Recombinant human bone morphogenetic protein-2 promotes Indian hedgehog-mediated osteo-chondrogenic differentiation of a human chondrocytic cell line in vivo and in vitro

Differentiation

Volumn 72, Issue 1, 2004, Pages 32-40

  Uyama, Yohei ^a   Yagami, Kimitoshi ^a   Hatori, Masashi ^a   Kakuta, Saburo ^a   Nagumo, Masao ^a  

^a SHOWA UNIVERSITY   (Japan)

Author keywords

Bone morphogenetic protein 2; Chondrocyte; Chondrogenesis; Indian hedgehog; Osteogenesis

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 10; COLLAGEN TYPE 2; MESSENGER RNA; OSTEOCALCIN; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR RUNX2; BMP2 PROTEIN, HUMAN; BMP2 PROTEIN, MOUSE; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; RECOMBINANT HUMAN BONE MORPHOGENETIC PROTEIN 2; RECOMBINANT HUMAN BONE MORPHOGENETIC PROTEIN-2; RECOMBINANT PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BONE DEVELOPMENT; CANCER GRAFT; CANCER TRANSPLANTATION; CARTILAGINOUS TISSUE; CELL DIFFERENTIATION; CELL LINE; CHONDROGENESIS; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOSARCOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; CARTILAGE CELL; CELL DIVISION; CYTOLOGY; DRUG EFFECT; GENETICS; METABOLISM; PHYSIOLOGY; UPREGULATION;

ANIMALIA; ERINACEIDAE;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE II; COLLAGEN TYPE X; CORE BINDING FACTOR ALPHA 1 SUBUNIT; HEDGEHOG PROTEINS; HUMANS; MICE; NEOPLASM PROTEINS; OSTEOBLASTS; OSTEOCALCIN; OSTEOGENESIS; RECOMBINANT PROTEINS; RNA, MESSENGER; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 7044271641     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2004.07201001.x     Document Type: Article

References (41)

1. Aikawa, T., Shirasuna, K., Iwamoto, M., Watatani, K., Nakamura, T., Okura, M., Yoshioka, H. and Matsuya, T. (1996) Establishment of bone morphogenetic protein 2 responsive chondrogenic cell line. J Bone Miner Res 11:544-553.
2. Bruder, S.P., Gazit, D., Passi-Even, L., Bab, I. and Caplan, A.I. (1990) Osteochondral differentiation and the emergence of stage-specific osteogenic cell-surface molecules by bone marrow cells in diffusion chambers. Bone Miner 11:141-151.
3. Carlberg, A.L., Pucci, B., Rallapalli, R., Tuan, R.S. and Hall, D.J. (2001) Efficient chondrogenic differentiation of mesenchymal cells in micro-mass culture by retroviral gene transfer of BMP-2. Differentiation 67:128-138.
4. Celeste, A.J., Iannazzi, J.A., Taylor, R.C., Hewick, R.M., Rosen, V., Wang, E.A. and Wozney, J.M. (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.
5. Chano, T., Okabe, H., Saeki, Y., Isizawa, M., Matsumoto, K. and Hukuda, S. (1998) Characterization of newly established human chondrosarcoma cell line, CS-OKB. Virchows Arch 432:529-534.
6. Chen, P., Carrington, J.L., Hammonds, R.G. and Reddi, A. (1991) Stimulation of chondrogenesis in limb bud mesoderm cells by recombinant human bone morphogenetic protein 2B (BMP-2B) and modulation by transforming growth factor β1 and β2. Exp Cell Res 195:509-515.
7. 2+-bindine slycoprotein. J Cell Biol 103:1615-1623.
8. Ducy, P., Zhang, R., Geoffroy, V., Ridall, A.L. and Karsenty, G. (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747-754.
9. Enomoto, H., Enomoto-Iwamoto, M., Iwamoto, M., Nomura, S., Himeno, M., Kitamura, Y., Kishimoto, T. and Komori, T. (2000) Cbfa1 is a positive regulatory factor in chondrocyte maturation. J Biol Chem 275:8695-8702.
10. Enomoto-Iwamoto, M., Nakamura, T., Aikawa, T., Higuchi, Y., Yuasa, T., Yamaguchi, A., Nohno, T., Noji, S., Matsuya, T., Kurisu, K., Koyama, E., Pacifia, M. and Iwamoto, M. (2000) Hedgehog proteins stimulate chondrogenic cell differentiation and cartilage formation. J Bone Miner Res 15:1659-1668.
11. Fochet, R.J. and Adams, S.L. (1984) Tissue specificity of type I collagen gene expression is determined at both transcriptional and post-transcriptional levels. Mol Cell Biol 4:1843-1852.
12. Francis, P.H., Richardson, K.M., Brickell, P.M. and Tickle, C. (1994) Bone morphogenetic proteins and a signaling pathway that controls patterning chick limb. Development 120:209-218.
13. Gerstenfeld, L.C., Crucete, J., Shea, C.M., Sampath, K., Barnes, G.L. and Einhorn, T.A. (2002) Chondrocytes provide morphogenic signals that selectively induce osteogenic differentiation of mesenchymal stem cells. J Bone Miner Res 17:221-230.
14. Hall, B.K. and Miyake, T. (2002) All for one and one for all: condensations and the initiation of skeletal development. Bioessays 22:138-147.
15. Haraki, T., Oshima, O., Kakuta, S., Kimura, Y. and Nagumo, M. (1992) Localization of types I, II and X collagen in the transplanted tumor derived from a human osteoaenic sarcoma. Bone 13:121-128.
16. Hiraki, Y., Inoue, H., Shigeno, C., Sanma, Y., Bentz, H., Rosen, D.M., Asada, A. and Suzuki, F. (1991) Bone morphogenetic proteins (BMP-2 and BMP-3) promote growth and expression of the differentiated phenotype of rabbit chondrocytes and osteoblastic MC3T3-E1 cells in vitro. J Bone Miner Res 6:1373-1385.
17. Imoto, E., Kakuta, S., Hori, M., Yagami, K. and Nagumo, M. (2002) Adhesion of a chondrocytic cell line (USAC) to fibronectin and its resulation by proteoelycan. J Oral Pathol Med 31:35-44.
18. Kalajzic, I., Kalajzic, Z., Kaliterna, M., Gronowicz, G., Clark, S.H., Lichtler, A.C. and Rowe, D. (2002) Use of type I collagen green fluorescent protein transgenes to identify subpopulations of cells at different stages of the osteoblast lineace. J Bone Miner Res 17:15-25.
19. 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. (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owine to maturational arrest of osteoblasts. Cell 89:755-764.
20. Kosher, R.A., Kulyd, W.M. and Gay, S.W. (1986) Collagen gene expression durine limb cartilage differentiation. J Cell Biol 102:1151-1156.
21. Kravis, D. and Upholt, W.B. (1985) Quantitaten of type II procollagen mRNA levels during chick limb cartilage differentiation. Dev Biol 108:164-172.
22. Lai, C.F. and Cheng, S.L. (2002) Signal transductions induced by bone morphogenetic protein-2 and transforming growth factor-β in normal human osteoblastic cells. J Biol Chem 277:15514-15522.
23. Minina, E., Wenzel, H.M., Kreschel, C., Karp, S., Gaffield, W., McMahon, A.P. and Vortkamp, A. (2001) BMP and Ihh/PTHrP signaling interact to coordinate chondrocyte proliferation and differentiation. Development 128:4523-4534.
24. Nah, H.D., Pacifici, M., Gerstenfeld, L.C., Adams, S.L. and Kirsch, T. (2000) Transient chondrogenic phase in the intra-membranous pathway during normal skeletal development. J Bone Miner Res 15:522-533.
25. Nakahara, H., Goldberg, V.M. and Caplan, A.I. (1991) Culture-expanded human periosteal-derived cells exhibit osteochondral potential m vivo. J Orthop Res 9:465-476.
26. Nakashima, K., Zhou, X., Kunkel, G., Zhang, Z., Deng, J.M., Behringer, R.R. and de Crombrugghe, B. (2002) The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 108:17-29.
27. Oyajobi, B.O., Frazer, A., Hollander, A.P., Graveley, R.M., Xu, C., Houghton, A., Hatten, P.V., Russell, R.G. and Stringer, B.M. (1998) Expression of type X collagen and matrix calcification in three-dimensional cultures of immortalized temperature-sensitive chondrocytes derived from adult human articular cartilage. J Bone Miner Res 13:432-442.
28. Pittenger, M.F., Mackay, A.M., Beck, S.C., Jaiswal, R.K., Douglas, R., Mosca, J.D., Moorman, M.A., Simonetti, D.W., Craig, S. and Marshak, D.R. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
29. Rivas, R. and Shapiro, F. (2002) Structural stages in the development of the long bones and epiphyses: a study in the New Zealand white rabbit. J Bone Joint Surg Am 84:85-100.
30. Shukunami, C., Ohta, Y., Sakuda, M. and Hiraki, Y. (1998) Sequential progression of the differentiation program by bone morphogenetic protein-2 in chondrogenic cell line ATDC5. Exp Cell Res 241:1-11.
31. Stein, G.S. and Lian, J.B. (1993) Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr Rev 14:424-442.
32. St-Jacques, B., Hammerschmidt, M. and McMahon, A.P. (1999) Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13:2072-2086.
33. Ueta, C., Iwamoto, M., Kanatani, N., Yoshida, C., Liu, Y., Enomoto-Iwamoto, M., Ohmori, T., Enomoto, H., Nakata, K., Takada, K., Kurisu, K. and Komori, T. (2001) Skeletal malformations caused by overexpression of Cbfa1 or its dominant negative form in chondrocytes. J Cell Biol 153:87-100.
34. von der Mark, K. and von der Mark, H. (1977) Immunological and biochemical studies of collagen type transition during in vitro chondrogenesis of chick limb mesodermal cells. J Cell Biol 73:736-747.
35. Vortkamp, A., Lee, K., Lanske, B., Segre, G.V., Kronenberg, H.M. and Tabin, C.J. (1996) Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273:613-622.
36. Wang, E.A., Rosen, V., D'Alessandro, J.S., Bauduyn, M., Cordes, P., Harada, T., Israel, D.I., Hewick, R.M., Kerns, K.M., LaPan, P., Luxenberg, D.P., McQuaid, D., Moutsatsos, I.K., Nove, J. and Wozney, J.M. (1990) Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224.
37. Weir, E.C., Philbrick, W.M., Amling, M., Neff, L.A., Baron, R. and Broadus, A.E. (1996) Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc Natl Acad Sci USA 93:10240-10245.
38. Wozney, J.M., Rosen, V., Celeste, A.J., Mitsock, L.M., Whitters, M.J., Kriz, R.W., Hewick, R.M. and Wang, E.A. (1988) Novel regulators of bone formation: molecular clones and activities. Science 242:1528-1534.
39. Yagami, K., Kakuta, S., Tachibana, H. and Nagumo, M. (2000) Establishment of a cell line with phenotypes of chondrocyte from a human osteosenic sarcoma of the mandible. J Oral Pathol Med 29:321-330.
40. Yamasuchi, A., Katagiri, T., Ikeda, T., Wozney, J.M., Rosen, V., Wang, E.A., Kahn, A., Suda, T. and Yoshiki, S. (1991) Recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687.
41. Yamaguchi, A., Ishizuya, T., Kintou, N., Wada, Y., Katagiri, T., Wozney, J.M., Rosen, V. and Yoshiki, S. (1996) Effects of BMP-2, BMP-4, and BMP-6 on osteoblastic differentiation of bone marrow-derived stromal cell lines, ST2 and MC3T3-G2/PA6. Biochem Biophys Res Commun 220:366-371.