M., Montecino M., Stein G.S., Stein J.L., and Lian J.B. CCAAT/enhancer-binding proteins (C/EBP) beta and delta activate osteocalcin gene transcription and synergize with Runx2 at the C/EBP element to regulate bone-specific expression. J. Biol. Chem. 277 (2002) 1316-1323
52. Hata K., Nishimura R., Ueda M., Ikeda F., Matsubara T., Ichida F., Hisada K., Nokubi T., Yamaguchi A., and Yoneda T. A CCAAT/enhancer binding protein beta isoform, liver-enriched inhibitory protein, regulates commitment of osteoblasts and adipocytes. Mol. Cell Biol. 25 (2005) 1971-1979
53. Bachner D., Ahrens M., Schroder D., Hoffmann A., Lauber J., Betat N., Steinert P., Flohe L., and Gross G. Bmp-2 downstream targets in mesenchymal development identified by subtractive cloning from recombinant mesenchymal progenitors (C3H10T1/2). Dev. Dyn. 213 (1998) 398-411
54. Ogasawara A., Arakawa T., Kaneda T., Takuma T., Sato T., Kaneko H., Kumegawa M., and Hakeda Y. Fluid shear stress-induced cyclooxygenase-2 expression is mediated by C/EBP beta, cAMP-response element-binding protein, and AP-1 in osteoblastic MC3T3-E1 cells. J. Biol. Chem. 276 (2001) 7048-7054
55. Pereira R.C., Delany A.M., and Canalis E. Effects of cortisol and bone morphogenetic protein-2 on stromal cell differentiation: correlation with CCAAT-enhancer binding protein expression. Bone 30 (2002) 685-691
56. Bruley C., Lyons V., Worsley A.G., Wilde M.D., Darlington G.D., Morton N.M., Seckl J.R., and Chapman K.E. A novel promoter for the 11beta-hydroxysteroid dehydrogenase type 1 gene is active in lung and is C/EBPalpha independent. Endocrinology 147 (2006) 2879-2885
57. Tomlinson J.W., Walker E.A., Bujalska I.J., Draper N., Lavery G.G., Cooper M.S., Hewison M., and Stewart P.M. 11beta-Hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr. Rev. 25 (2004) 831-866
58. Eyre L.J., Rabbitt E.H., Bland R., Hughes S.V., Cooper M.S., Sheppard M.C., Stewart P.M., and Hewison M. Expression of 11 beta-hydroxysteroid dehydrogenase in rat osteoblastic cells: pre-receptor regulation of glucocorticoid responses in bone. J. Cell Biochem. 81 (2001) 453-462
59. Bland R., Worker C.A., Noble B.S., Eyre L.J., Bujalska I.J., Sheppard M.C., Stewart P.M., and Hewison M. Characterization of 11beta-hydroxysteroid dehydrogenase activity and corticosteroid receptor expression in human osteosarcoma cell lines. J. Endocrinol. 161 (1999) 455-464
60. Sher L.B., Woitge H.W., Adams D.J., Gronowicz G.A., Krozowski Z., Harrison J.R., and Kream B.E. Transgenic expression of 11beta-hydroxysteroid dehydrogenase type 2 in osteoblasts reveals an anabolic role for endogenous glucocorticoids in bone. Endocrinology 145 (2004) 922-929
61. Eijken M., Hewison M., Cooper M.S., de Jong F.H., Chiba H., Stewart P.M., Uitterlinden A.G., Pols H.A., and van Leeuwen J.P. 11beta-Hydroxysteroid dehydrogenase expression and glucocorticoid synthesis are directed by a molecular switch during osteoblast differentiation. Mol. Endocrinol. 19 (2005) 621-631
62. Canalis E., and Delany A.M. 11beta-Hydroxysteroid dehydrogenase, an amplifier of glucocorticoid action in osteoblasts. J. Bone Miner. Res. 17 (2002) 987-990
63. Masuzaki H., Paterson J., Shinyama H., Morton N.M., Mullins J.J., Seckl J.R., and Flier J.S. A transgenic model of visceral obesity and the metabolic syndrome 1. Science 294 (2001) 2166-2170
64. Bujalska I.J., Walker E.A., Hewison M., and Stewart P.M. A switch in dehydrogenase to reductase activity of 11 beta-hydroxysteroid dehydrogenase type 1 upon differentiation of human omental adipose stromal cells 1. J. Clin. Endocrinol. Metab. 87 (2002) 1205-1210