Bone morphogenetic protein-6 production in human osteoblastic cell lines: Selective regulation by estrogen

Journal of Clinical Investigation

Volumn 101, Issue 2, 1998, Pages 413-422

  Rickard, David J ^a   Hofbauer, Lorenz C ^a   Bonde, Susan K ^a   Gori, Francesca ^a   Spelsberg, Thomas C ^b   Riggs, B Lawrence ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Antiestrogens; BMP; Differentiation; Estrogen; Osteoblasts

Indexed keywords

4 HYDROXYTAMOXIFEN; BONE MORPHOGENETIC PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; MESSENGER RNA; OSTEOGENIC PROTEIN 1; OSTEOGENIN; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL IMMORTALIZATION; ESTROGEN THERAPY; FETUS; HUMAN; HUMAN CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; RECEPTOR GENE; SEQUENCE ANALYSIS;

EID: 0032518282     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119880     Document Type: Article

References (53)

1. Turner, R.T., G.L. Evans, and G.K. Wakley. 1993. Mechanism of action of estrogen on cancellous bone balance in tibiae of ovariectomized growing rats: inhibition of indices of formation and resorption. J. Bone Miner. Res. 8: 359-366.
2. Komm, B.S., C.M. Terpening, D.J. Benz, K.A. Graeme, B.W. O'Malley, and M.R. Haussler. 1988. Estrogen binding sites, receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science. 241:81-84.
3. Eriksen, E.F., D.S. Colvard, N.J. Berg, M.L. Graham, K.G. Mann, T.C. Spelsberg, and B.L. Riggs. 1988. Evidence of estrogen receptors in normal human osteoblast-like cells. Science. 241:84-86.
4. Oursler, M.J., P. Osdoby, J. Pyfferoen, B.L. Riggs, and T. Spelsberg. 1991. Avian osteoclasts as estrogen target cells. Proc. Natl. Acad. Sci. USA. 88: 6613-6617.
5. Oursler, M.J., L. Pederson, L. Fitzpatrick, and B.L. Riggs. 1994. Human giant cell tumors of the bone (osteoclastomas) are estrogen target cells. Proc. Natl. Acad. Sci. USA. 91:5227-5231.
6. Kimble, R.B., A.B. Matayoshi, J.L. Vannice, V.T. Kung, C. Williams, and R. Pacifici. 1995. Simultaneous block of interleukin-1 and tumor necrosis factor is required to completely prevent bone loss in the early postovariectomy period. Endocrinology. 136:3054-3061.
7. Manolagas, S.C., and R.L. Jilka. 1995. Bone marrow, cytokines, and bone remodeling: emerging insights into the pathophysiology of osteoporosis. N. Engl. J. Med. 332:305-311.
8. Oursler, M.J., C. Cortese, P.E. Keeting, M.A. Anderson, S.K. Bonde, B.L. Riggs, and T.C. Spelsberg. 1991. Modulation of transforming growth factor-β production in normal human osteoblast-like cells by 17β-estradiol and parathyroid hormone. Endocrinology. 129:3313-3320.
9. Ernst, M., J.K. Heath, and G.A. Rodan. 1989. Estradiol effects on proliferation, messenger ribonucleic acid for collagen and insulin-like growth factor-I, and parathyroid hormone-stimulated adenylate cyclase activity in osteoblastic cells from calvariae and long bones. Endocrinology. 125:825-833.
10. Kassem, M., R. Okazaki, D. DeLeon, S.A. Harris, J.A. Robinson, T.C. Spelsberg, C.A. Conover, and B.L. Riggs. 1996. Potential mechanism of estrogen-mediated decrease in bone formation: estrogen increases production of inhibitory insulin-like growth factor binding protein-4. Proc. Assoc. Am. Physicians. 108:155-164.
11. Kessler, E., K. Takahara, L. Biniaminov, M. Brusel, and D.S. Greenspan. 1996. Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science. 271:360-362.
12. Wozney, J.M., V. Rosen, A.J. Celeste, L.M. Mitsock, M.J. Whitters, R.W. Kriz, R.M. Hewick, and E.A. Wang. 1988. Novel regulators of bone formation: molecular clones and activities. Science. 242:1528-1534.
13. Wang, E.A., V. Rosen, J.S. D'Alessandro, M. Bauduy, P. Cordes, T. Harada, D.I. Israel, R.M. Hewick, K.M. Kerns, P. LaPan, et al. 1990. Recombinant human bone morphogenetic protein induces bone formation. Proc. Natl. Acad. Sci. USA. 87:2220-2224.
14. Kingsley, D.M. 1994. What do BMPs do in mammals? Clues from the mouse short-ear mutation. Trends Genet. 10:16-21.
15. Lyons, K.M., R.W. Pelton, and B.L. Hogan. 1989. Patterns of expression of murine Vgr-1 and BMP-2a RNA suggest that TGFβ-like genes co-ordinately regulate aspects of embryonic development. Genes Dev. 3:1657-1668.
16. Jones, C.M., K.M. Lyons, and B.L.M. Hogan. 1991. Involvement of bone morphogenetic protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development (Camb.) 111:531-542.
17. Rosen, V., J. Nove, J.J. Song, R.S. Thies, K. Cox, and J.M. Wozney. 1994. Responsiveness of clonal limb bud cell lines to BMP-2 reveals a sequential relationship between cartilage and bone phenotypes. J. Bone Miner. Res. 9: 1759-1768.
18. Thies, R.S., M. Bauduy, B.A. Ashton, L. Kurtzberg, J.M. Wozney, and V. Rosen. 1992. Recombinant human bone morphogenetic protein-2 induces differentiation in W-20-17 stromal cells. Endocrinology. 130:1318-1324.
19. Amedee, J., R. Bareille, F. Rouais, N. Cunningham, H. Reddi, and M.F. Harmand. 1994. Osteogenin (BMP-3) inhibits proliferation and stimulates differentiation of osteoprogenitors in human bone marrow. Differentiation. 58: 157-164.
20. Vukicevic, S., F.P. Luyten, and A.H. Reddi. 1989. Stimulation of expression of osteogenic and chondrogenic phenotypes in vitro by osteogenin. Proc. Natl. Acad. Sci. USA. 86:8793-8797.
21. Harris, S.A., R.J. Enger, B.L. Riggs, and T.C. Spelsberg. 1995. Development and characterization of a conditionally immortalized human fetal osteoblastic cell line. J. Bone Miner. Res. 10:178-186.
22. Harris, S., K.R. Tau, R.J. Enger, D.O. Toft, B.L. Riggs, and T.C. Spelsberg. 1995. Estrogen response in the hFOB1.19 human fetal osteoblastic cell line stably transfected with the human estrogen receptor gene. J. Cell. Biochem. 59:193-201.
23. Spelsberg, T.C., M.L. Graham, N.J. Berg, T. Umehara, E. Riehl, C.B. Coulam, J.N. Ingle. 1987. A nuclear binding assay to assess the biological activity of steroid receptors in isolated animal and human tissues. Endocrinology. 121:631-644.
24. Colvard, D.S., W.R. Jankus, N.J. Berg, M.L. Graham, N.-S. Jiang, J.N. Ingle, and T.C. Spelsberg. 1988. Microassay for nuclear binding of steroid receptors with use of intact cells from small samples of avian and human tissues. Clin. Chem. 34:363-369.
25. Robinson, J.A., S.A. Harris, B.L. Riggs, and T.C. Spelsberg. 1997. Estrogen regulation of human osteoblast cell proliferation and differentiation. Endocrinology. 138:2919-2927.
26. Parker, M.G. 1993. Action of 'pure' antiestrogens in inhibiting estrogen receptor action. Breast Cancer Res. Treat. 26:131-137.
27. Celeste, A.J., J.A. Iannazzi, R.C. Taylor, R.M. Hewick, V. Rosen, E.A. Wang, and J.M. Wozney. 1990. Identification of transforming growth factor-β family members present in bone-inductive protein purified from bovine bone. Proc. Natl. Acad. Sci. USA. 87:9843-9847.
28. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
29. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
30. Katzenellenbogen, J.A., B.W. O'Malley, and B.S. Katzenellenbogen. 1996. Tripartite steroid hormone receptor pharmacology: Interaction with multiple effector sites as a basis for the cell-and promoter-specific action of these hormones. Mol. Endocrinol. 10:119-131.
31. Schuchard, M., J.P. Landers, N. Punkay-Sandhu, and T.C. Spelsberg. 1993. Steroid hormone regulation of nuclear proto-oncogenes. Endocr. Rev. 14: 659-669.
32. Weisz, A., and F. Bresciani. 1988. Estrogen induces expression of c-fos and c-myc protooncogenes in rat uterus. Mol. Endocrinol. 2:816-824.
33. Gitelman, S.E., M.S. Kobrin, J.-Q. Ye, A.R. Lopez, A. Lee, and R. Derynck. 1994. Recombinant Vgr-1/BMP 6-expressing tumors induce fibrosis and endochondral bone formation in vivo. J. Cell Biol. 126:1595-1609.
34. Carey, D.E., and X. Liu. 1995. Expression of bone morphogenetic protein-6 messenger RNA in bovine growth plate chondrocytes of different size. J. Bone Miner. Res. 10:401-405.
35. Wall, N.A., M. Blessing, C.V.E. Wright, and B.L.M. Hogan. 1993. Biosynthesis and in vivo localization of the decapentaplegic-Vg-related protein, DVR-6 (bone morphogenetic protein-6). J. Cell Biol. 120:493-502.
36. Boden, S.D., G. Hair, L. Titus, M. Racine, K. McCuaig, J.M. Wozney, and M.S. Nanes. 1997. Glucocorticoid-induced differentiation of fetal rat calvarial osteoblasts is mediated by bone morphogenetic protein-6. Endocrinology. 138:2820-2828.
37. Komm, B., R. Henderson, P. Bodine, J. Green, J. Lian, and G. Stein. 1996. The estrogen receptor is developmentally up-regulated during osteoblast differentiation. J. Bone Miner. Res. 11(Suppl.1):S258.
38. Corvol, M.-T., A. Carrascosa, L. Tsagris, O. Blanchard, and R. Rappaport. 1987. Evidence for a direct in vitro action of sex steroids on rabbit cartilage cells during skeletal growth: influence of age and sex. Endocrinology. 120: 1422-1429.
39. Korach, K.S. 1994. Insights from the study of animals lacking functional estrogen receptor. Science. 266:1524-1527.
40. Smith, E.P., J. Boyd, G.R. Frank, H. Takahashi, R.M. Cohen, B. Specker, T.C. Williams, D.B. Lubahn, and K.S. Korach. 1994. Estrogen resistance caused by a mutation in the estrogen receptor gene in a man. N. Engl. J. Med. 331:1056-1061.
41. Pinus, H., A. Ornoy, N. Patlas, P. Yaffe, and Z. Schwartz. 1993. Specific β-estradiol binding in cartilage and serum from young mice and rats is age dependent. Connect. Tissue Res. 30:85-98.
42. Ben-Hur, H., G. Mor, I. Blickstein, I. Likhman, F. Kohen, R. Dgani, V. Insler, P. Yaffe, and A. Ornoy. 1993. Localization of estrogen receptors in long bones and vertebrae of human fetuses. Calcif. Tissue Int. 53:91-96.
43. Reddi, A.H., and N.S. Cunningham. 1993. Initiation and promotion of bone differentiation by bone morphogenetic proteins. J. Bone Miner. Res. 8 (Suppl.2):S499-S502.
44. Wang, E.A., D.I. Israel, S. Kelly, and D.P. Luxenberg. 1993. Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors. 9:57-71.
45. Ahrens, M., T. Ankenbauer, D. Schroder, A. Hollnagel, H. Mayer, and G. Gross. 1993. Expression of human bone morphogenetic proteins -2 or -4 in murine mesenchymal C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol. 12:871-880.
46. Gitelman, S.E., M. Kirk, J.Q. Ye, E.H. Filvaroff, A.J. Kahn, and R. Deryack. 1995. Vgr-1/BMP-6 induces osteoblastic differentiation of pluripotential mesenchymal cells. Cell Growth Diff. 6:827-836.
47. Hughes, F.J., J. Collyer, M. Stanfield, and S.A. Goodman. 1995. The effects of BMP-2, -4 and -6 on differentiation of rat osteoblast cells in vitro. Endocrinology, 136:2671-2677.
48. Lyons, K.M., R.W. Pelton, and B.L.M. Hogan. 1990. Organogenesis and pattern formation in the mouse: RNA distribution patterns suggest a role for bone morphogenetic protein-2A (BMP-2A). Development. 109:833-844.
49. Wozney, J.M. 1993. Bone morphogenetic proteins and their gene expression. In Cellular and Molecular Biology of Bone. M. Noda. editor. Academic Press, San Diego, CA. 131-167.
50. Chang, S.C., B. Hoang, J.T. Thomas, S. Vukicevic, F.P. Luyten, N.J. Ryba, C.A. Kozak, A.H. Reddi, and M. Moos. 1994. Cartilage-derived morphogenetic proteins. New members of the TGFβ superfamily predominantly expressed in long bones during human embryonic development. J. Biol. Chem. 269:28227-28234.
51. Vukicevic, S., V. Latin, P. Chen, R. Batorsky, A.H. Reddi, and T.K. Sampath. 1994. Localization of OP-1 (BMP-7) during human embryonic development: high affinity binding to basement membranes. Biochem. Biophys. Res. Commun. 198:693-700.
52. Boden, S.D., K. McCuaig, G. Hair, M. Racine, L. Titus, J.M. Wozney, and M.S. Nanes. 1996. Differential effects and glucocorticoid polentiation of bone morphogenetic protein action during rat osteoblast differentiation in vitro. Endocrinology. 137:3401-3407.
53. Levenson, A.S., and V.C. Jordan. 1994. Transfection of human estrogen receptor (ER) cDNA into ER-negative mammalian cells. J. Steroid Biochem. Mol. Biol. 51:229-239.