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)

References

• Arrick B. A., Lopez A. R., Elfman F., Ebner R., Damsky C. H., Derynck R. Altered metabolic and adhesive properties and increased tumorigenesis associated with increased expression of transforming growth factor beta 1. J. Cell Biol. 1992; 118: 715–726
   PubMedGoogle Scholar
• Assoian R. K. Purification of type-beta transforming growth factor from human platelets. Methods Enzymol. 1987; 146: 153–163
   PubMedGoogle Scholar
• Assoian R. K., Grotendorst G. R., Miller D. M., Sporn M. B. Cellular transformation by coordinated action of three peptide growth factors from human platelets. Nature (Lond.) 1984; 309: 804–806
   PubMed Web of Science ®Google Scholar
• Baldwin C. T., Reginato A. M., Smith C., Jimenez S. A., Prockop D. J. Structure of cDNA clones coding for human type II procollagen. The alpha 1 (II) chain is more similar to the alpha 1 (I) chain than two other alpha chains of fibrillar collagen. Biochem. J. 1989; 262: 521–528
   PubMed Web of Science ®Google Scholar
• Beck L. S., DeGuzman L., Lee W. P., Xu Y., McFatridge L. A., Gillett N. A., Amento E. P. TGF-β1 induces bone closure of skull defects. J. Bone Miner. Res. 1991; 6: 1257–1265
   PubMed Web of Science ®Google Scholar
• Beck L. S., Amento E. P., Xu Y., DeGuzman L., Lee W. P., Nguyen T., Gillett N. A. TGF-β1 induces bone closure of skull defects: Temporal dynamics of bone formation in defects exposed to rhTGF-β1. J. Bone Miner. Res. 1993; 8: 753–761
   PubMed Web of Science ®Google Scholar
• Bentz H., Nathan R. M., Rosen D., Armstrong R. M., Thompson A. Y., Segarini P. R., Mathews M. C., Dasch J. R., Piez K. A., Seyedin S. M. Purification and characterization of an unique osteoinductive factor from bovine bone. J. Biol. Chem. 1989; 264: 20805–20810
   PubMed Web of Science ®Google Scholar
• Bentz H., Thompson A., Armstrong R., Chang R.-J., Piez K. A., 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 1991; 11: 269–275
   PubMedGoogle Scholar
• Carrington J. L., Roberts A. B., Flanders K. C., Roche N. S., Reddi A. H. Accumulation, localization, and compartmentation of transforming growth factor β during endochondral bone development. J. Cell Biol. 1988; 107: 1969–1975
   PubMed Web of Science ®Google Scholar
• Cassiede P., Dennis J. E., Ma F., Caplan A. I. Osteochondrogenic potential of marrow mesenchymal progenitor cells exposed to TGF-β1 or PDGF-BB as assayed in vivo and in vitro. J. Bone Miner. Res. 1996; 11: 1264–1273
   PubMed Web of Science ®Google Scholar
• Celeste A. J., Iannazzi J. M., Taylor J. A., Hewick R. M., Rosen V., Wang E. A., Wozney J. M. Identification of transforming growth factor ß family members present in bone-inductive protein purified from bovine bone. Proc. Natl. Acad. Sci. USA 1990; 87: 9843–9847
   PubMed Web of Science ®Google Scholar
• Centrella M., Horowitz M., Wozney J. M., McCarthy T. L. Transforming growth factor β (TGF-β) family members and bone. Endocrine Rev. 1994; 15: 27–39
   PubMed Web of Science ®Google Scholar
• Centrella M., Casinghino S., Kim J., Pham T., Rosen V., Wozney J., 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. 1995; 15: 3273–3281
   PubMed Web of Science ®Google Scholar
• Derynk R., Janet J. A., Chen E. Y., Eaton E. H., Bell J. R., Assoian R. K., Roberts A. B., Sporn M. B., Goeddel D. V. Human transforming growth factor-ß complementary DNA sequence and expression in normal and trans-formed cells. Nature (Lond.) 1985; 316: 701–705
   PubMed Web of Science ®Google Scholar
• Hammonds R. G., Schwall R., Dudley A., Berkemeier L., Lai C., Lee J., Cunningham N., Reddi A. H., Wood W. I., Mason A. J. Bone inducing activity of mature BMP-2b produced from a hybrid BMP-2a/2b precursor. Mol. Endocrinol. 1991; 5: 149–155
   PubMedGoogle Scholar
• Helder M. N., Özkaynak E., Sampath T. K., Luyten F. P., Latin V., Oppermann H., Vukicevic S. Expression pattern of osteogenic protein-1 (bone morphogenetic protein-7) in human and mouse development. J. Histochem. Cytochem. 1995; 43: 1035–1044
   PubMed Web of Science ®Google Scholar
• Hostikka S. L., Tryggvason K. The complete primary structure of the alpha 2 chain of human type IV collagen and comparison with the alpha 1 (IV) chain. J. Biol. Chem. 1988; 263: 19488–19493
   PubMed Web of Science ®Google Scholar
• Hotten G. C., Matsumoto T., Kimura M., Bechtold R. F., Kron R., Ohara T., Tanaka H., Satoh Y., Okazaki M., Shirai T., Pan H., Kawai S., Pohl J. S., Kudo A. Recombinant human growth/differentiation factor 5 stimulates mesenchyme aggregation and chondrogenesis responsible for the skeletal development of limbs. Growth Factors 1996; 13: 65–74
   PubMed Web of Science ®Google Scholar
• Joyce M. E., Roberts A. B., Spom M. B., Bolander M. E. Transforming growth factor-β and the initiation of chondrogenesis and osteogenesis in the rat femur. J. Cell Biol. 1990; 110: 2195–2207
   PubMed Web of Science ®Google Scholar
• Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.) 1970; 227: 680–685
   PubMed Web of Science ®Google Scholar
• Leary J. J., Brigati D. J., Ward D. C. Rapid and sensitive colorimetric method for visualizing biotin-labeled DNA probes hybridized to DNA or RNA immobilized on nitrocellulose: Bio-blots. Proc. Natl. Acad. Sci. USA 1983; 80: 4045–4049
   PubMed Web of Science ®Google Scholar
• Liu F., Ventura F., Doody J., Massagué J. Human type II receptor for bone morphogenetic proteins (BMPs): Extension of the two-kinase receptor model to the BMPs. Mol. Cell. Biol. 1995; 15: 3479–3486
   PubMed Web of Science ®Google Scholar
• Lowry O. H., Rosebrough N. J., Fan A. L. Protein measurement with the folin phenol reagent. J. Biol. Chem. 1951; 193: 265–275
   PubMed Web of Science ®Google Scholar
• Luyten F. P., Cunningham N. S., Ma S., Muthukumaran N., Hammonds R. G., Nevins W. B., Wood W. I., Reddi A. H. Purification and partial amino acid sequence of osteogenin, a protein initiating bone differentiation. J. Biol. Chem. 1989; 264: 13377–13380
   PubMed Web of Science ®Google Scholar
• Nemeth G. G., Heydemann A., Bolander M. E. Isolation and analysis of ribonucleic acids from skeletal tissues. Anal. Biochem. 1989; 183: 301–304
   Google Scholar
• Noda M., Camilliere J. J. In vivo stimulation of bone formation by transforming growth factor-β. Endocrinology 1989; 124: 2991–2994
   PubMed Web of Science ®Google Scholar
• Özkaynak E., Rueger D. C., Drier E. A., Corbett C., Ridge R. J., Sampath T. K., Oppermann H. OP-1 cDNA encodes an osteogenic protein in the TGF-β family. EMBO (Eur. Mol. Biol. Organ.) J. 1990; 9: 2085–2093
   PubMed Web of Science ®Google Scholar
• Özkaynak E., Schnegelsberg P. N. J., Oppermann H. Murine osteogenic protein (OP-1): High levels of mRNA in kidney. Biochem. Biophys. Res. Commun. 1991; 179: 116–123
   PubMed Web of Science ®Google Scholar
• Özkaynak E., Schnegelsberg P. N. J., Jin D. F., Clifford G. M., Warren F. D., Drier E. A., Oppermann H. Osteogenic protein-2. A new member of the transforming growth factor-ß superfamily expressed early in embryogenesis. J. Biol. Chem. 1992; 267: 25220–25227
   PubMed Web of Science ®Google Scholar
• Parfitt A. M. Stereologic basis of bone histomorphometry; theory of quantitative microscopy and reconstruction of the third dimension. Bone histomorphometry: techniques and interpretation, R. R. Recker. CRC Press, Boca Raton 1983; 53–87
   Google Scholar
• Parfitt A. M., Drezner M. K., Glorieux F. H., Kanis J. A., Malluche H., Meunier P. J., Ott S. M., Recker R. R. Bone histomorphometry: Standardization of nomenclature, symbols, and units. J. Bone Miner. Res. 1987; 2: 595–610
   PubMed Web of Science ®Google Scholar
• Reddi A. H., Huggins C. B. Biochemical sequences in the transformation of normal fibroblasts in adolescent rats. Proc. Natl. Acad. Sci. USA 1972; 69: 1601–1605
   PubMed Web of Science ®Google Scholar
• Reddi A. H. Bone and cartilage differentiation. Curr. Opin. Genet. Dev. 1994; 4: 737–744
   PubMed Web of Science ®Google Scholar
• Reddi A. H. Bone morphogenetic proteins: An unconventional approach to isolation of first mammalian morphogens. Cytokine Growth Factor Rev. 1997; 8: 11–20
   PubMedGoogle Scholar
• Ripamonti U. Bone induction in nonhuman primates. An experimental study on the baboon (Papio ursinus). Clin. Orthop. 1991; 269: 284–294
   Google Scholar
• Ripamonti U., Magan A., van den Heever B., Moehl T., Reddi A. H. Xenogeneic osteogenin, a bone morphogenetic protein, and demineralized bone matrices, including human, induce bone differentiation in athymic rats and baboons. Matrix 1991; 11: 404–411
   PubMedGoogle Scholar
• Ripamonti U., Ma S., Cunningham N., Yeates L., Reddi A. H. Initiation of bone regeneration in adult baboons by osteogenin, a bone morphogenetic protein. Matrix 1992; 12: 369–380
   PubMedGoogle Scholar
• Ripamonti U., van den Heever B., Sampath T. K., Tucker M. M., Rueger D. C., Reddi A. H. Complete regeneration of bone in the baboon by recombinant human osteogenic protein-1 (hOP-1, bone morphogenetic protein-7). Growth Factors 1996a; 13: 273–289
   PubMed Web of Science ®Google Scholar
• Ripamonti U., Bosch C., van den Heever B., Duneas N., Melsen B., Ebner R. Limited chondro-osteogenesis by recombinant human transforming growth factor-β1 in calvarial defects of adult baboons (Papio ursinus). J. Bone Miner. Res. 1996b; 11: 938–945
   PubMed Web of Science ®Google Scholar
• Ripamonti U., Duneas N., van den Heever B., Bosch C., 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. 1997; 12: 1584–1595
   PubMed Web of Science ®Google Scholar
• Roberts A. B., Sporn M. B., Assoian R. K., Smith J. M., Roche N. S., Wakefield L. M., Heine U. I., Liotta L. A., Falanga V., Kehrl J. H., Fauci A. S. Transforming growth factor type ß: Rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc. Natl. Acad. Sci. USA 1986; 83: 4167–4171
   PubMed Web of Science ®Google Scholar
• Robey P. G., Young M. F., Flanders K. C., Roche N. S., Kondaiah P., Reddi A. H., Termine J. D., Sporn M. B., Roberts A. B. Osteoblasts synthetize and respond to TGF-β in vitro. J. Cell Biol. 1987; 105: 457–463
   PubMed Web of Science ®Google Scholar
• Rosenzweig B. L., Imanura T., Okadome T., Cox G. N., Yamashita H., ten Dijke P., Heldin C.-H., Miyazono K. Cloning and characterization of a human type 11 receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 1995; 92: 7632–7636
   PubMed Web of Science ®Google Scholar
• Sampath T. K., Reddi A. H. Dissociative extraction and reconstitution of extracellular matrix components involved in local bone differentiation. Proc. Natl. Acad. Sci. USA 1981; 78: 7599–7603
   PubMed Web of Science ®Google Scholar
• Sampath T. K., Muthukumaran N., Reddi A. H. Isolation of osteogenin, an extracellular matrix-associated bone-inductive protein, by heparin affinity chromatography. Proc. Natl. Acad. Sci. USA 1987; 84: 7109–7113
   PubMed Web of Science ®Google Scholar
• Sampath T. K., Maliakal J. C., Hauschka P. V., Jones W. K., Sasak H., Tucker R. F., White H. K., Coughlin J. E., Tucker M. M., Pang R. H. L., Corbett C., Özkaynak E., Oppermann H., Rueger D. C. 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. 1992; 267: 20352–20362
   PubMed Web of Science ®Google Scholar
• Sampath T. K., Rashka K. E., Doctor J. S., Tucker R. F., Hoffmann F. M. Drosophila TGF-ß superfamily proteins induce endochondral bone formation in mammals. Proc. Natl. Acad. Sci. USA 1993; 90: 6004–6008
   PubMed Web of Science ®Google Scholar
• Schnitzler C. M., Ripamonti U., Mesquita J. M. Histomorphometry of iliac crest trabecular bone in adult male baboons in captivity. Calcif. Tiss. Int. 1993; 52: 447–454
   Google Scholar
• Statistical Analysis System. SAS/STATS User's Guide, Version 6, 4th ed. Sas Institute Inc., Cary, NC 1989; 2: 891–996
   Google Scholar
• Sumner D. R., Turner T. M., Purchio A. F., Gombotz W. R., Urban R. M., Galante J. O. Enhancement of bone ingrowth by transforming growth factor-β. J. Bone Joint Surg. 1995; 77-A: 1135–1147
   Google Scholar
• ten Dijke P., Yamashita H., Sampath T. K., Reddi A. H., Estevez M., Riddle D. L., Ichijo H., Heldin C.-H., Miyazono K. Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem. 1994; 269: 16985–16988
   PubMed Web of Science ®Google Scholar
• Urist M. R. Bone: Formation by autoinduction. Science (Wash. DC) 1965; 159: 893–899
   Google Scholar
• Urist M. R., DeLange R. J., Finerman G. A. Bone cell differentiation and growth factors. Science (Wash. DC) 1983; 220: 680–686
   PubMed Web of Science ®Google Scholar
• Vukicevic S., Latin V., Chen P., Batorsky R., Reddi A. H., Sampath T. K. Localization of osteogenic protein-1, a bone morphogenetic protein, during human embryonic development. Biochem. Biophys. Res. Commun. 1994a; 198: 693–700
   PubMed Web of Science ®Google Scholar
• Vukicevic S., Helder M. N., Luyten F. P. Developing human lung and kidney are major sites for synthesis of bone morphogenetic protein-3 (osteogenin). J. Histochem. Cytochem. 1994b; 42: 869–875
   PubMed Web of Science ®Google Scholar
• Wang E. A., Rosen V., D'Alessandro J. S., Bauduy 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., Wozney J. M. Recombinant human bone morphogenetic protein induces bone formation. Proc. Natl. Acad. Sci. USA 1990; 87: 2220–2224
   PubMed Web of Science ®Google Scholar
• Wozney J. M., Rosen V., Celeste A. J., Mitsock L. M., Whitters M. J., Kriz R. W., Hewick R. M., Wang E. A. Novel regulators of bone formation: Molecular clones and activities. Science (Wash. DC) 1988; 242: 1528–1534
   PubMed Web of Science ®Google Scholar
• Wozney J. M. The bone morphogenetic protein family and osteogenesis. Malec. Reprod. Dev. 1992; 32: 160–167
   PubMed Web of Science ®Google Scholar