Inhibition of TGF-β receptor signaling in osteoblasts leads to decreased bone remodeling and increased trabecular bone mass

Development

Volumn 126, Issue 19, 1999, Pages 4267-4279

  Filvaroff, Ellen ^a,c   Erlebacher, Adrian ^a   Ye, Jian Qin ^a,b   Gitelman, Stephen E ^a,b   Lotz, Jeffrey ^a   Heillman, Moira ^a   Derynck, Rik ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GENENTECH INC   (United States)

Author keywords

Biochemical property; Bone; Osteoblast; TGF ; Transgenic mouse

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE MASS; BONE MATRIX; BONE REMODELING; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOPLASM; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; TRABECULAR BONE; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; BONE AND BONES; BONE DENSITY; BONE DEVELOPMENT; BONE REMODELING; FEMALE; FEMUR; GENES, DOMINANT; KINETICS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; OSTEOBLASTS; OSTEOCALCIN; OVARY; PROMOTER REGIONS (GENETICS); RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SKULL;

EID: 0032710016     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. Bain, S. D., Jensen, E., Celino, D. L., Bailey, M. C., Lantry, M. M. and Edwards, M. W. (1993). High-dose gestagens modulate bone resorption and formation and enhance estrogen-induced endosteal bone formation in the ovariectomized mouse. J. Bone Min. Res. 8, 219-230.
2. Baker, A. R., Hollingshead, P. G., Pitts, M. S., Hansen, S., Taylor, R. and Stewart, T. A. (1992). Osteoblast-specific expression of growth hormone stimulates bone growth in transgenic mice. Mol. Cell. Biol. 12, 5541-5547.
3. Beaudreuil, J., Mbalaviele, G., Cohen-Solal, M., Morieux, C., De Vernejoul, M. C. and Orcel, P. (1995). Short-term local injections of transforming growth factor-β1 decrease ovariectomy-stimulated osteoclastic resorption in vivo in rats. J. Bone Miner. Res. 10, 971-977.
4. Beck, L. S., DeGuzman, L., Lee, W. P., Xu, Y., McFatridge, L. A., Gillett, N. A. and Amento, E. P. (1991). TGF-β1 induces bone closure of skull defects. J. Bone Miner. Res. 6, 1257-1265.
5. Bonewald, L. F. and Dallas, S. L. (1994). Role of active and latent transforming growth factor β in bone formation. J. Cell. Biochem. 55, 350-357.
6. Bostrom, M. P. G. and Asnis, P. (1998). Transforming growth factor β in fracture repair. Clin. Orthop. Rel. Res. 355S, S124-S131.
7. Brand, T., McClellan, W. R. and Schneider, M. D. (1993) A dominant-negative receptor for type β transforming growth factors created by deletion of the kinase domain. J. Biol. Chem. 268, 11500-11503.
8. Brand, T. and Schneider, M. D. (1995). Inactive type II and type I receptors for TGF-β are dominant negative inhibitors of TGF-β dependent transcription. J. Biol. Chem. 270, 8274-8284.
9. Breen, E. C., Ignotz, R. A., McCabe, L., Stein, J. L., Stein, G. S. and Lian, J. B. (1994). TGF-β alters growth and differentiation related gene expression in proliferating osteoblasts in vitro, preventing development of the mature bone phenotype. J. Cell. Physiol. 160, 323-335.
10. Bronckers, A. L., Gay, S., Dimuzio, M. T. and Butler, W. T. (1985). Immunolocalization of γ-carboxyglutamic acid containing proteins in developing rat bones. Coll. Relat. Res. 5, 273-281.
11. Bucay, N., Sarosi, I., Dunstan, C.R., Morony, S., Tarpley, J., Capparelli, C., Scully, S., Tan, H. L., Xu, W., Lacey, D. L., Boyle, W. J. and Simonet, W. S. (1998). Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 12, 1260-1268.
12. Carrington, J. L., Roberts, A. B., Flanders, K. C., Roche, N. S. and Reddi, A. H. (1988). Accumulation, localization, and compartmentation of transforming growth factor β during endochondral bone development. J. Cell Biol. 107, 1969-1975.
13. Cauley, J. A., Seeley, D. G., Ensrud, R., Ettinger, B., Black, D. and Cummings, S. R. (1995). Estrogen replacement therapy and fractures in older women. Ann. Int. Med. 122, 9-16.
14. Centrella, M., McCarthy, T. L. and Canalis, E. (1988). Parathyroid hormone modulates transforming growth factor β activity and binding in osteoblastic cells. Proc. Natl. Acad. Sci. USA 85, 5889-5893.
15. Centrella, M., Horowitz, M. C., Wozney, J. M. and McCarthy, T. L. (1994). Transforming growth factor-β gene family members and bone. Endocr. Rev. 15, 27-39.
16. Centrella, M., Casinghino, S., Kim, J., Pham, T., Rosen, V., Wozney, J. and McCarthy, T. L. (1995). Independent changes in type I and type II receptors for transforming growth factor β induced by bone morphogenetic protein 2 parallel expression of the osteoblast phenotype. Mol. Cell. Biol. 15, 3273-3281.
17. Chen, R.-H., Ebner, R. and Derynck, R. (1993). Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-β activities. Science 260, 1335-1338.
18. Chénu, C., Pfeilschifter, J., Mundy, G. R. and Roodman, G. D. (1988). Transforming growth factor-β inhibits formation of osteoclast-like cells in long-term human marrow cultures. Proc. Natl. Acad. Sci. USA 85, 5683-5687.
19. Chomczynski P, and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 162, 156-159.
20. Cohen, M. M. (1997). Transforming growth factor βs and fibroblast growth factors and their receptors: role in sutural biology and craniosynostosis. J. Bone and Min. Res. 12, 322-331.
21. Corral, D. A., Amling, M., Priemel, M., Loyer, E., Fuchs, S., Ducy, P., Baron, R. and Karsenty, G. (1998). Dissociation between bone resorption and bone formation in osteopenic transgenic mice. Proc. Natl. Acad. Sci. USA 95, 13835-13840.
22. Derynck, R. and Feng, X.-H. (1997). TGF-β receptor signaling. BBA Reviews in Cancer 1333, F105-F150
23. Diebold, R. J., Eis, M. J., Yin, M., Ormsby, I., Boivin, G. P., Darrow, B. J., Saffitz, J. E. and Doetschman, T. (1995). Early-onset multifocal inflammation in the transforming growth factor β1-null mouse is lymphocyte mediated. Proc. Natl. Acad. Sci. USA 92, 12215-12219.
24. Dieudonné, S. C., Foo, P., van Zoelen, E. J. and Burger, E. H. (1991). Inhibiting and stimulating effects of TGF-ßl on osteoclastic bone résorption in fetal mouse bone organ cultures. J. Bone Miner. Res. 6, 479-487.
25. 32P-based hybridizations. Anal. Biochem. 210, 235-244.
26. Erlebacher, A., Filvaroff, E. H., Gitelman, S. E. and Derynck, R. (1995) Toward a molecular understanding of skeletal morphogenesis. Cell 80, 371-378.
27. Erlebacher, A. and Derynck, R. (1996). Increased expression of TGF-β2 in osteoblasts results in an osteoporosis-like phenotype. J. Cell Biol. 132, 195-210.
28. Erlebacher, A., Filvarotf, E. H., Ye, J.-Q. and Derynck, R. (1998). Osteoblastic responses to TGF-beta during bone remodeling. Mol Biol Cell. 7, 1903-1918.
29. Evan, G. I., Lewis, G. K., Ramsay, G. and Bishop, J. M. (1985). Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5, 3610-3616.
30. Filvaroff, E., Ebner, R. and Derynck, R. (1994). Inhibition of myogenic differentation in myoblasts expressing a truncated type II TGF-β receptor. Development 120, 1085-1095.
31. Filvaroff, E. and Derynck, R. (1998). Bone remodelling: a signalling system for osteoclast regulation. Curr. Biol. 8, R679-R682.
32. Finkelman, R. D., Bell, N. H., Strong, D. D., Demers, L. M. and Baylink, D. J. (1992). Ovariectomy selectively reduces the concentration of transforming growth factor β in rat bone: implication for estrogen deficiency-associated bone loss. Proc. Natl. Acad. Sci. USA 89, 12190-12193.
33. Frenkel, B., Capparelli, C., Van Auken, M., Baran, D., Bryan, J., Stein, J. L. Stein, G. S. and Lian, J. B. (1997). Activity of the osteocalcin promoter in skeletal sites of transgenic mice and during osteoblast differentiation in bone marrow-derived stromal cell cultures: effect of age and sex. Endocrinology 138, 2109-2116.
34. Gazit, D., Ebner, R., Kahn, A. J. and Derynck, R. (1993). Modulation of expression and cell surface binding of members of the transforming growth factor-β superfamily during retinoic acid-induced osteoblastic differentiation of multipotential mesenchymal cells. Mol. Endocrinol. 7, 189-198.
35. Geiser, A. G., Zeng, Q. Q., Sato, M., Helvering, L. M., Hirano, T. and Turner, C. H. (1998). Decreased bone mass and bone elasticity in mice lacking the transforming growth factor-b1 gene. Bone 23, 87-93.
36. Hattersley, G., and Chambers, T. J. (1991). Effects of transforming growth factor β1 on the regulation of osteoclastic development and function. J. Bone Miner. Res. 6, 165-172.
37. Hogan, B., Constantini, F. and Lacy, E. (1986). Manipulating the Mouse Embryo. A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 332 pp.
38. Hughes, D.E., Dai, A., Tiffee, J.C., Li, H. H., Mundy, G. R. and Boyce, B. F. (1996). Estrogen promotes apoptosis of murine osteoclasts mediates by TGF-β. Nat. Med. 2, 1132-1136.
39. Iba, K., Sawada, N., Nuka, S., Chiba, H., Obata, H., Isomura, H., Satoh, M., Ishii, S. and Mori, M. (1996). Phase-dependent effects of transforming growth factor β1 on osteoblastic markers of human osteoblastic cell line SV-HFO during mineralization. Bone 19, 363-369.
40. Ikeda, T., Shigeno, C., Kasai, R., Kohno, H., Ohta, S., Okumura, H., Konishi, J. and Yamamuro, T. (1993). Ovariectomy decreases the mRNA levels of transforming growth factor-β1 and increases the mRNA levels of osteocalcin in rat bone in vivo. Biochem. Biophys. Res. Comm. 194, 1228-1233.
41. Kalu, D. N., Salerno, E., Liu, C. C., Ferarro, F., Arjmandi, B. N. and Salih, M. A. (1993). Ovariectomy-induced bone loss and the hematopoietic system. Bone and Mineral 23, 145-161.
42. Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenisch, R. and Berns, A. (1991). Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293.
43. Lin, H.Y., Wang, X.-F., Ng-Eaton, E., Weinberg, R. A. and Lodish, H. F. (1992). Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell 68, 775-785.
44. Mackie, E. J. and Trechsel, U. (1990). Stimulation of bone formation in vivo by transforming growth factor-β: remodeling of woven bone and lack of inhibition by indomethacin. Bone 11, 295-300.
45. Manolagas, S.C. and Jilka, R. L. (1995). Bone marrow, cytokines, and bone remodeling: emerging insights into the pathophysiology of osteoporosis. New Engl. J. Med. 332, 305-311.
46. Marcelli, C., Yates, A. J. and Mundy, G. R. (1990). In vivo effects of human recombinant transforming growth factor β on bone turnover in normal mice. J. Bone Min. Res. 5, 1087-1096.
47. Marcus, R. (1996). Clinical review 76. The nature of osteoporosis. J. Clin. Endocrinol. Metab. 81, 1-5.
48. Miettinen P.J., Ebner, R., Lopez, A. R. and Derynck, R. (1994). TGF-β-induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 127, 2021-2036.
49. Most, D., Levine, J. P., Chang, J., Sung, J., McCarthy, J. G., Schendel, S. A. and Longaker, M. T. (1998). Studies in cranial suture biology: up-regulation of transforming growth factor-β1 and basic fibroblast growth factor mRNA correlates with posterior frontal cranial suture fusion in the rat. Plast. Reconstr. Surg. 101, 1431-1440.
50. Murakami, T., Yamamoto, M., Yamamoto, M., Ono, K., Nishikawa, M., Nagata, N., Motoyoshi, K. and Akatsu, T. (1998). Transforming growth factor-β1 increase mRNA levels of osteoclastogenesis inhibitory factor in osteoblastic/stromal cells and inhibits the survival of mutine osteoblast-like cells. Biochem. Biophys. Res. Comm. 252, 747-752.
51. O'Hare, K., Benoist, C. and Breathnach, R. (1981). Transformation of mouse fibroblasts to methotrexate resistance by a recombinant plasmid expressing a prokaryotic dihydrofolate reductase. Proc. Natl. Acad. Sci. USA. 78, 1527-1531.
52. Oreffo, R. O., Mundy, G. R., Seyedin, S. M. and Bonewald, L. F. (1989). Activation of the bone-derived latent TGF-β complex by isolated osteoclasts. Biochem. Biophys. Res. Commun. 158, 817-823.
53. Oursler, M. J., Cortese, C., Keeting, P., Anderson, M. A., Bonde, S. K. Riggs, B. L. and Spelsberg, T. C. (1991). Modulation of transforming growth factor-β production in normal human osteoblast-like cells by 17β-estradiol and parathyroid hormone. Endocrinology 129, 3313-3320.
54. Parfitt, A. M. (1983). The physiological and clinical significance of bone histomorphometric data. In Bone Histomorphometry: Techniques and Interpretation. (ed. R. R. Recker). pp. 143-223. Boca Raton, FL: CRC Press.
55. Parfitt, A. M., Drezner, M. K., Glorieux, G. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M. and Recker, R. R. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2, 595-610.
56. Parfitt, A. M. (1994). Osteonal and hemi-osteonal remodeling: the spatial and temporal framework for signal traffic in adult human bone. J. Cell. Biochem. 55, 273-286.
57. Pelton, R. W., Saxena, B., Jones, M., Moses, H. L. and Gold, L. I. (1991). Immunohistochemical localization of TGF-β1, TGF-β2. and TGF-β3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J. Cell. Biol. 115, 1091-105.
58. Pereira, R., Khillan, J. S., Helminen, H. J., Hume, E. L. and Prockop, D. J. (1993). Transgenic mice expressing a partially deleted gene for type I procollagen (COL1A1). A breeding line with a phenotype of spontaneous fractures and decreased bone collagen and mineral. J. Clin. Invest. 91, 709-716.
59. Pereira, R. F., Hume, E. L., Halford, K. W. and Prockop, D. J. (1995). Bone fragility in transgenic mice expressing a mutated gene for type 1 procollagen (Col1A1) parallels the age-dependent phenotype of human osteogenesis imperfecta. J. Bone Min. Res. 10, 1837-1843.
60. Pfeilschifter, J. and Mundy, G. R. (1987). Modulation of type β transforming growth factor activity in bone cultures by osteotropic hormones. Proc. Natl. Acad. Sci. USA 84, 2024-2028.
61. Pfeilschifter, J., Seyedin, S. M. and Mundy, G. R. (1988). Transforming growth factor β inhibits bone resorption in fetal rat long bone cultures. J. Clin. Invest. 82, 680-685.
62. Pfeilschifter, J., Diel, I., Scheppach, B., Bretz, A., Krempien, R., Erdmann, J., Schmid, G., Reske, N., Bismar, H., Seek, T., Krempien, B. and Ziegler, R. (1998). Concentration of transforming growth factor beta in human bone tissue: relationship to age, menopause, bone turnover, and bone volume. J. Bone Min. Res. 13, 716-730.
63. Pfeilschifter, F., Laukhuf, F., Muller-Beckmann, B., Blum, W. F., Pfister, T. and Ziegler, R. (1995). Parathyroid hormone increases the concentration of insulin-like growth factor I and transforming growth factor-β1 in rat bone. J. Clin. Invest. 96, 767-774.
64. Robey, P. G., Young, M. F., Flanders, K. C., Roche, N. S., Kondaiah, P., Reddi, A. H., Termine, J. D., Sporn, M. B. and Roberts, A. B. (1987). Osteoblasts synthesize and respond to transforming growth factor-type β (TGF-β) in vitro. J. Cell. Biol. 105, 457-463.
65. Rosen, D. M., Stempien, S. A., Thompson, A. Y. and Seyedin, S. M. (1988). Transforming growth factor-β modulates the expression of osteoblast and chondrocyte phenotypes in vitro. J. Cell. Physiol. 134, 337-346.
66. Rosier, R. N., O'Keefe, R. J. and Hicks, D. G. (1998). The potential role of transforming growth factor β in fracture healing. Clin. Orthop. Rel. Res. 355S, S294-S300.
67. Serra, R., Johnson, M., Filvaroff, E. H., LaBorde, J., Sheehan, D., Derynck, R. and Moses, H. J. (1997). Expression of a truncated, kinase-defective TGF-β type II receptor in mouse skeletal tissue promotes terminal chondrocyte differentiation and osteoarthritis. J. Cell Biol. 139, 541-552.
68. Seyedin, S. M., Thomas, T. C., Thompson, A. Y., Rosen, D. M. and Piez, K. A. (1985). Purification and characterization of two cartilage-inducing factors from bovine demineralized bone. Proc. Natl Acad. Sci. USA 82, 2267-2271.
69. Seyedin, S., Thompson, A.Y., Bentz, H., Rosen, D. M., McPherson, J. M., Conti, A., Siegel, N. R., Gallupi, G. R. and Piez, K. A. (1986). Cartilage-inducing factor-A: apparent identity to transforming frowth factor-β. J. Biol. Chem. 261, 5693-5695.
70. Sheehan, D. C. and Hrapchak, B. B. editors (1980). Theory and Practice of Histotechnology, 2nd edition, Columbus, OH: Batelle Press, p. 481.
71. Shinar, D. M. and Rodan, G. A. (1990). Biphasic effects of transforming growth factor-beta on the production of osteoclast-like cells in mouse bone marrow cultures: the role of prostaglandins in the generation of these cells. Endocrinol. 126, 3153-3158.
72. Shull, M. M., Ormsby, I., Kier, A. B., Pawlowski, S., Diebold, R. J., Yin, M., Allen, R., Sidman, C., Proetzel, G., Calvin, D., Annunziata, N. and Doetschman, T. (1992). Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359, 693-699.
73. Takai, H., Kanematsu, H., Yano, K., Tsuda, E., Higashio, K., Ikeda, K., Watanabe, K. and Yamada, Y. (1998). Transforming growth factor-β stimulates the production of osteoprotegerin/osteoclastogenesis inhibitory factor by bone marrow stromal cells. J. Biol. Chem. 42, 27091-27096.
74. Takaishi, T., Matsui, T., Tsukamoto, T., Ito, M., Taniguchi, T., Fukase, M. and Chihara, K. (1994). TGF-β-induced macrophage colony-stimulating factor gene expression in various mesenchymal cell lines. Am. J. Physiol. 267. C25-C31.
75. Tashjian, A. J., Voelkel, E. F., Lazzaro, M., Singer, F. R., Roberts, A. B., Derynck, R., Winkler, M. E. and Levine, L. (1985). α and β human transforming growth factors stimulate prostaglandin production and bone resorption in cultured mouse calvaria. Proc. Natl. Acad. Sci. USA 82, 4535-4538.
76. Vermeulen, A. H., Vermeer, C. and Bosman, F. T. (1989). Histochemical detection of osteocalcin in normal and pathological human bone. J. Histochem. Cytochem. 37,1503-1508.
77. Weibel, E. R. (1969). Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol. 26, 235-302.
78. Wrana, J. L., Attisano, L., Wieser, R., Ventura, F. and Massagué, J. (1994). Mechanism of activation of the TGF-β receptor. Nature 370, 341-247.
79. Wronski, T. J., Lowry, P. L., Walsh, C. C. and Ignaszewski, A. (1985). Skeletal alterations in ovariectomized rats. Calcif. Tissue Int. 37, 324-328.
80. Wronski, T. J., Walsh, C. C. and Ignaszewski, A. (1986). Histologic evidence for osteopenia and increased bone turnover in ovariectomized rats. Bone 7, 119-123.
81. Yamada, Y., Miyauchi, A., Goto, J., Takagi, Y., Okuizumi, H., Kanematsu, M., Hase, M., Takai, H., Harada, A. and Ikeda, K. 1998. Association of a polymorphism of the transforming growth factor-β1 gene with genetic susceptibility to osteoporosis in postmenopausal Japanese women. J. Bone Min. Res. 13, 1569-1576.