Enhancement of bone morphogenetic protein-2-induced ectopic bone formation by transforming growth factor-β1

Tissue Engineering - Part A

Volumn 17, Issue 5-6, 2011, Pages 597-606

  Tachi, Keita ^a   Takami, Masamichi ^a   Sato, Hana ^a   Mochizuki, Ayako ^a   Zhao, Baohong ^a,d   Miyamoto, Yoichi ^a   Tsukasaki, Hiroaki ^a   Inoue, Tomio ^a   Shintani, Satoru ^a   Koike, Tatsuya ^b   Honda, Yoshitomo ^c   Suzuki, Osamu ^c   Baba, Kazuyoshi ^a   Kamijo, Ryutaro ^a  

^a SHOWA UNIVERSITY   (Japan)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

^d HOSPITAL FOR SPECIAL SURGERY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMINERALIZATION; COLLAGEN; DEFECTS; HISTOLOGY; OSTEOBLASTS; PEPTIDES;

BONE DEFECT; BONE MORPHOGENETIC PROTEIN-2; BONE MORPHOGENETIC PROTEINS; BONE REGENERATION; BONE VOLUME; CLINICAL TREATMENTS; COLLAGEN SPONGE; ECTOPIC BONES; MOUSE CALVARIA; MUSCLE TISSUES; ORTHOTOPIC; PARTIAL FILLING; TRANSFORMING GROWTH FACTORS; TREATMENT METHODS;

BONE;

BONE MORPHOGENETIC PROTEIN 2; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; ARTICLE; BONE DEVELOPMENT; BONE REGENERATION; CELL COUNT; CELL DIFFERENTIATION; CHORISTOMA; CYTOLOGY; DRUG EFFECT; HUMAN; MOUSE; ORGAN SIZE; OSTEOBLAST; OSTEOCLAST; PATHOLOGY; RADIOGRAPHY; SKULL; TIME;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CELL COUNT; CELL DIFFERENTIATION; CHORISTOMA; HUMANS; MICE; ORGAN SIZE; OSTEOBLASTS; OSTEOCLASTS; OSTEOGENESIS; SKULL; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 79952177539     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2010.0094     Document Type: Article

References (57)

1. Hogan, B. L. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev 10, 1580, 1996.
2. Newfeld, S. J., Wisotzkey, R. G., and Kumar, S. Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-β family ligands, receptors and Smad signal transducers. Genetics 152, 783, 1999.
3. Chang, W., ten Dijke, P., and Wu, D. K. BMP pathways are involved in otic capsule formation and epithelial-mesenchymal signaling in the developing chicken inner ear. Dev Biol 251, 380, 2002.
4. Zhao, G. Q. Consequences of knocking out BMP signaling in the mouse. Genesis 35, 43, 2003.
5. Katagiri, T., and Takahashi, N. Regulatory mechanisms of osteoblast and osteoclast differentiation. Oral Dis 8, 147, 2002.
6. Canalis, E., Economides, A. N., and Gazzerro, E. Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24, 218, 2003.
7. Waite, K. A., and Eng, C. From developmental disorder to heritable cancer: it's all in the BMP/TGF-β family. Nat Rev Genet 4, 763, 2003.
8. Wan, M., and Cao, X. BMP signaling in skeletal development. Biochem Biophys Res Commun 328, 651, 2005.
9. Yasko, A. W., Lane, J. M., Fellinger, E. J., Rosen, V., Wozney, J. M., and Wang, E. A. The healing of segmental bone defects, induced by recombinant human bone morphogenetic protein (rhBMP-2). A radiographic, histological, and biomechanical study in rats. J Bone Joint Surg Am 74, 659, 1992.
10. Marukawa, E., Asahina, I., Oda, M., Seto, I., Alam, M. I., and Enomoto, S. Bone regeneration using recombinant human bone morphogenetic protein-2 (rhBMP-2) in alveolar defects of primate mandibles. Br J Oral Maxillofac Surg 39, 452, 2001.
11. Matin, K., Nakamura, H., Irie, K., Ozawa, H., and Ejiri, S. Impact of recombinant human bone morphogenetic protein-2 on residual ridge resorption after tooth extraction: an experimental study in the rat. Int J Oral Maxillofac Implants 16, 400, 2001.
12. Urist, M. R. Bone: formation by autoinduction. Science 150, 893, 1965.
13. Thies, R. S., Bauduy, M., Ashton, B. A., Kurtzberg, L., Wozney, J. M., and Rosen, V. Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells. Endocrinology 130, 1318, 1992.
14. Wozney, J. M., Rosen, V., Celeste, A. J., Mitsock, L. M., Whitters, M. J., Kriz, R. W., Hewick, R. M., and Wang, E. A. Novel regulators of bone formation: molecular clones and activities. Science 242, 1528, 1988.
15. Wang, E. A., Rosen, V., D'Alessandro, J. S., Bauduy, M., Cordes, P., Harada, T., Israel, D. I., Hewick, R. M., Kerns, K. M., and LaPan, P. Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci U S A 87, 2220, 1990.
16. Sampath, T. K., Maliakal, J. C., Hauschka, P. V., Jones, W. K., Sasak, H., Tucker, R. F., White, K. H., Coughlin, J. E., Tucker, M. M., and Pang, RH. Recombinant human osteogenic protein-1 (hOP-1) induces new bone formation in vivo with a specific activity comparable with natural bovine osteogenic protein and stimulates osteoblast proliferation and differentiation in vitro. J Biol Chem 267, 20352, 1992.
17. Hughes, F. J., Collyer, J., Stanfield, M., and Goodman, S. A. The effects of bone morphogenetic protein-2,-4, and-6 on differentiation of rat osteoblast cells in vitro. Endocrinology 136, 2671, 1995.
18. Boden, S. D., Hair, G., Titus, L., Racine, M., McCuaig, K., Wozney, J. M., and Nanes, M. S. Glucocorticoid-induced differentiation of fetal rat calvarial osteoblasts is mediated by bone morphogenetic protein-6. Endocrinology 138, 2820, 1997.
19. Yamaguchi, A., Komori, T., and Suda, T. Regulation of osteoblast differentiation mediated by bone morphogenetic proteins, hedgehogs, and Cbfa1. Endocr Rev 21, 393, 2000.
20. Bentz, H., Thompson, A. Y., Armstrong, R., Chang, R. J., Piez, K. A., and Rosen, D. M. Transforming growth factor-β2 enhances the osteoinductive activity of a bovine bone-derived fraction containing bone morphogenetic protein-2 and 3. Matrix 11, 269, 1991.
21. Urist, M. R., Kovacs, S., and Yates, K. A. Regeneration of an enchondroma defect under the influence of an implant of human bone morphogenetic protein. J Hand Surg Am 11, 417, 1986.
22. Boden, S. D., Zdeblick, T. A., Sandhu, H. S., and Heim, S. E. The use of rhBMP-2 in interbody fusion cages. Definitive evidence of osteoinduction in humans: a preliminary report. Spine (Phila Pa 1976) 25, 376, 2000.
23. Boden, S. D., Kang, J., Sandhu, H., and Heller, J. G. Use of recombinant human bone morphogenetic protein-2 to achieve posterolateral lumbar spine fusion in humans: a prospective, randomized clinical pilot trial: 2002 Volvo Award in clinical studies. Spine (Phila Pa 1976) 27, 2662, 2002.
24. Burkus, J. K., Gornet, M. F., Dickman, C. A., and Zdeblick, T. A. Anterior lumbar interbody fusion using rhBMP-2 with tapered interbody cages. J Spinal Disord Tech 15, 337, 2002.
25. Friess, W., Uludag, H., Foskett, S., Biron, R., and Sargeant, C. Characterization of absorbable collagen sponges as recombinant human bone morphogenetic protein-2 carriers. Int J Pharm 185, 51, 1999.
26. Winn, S. R., Uludag, H., and Hollinger, J. O. Carrier systems for bone morphogenetic proteins. Clin Orthop Relat Res (367 Suppl), S95, 1999.
27. Horiuchi, H., Saito, N., Kinoshita, T., Wakabayashi, S., Yotsumoto, N., and Takaoka, K. Effect of phosphodiesterase inhibitor-4, rolipram, on new bone formations by recombinant human bone morphogenetic protein-2. Bone 30, 589, 2002.
28. Yamamoto, M., Takahashi, Y., and Tabata, Y. Controlled release by biodegradable hydrogels enhances the ectopic bone formation of bone morphogenetic protein. Biomaterials 24, 4375, 2003.
29. Horiuchi, H., Saito, N., Kinoshita, T., Wakabayashi, S., Tsutsumimoto, T., Otsuru, S., and Takaoka, K. Enhancement of recombinant human bone morphogenetic protein-2 (rhBMP-2)-induced new bone formation by concurrent treatment with parathyroid hormone and a phosphodiesterase inhibitor, pentoxifylline. J Bone Miner Metab 22, 329, 2004.
30. Kim, C. S., Kim, J. I., Kim, J., Choi, S. H., Chai, J. K., Kim, C. K., and Cho, K. S. Ectopic bone formation associated with recombinant human bone morphogenetic proteins-2 using absorbable collagen sponge and beta tricalcium phosphate as carriers. Biomaterials 26, 2501, 2005.
31. Hosseinkhani, H., Yamamoto, M., Inatsugu, Y., Hiraoka, Y., Inoue, S., Shimokawa, H., and Tabata, Y. Enhanced ectopic bone formation using a combination of plasmid DNA impregnation into 3-D scaffold and bioreactor perfusion culture. Biomaterials 27, 1387, 2006.
32. Hsu, H. P., Zanella, J. M., Peckham, S. M., and Spector, M. Comparing ectopic bone growth induced by rhBMP-2 on an absorbable collagen sponge in rat and rabbit models. J Orthop Res 24, 1660, 2006.
33. Majid, K., Tseng, M. D., Baker, K. C., Reyes-Trocchia, A., and Herkowitz, H. N. Biomimetic calcium phosphate coatings as bone morphogenetic protein delivery systems in spinal fusion. Spine J 2010 Jan 22 [Epub ahead of print].
34. Zhao, B., Katagiri, T., Toyoda, H., Takada, T., Yanai, T., Fukuda, T., Chung, U. I., Koike, T., Takaoka, K., and Kamijo, R. Heparin potentiates the in vivo ectopic bone formation induced by bone morphogenetic protein-2. J Biol Chem 281, 23246, 2006.
35. Kubota, K., Iseki, S., Kuroda, S., Oida, S., Iimura, T., Duarte, W. R., Ohya, K., Ishikawa, I., and Kasugai, S. Synergistic effect of fibroblast growth factor-4 in ectopic bone formation induced by bone morphogenetic protein-2. Bone 31, 465, 2002.
36. Suzuki, O., Kamakura, S., Katagiri, T., Nakamura, M., Zhao, B., Honda, Y., and Kamijo, R. Bone formation enhanced by implanted octacalcium phosphate involving conversion into Ca-deficient hydroxyapatite. Biomaterials 27, 2671, 2006.
37. Sato, Y., Takita, H., Ohata, N., Tamura, M., and Kuboki, Y. Pleiotrophin regulates bone morphogenetic protein (BMP) - induced ectopic osteogenesis. J Biochem 131, 877, 2002.
38. Nakamura, Y., Tensho, K., Nakaya, H., Nawata, M., Okabe, T., and Wakitani, S. Low dose fibroblast growth factor-2 (FGF-2) enhances bone morphogenetic protein-2 (BMP-2) - induced ectopic bone formation in mice. Bone 36, 399, 2005.
39. Ogawa, Y., Schmidt, D. K., Nathan, R. M., Armstrong, R. M., Miller, K. L., Sawamura, S. J., Ziman, J. M., Erickson, K. L., de Leon, E. R., and Rosen, D. M. Bovine bone activin enhances bone morphogenetic protein-induced ectopic bone formation. J Biol Chem 267, 14233, 1992.
40. Toyoda, H., Terai, H., Sasaoka, R., Oda, K., and Takaoka, K. Augmentation of bone morphogenetic protein-induced bone mass by local delivery of a prostaglandin E EP4 receptor agonist. Bone 37, 555, 2005.
41. Horiuchi, H., Saito, N., Kinoshita, T., Wakabayashi, S., Tsutsumimoto, T., and Takaoka, K. Enhancement of bone morphogenetic protein-2-induced new bone formation in mice by the phosphodiesterase inhibitor pentoxifylline. Bone 28, 290, 2001.
42. Ripamonti, U., Duneas, N., Van Den Heever, B., Bosch, C., and Crooks, J. Recombinant transforming growth factor-β1 induces endochondral bone in the baboon and synergizes with recombinant osteogenic protein-1 (bone morphogenetic protein-7) to initiate rapid bone formation. J Bone Miner Res 12, 1584, 1997.
43. Duneas, N., Crooks, J., and Ripamonti, U. Transforming growth factor-β1: induction of bone morphogenetic protein genes expression during endochondral bone formation in the baboon, and synergistic interaction with osteogenic protein-1 (BMP-7). Growth Factors 15, 259, 1998.
44. Simmons, C. A., Alsberg, E., Hsiong, S., Kim, W. J., and Mooney, D. J. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 35, 562, 2004.
45. Alliston, T., Choy, L., Ducy, P., Karsenty, G., and Derynck, R. TGF-β-induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation. EMBO J 20, 2254, 2001.
46. Spinella-Jaegle, S., Roman-Roman, S., Faucheu, C., Dunn, F. W., Kawai, S., Gallea, S., Stiot, V., Blanchet, A. M., Courtois, B., Baron, R., and Rawadi, G. Opposite effects of bone morphogenetic protein-2 and transforming growth factor-β1 on osteoblast differentiation. Bone 29, 323, 2001.
47. Centrella, M., Horowitz, M. C., Wozney, J. M., and McCarthy, T. L. Transforming growth factor-β gene family members and bone. Endocr Rev 15, 27, 1994.
48. Centrella, M., Casinghino, S., Kim, J., Pham, T., Rosen, V., Wozney, J., and McCarthy, T. L. 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, 1995.
49. Maeda, S., Hayashi, M., Komiya, S., Imamura, T., and Miyazono, K. Endogenous TGF-β signaling suppresses maturation of osteoblastic mesenchymal cells. EMBO J 23, 552, 2004.
50. Sells Galvin, R. J., Gatlin, C. L., Horn, J. W., and Fuson, T. R. TGF-β enhances osteoclast differentiation in hematopoietic cell cultures stimulated with RANKL and M-CSF. Biochem Biophys Res Commun 265, 233, 1999.
51. Chenu, C., Pfeilschifter, J., Mundy, G. R., and Roodman, G. D. Transforming growth factor β inhibits formation of osteoclast-like cells in long-term human marrow cultures. Proc Natl Acad Sci U S A 85, 5683, 1988.
52. Chenu, C., Serre, C. M., Raynal, C., Burt-Pichat, B., and Delmas, P. D. Glutamate receptors are expressed by bone cells and are involved in bone resorption. Bone 22, 295, 1998.
53. Tang, Y., Wu, X., Lei, W., Pang, L., Wan, C., Shi, Z., Zhao, L., Nagy, T. R., Peng, X., Hu, J., Feng, X., Van Hul, W., Wan, M., and Cao, X. TGF-β1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat Med 15, 757, 2009.
54. Roman, A. C., Carvajal-Gonzalez, J. M., Rico-Leo, E. M., and Fernandez-Salguero, P. M. Dioxin receptor deficiency impairs angiogenesis byamechanism involving VEGF-A depletion in the endothelium and transforming growth factor-β overexpression in the stroma. J Biol Chem 284, 25135, 2009.
55. Ferrari, G., Cook, B. D., Terushkin, V., Pintucci, G., and Mignatti, P. Transforming growth factor-β 1 (TGF-β1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J Cell Physiol 219, 449, 2009.
56. Merwin, J. R., Anderson, J. M., Kocher, O., Van Itallie, C. M., and Madri, J. A. Transforming growth factor β 1 modulates extracellular matrix organization and cell-cell junctional complex formation during in vitro angiogenesis. J Cell Physiol 142, 117, 1990.
57. Tuxhorn, J. A., McAlhany, S. J., Yang, F., Dang, T. D., and Rowley, D. R. Inhibition of transforming growth factor-β activity decreases angiogenesis in a human prostate cancer-reactive stroma xenograft model. Cancer Res 62, 6021, 2002.