Transforming growth factor-β gene family members and bone

Endocrine Reviews

Volumn 15, Issue 1, 1994, Pages 27-39

  Centrella, Michael ^a   Horowitz, Mark C ^b   Wozney, John M ^c   Mccarthy, Thomas L ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

BINDING SITE; BONE CELL; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL DIVISION; GENE EXPRESSION REGULATION; HORMONE ACTION; HORMONE SYNTHESIS; IN SITU HYBRIDIZATION; MULTIGENE FAMILY; NORTHERN BLOTTING; OSTEOLYSIS; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION;

ACTIVINS; ANIMALS; BONE AND BONES; BONE RESORPTION; CARRIER PROTEINS; HUMANS; INHIBINS; OSTEOGENESIS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 85003186936     PISSN: 0163769X     EISSN: None     Source Type: Journal    
DOI: 10.1210/er.15.1.27     Document Type: Review

References (127)

1. Roberts AB, Sporn MB 1990 Transforming growth factor betas. In: Sporn MB, Roberts AB (eds) Peptide Growth Factors and Their Receptors. Springer-Verlag, Heidelberg, Germany, pp 419-472
2. Centrella M, McCarthy TL, Canalis E 1991 Current concepts review: transforming growth factor beta and remodeling of bone. J Bone Joint Surg 73A:1418-1428
3. Ying S-Y 1988 Inhibins, activins and follistatins: gonadal proteins modulating the secretion of follicle stimulating hormone. Endocr Rev 9:267-293
4. Rosen V, Thies RS 1992 The BMP proteins in bone formation and repair. Trends Genet 8:97-102
5. Derynck R 1994 Transforming growth factor β. In: Thompson A (ed) The Cytokine Handbook, ed 2. Academic Press, Inc, New York, in press
6. Massague J 1992 Receptors for the TGF-β family. Cell 69: 1067-1070
7. Ogawa Y, Schmidt DK, Dasch JR, Chang R-J, Glaser CB 1992 Purification and characterization of transforming growth factor-β2.3 and β1.2 heterodimers from bovine bone. J Biol Chem 267:2325-2328
8. Schmid P, Cox D, Bube G, Maier R, McMaster GK 1991 Differential expression of TGF β1, β2 and β3 genes during mouse embryogenesis. Development 111:117-130
9. Millan FA, Denhez F, Kondaiah P, Akhurst RJ 1991 Embryonic gene expression of TGF β1, β2 and β3 suggest different developmental functions in vivo. Development 111:131-144
10. Heine UI, Munoz EF, Flanders KC, Ellingsworth LR, Lam H-Y, Thompson NL, Roberts AB, Sporn MB 1987 Role of transforming growth factor-β in the development of the mouse embryo. J Cell Biol 105:2861-2876
11. Gatherer D, tenDijke P, Baird DT, Akhurst RJ 1990 Expression of TGF-β isoforms during first trimester human embryogenesis. Development 110:445-460
12. Thorp BH, Anderson I, Jakowlew SB 1992 Transforming growth factor-β1, -β2 and -β3 in cartilage and bone cells during endochondral ossification in the chick. Development 114:907-911
13. Bascom C, Wolfshohl JR, Coffey Jr RJ, Madisen L, Webb NR, Purchio AR, Derynck R, Moses HL 1989 Complex regulation of transforming growth factor β1, β2, and β3 mRNA expression in mouse fibroblasts and keratinocytes by transforming growth factors β1 and β2. Mol Cell Biol 9:5508-5515
14. Roberts AB, Kim SJ, Noma T, Glick AB, Lafyatis R, Lechleider R, Jakowlew SB, Geiser A, O'Reilly MA, Danielpour D, Sporn MB 1991 Multiple forms of TGF-β: distinct promoters and differential expression. Ciba Found Symp 157:7-15
15. Bonewald LF, Wakefield L, Oreffo ROC, Escobedo A, Twsrdzik DR, Mundy GR 1991 Latent forms of transforming growth factor-β (TGFβ) derived from bone cultures: identification of a naturally occurring 100-kDa complex with similarity to recombinant latent TGFβ. Mol Endocrinol 5:741-751
16. Allan EH, Zeheb R, Gelehter TD, Heaton JH, Fukumoto S, Yee JA, Martin TJ 1991 Transforming growth factor beta inhibits plasminogen activator (PA) activity and stimulates production of urokinase-type PA, PA inhibitor-1 mRNA, and protein in rat osteoblast-like cells. J Cell Physiol 149:34-43
17. Baron R, Neff L, Louvard I, Courtoy PJ 1985 Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kd lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 101:2210-2222
18. Oreffo RO, Mundy GR, Seyedin SM, Bonewald LF 1989 Activation of the latent bone derived TGF beta complex by isolated osteoclasts. Biochem Biophys Res Commun 158:817-823
19. Wrana JL, Attisano L, Carcamo J, Zentella A, Doody J, Laiho M, Wang X-F, Massague J 1992 TGFβ signals through a heteromeric protein kinase receptor complex. Cell 71:1003-1014
20. Chen R-H, Ebner R, Derynck R 1993 Inactivation of the type II receptor reveals two receptor pathways for the diverse TGF-β activities. Science 260:1335-1338
21. Ebner R, Chen R-H, Shum L, Lawler S, Zioncheck TF, Lee A, Lopez AR, Derynck R 1993 Cloning of a type I TGF-β receptor and its effect on TGF-β binding to the type II receptor. Science 260:1344-1348
22. Lopez-Casillas F, Wrana JL, Massague J 1993 Betaglycan presents ligand to the TGF-β signaling receptor. Cell 73:1435-1444
23. Andres JL, Stanley K, Cheifetz S, Massague J 1989 Membrane-anchored and soluble forms of betaglycan, a polymorphic proteoglycan that binds transforming growth factor-β. J Cell Biol 109:3137-3145
24. Centrella M, McCarthy TL, Canalis E 1991 Activin-A binding and biochemical effects in osteoblast-enriched cultures from fetal rat parietal bone. Mol Cell Biol 11:250-258
25. Paralkar VM, Hammonds RG, Reddi AH 1991 Identification and characterization of cellular binding proteins (receptors) for recombinant human bone morphogenetic protein 2B, an initiator of bone differentiation cascade. Proc Natl Acad Sci USA 88:3397-3401
26. Mathews LS, Vale WW 1991 Expression cloning of an activin receptor, a predicted transmembrane kinase. Cell 65:973-982
27. Attisano L, Wrana JL, Cheifetz S, Massague J 1992 Novel activin receptors: distinct genes and alternate mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68:97-108
28. Ichijo H, Ronnstrand L, Miyagawa K, Ohashi H, Heldin CH, Miyazono K 1991 Purification of transforming growth factor-β 1 binding proteins from porcine uterus membranes. J Biol Chem 266:22459-22464
29. Mitchell EJ, Lee K, O'Connor-McCourt MD 1992 Characterization of transforming growth factor-β (TGF-β) receptors on BeWo choriocarcinoma cells including the identification of a novel 38-kDa TGF-beta binding glycoprotein. Mol Biol Cell 3:1295-1307
30. Centrella M, McCarthy TL, Canalis E 1988 Parathyroid hormone modulates transforming growth factor β activity and binding in osteoblastic cells. Proc Natl Acad Sci USA 85:5889-5893
31. Massague J 1985 Subunit structure of a high-affinity receptor for type β-transforming growth factor. J Biol Chem 260:7059-7066
32. Centrella M 1993 Growth factor receptors and responses: comparison between normal and osteosarcoma-derived cell cultures. In: Novak JF, McMaster JH (eds) Frontiers in Osteosarcoma Research. Hogrefe and Huber, Seattle, WA, pp 457-468
33. Centrella M, Wozney J, McCarthy TL 1993 Differential regulation of transforming growth factor β (TGF-β) binding site expression on bone cells by bone morphogenetic protein (BMP-2), cortisol, and TGF-β1. J Bone Miner Res 8:5294 (Abstract)
34. Lin HY, Lodish HF 1993 Receptors for the TGF-β superfamily: multiple polypeptides and serine/threonine kinases. Trends Cell Biol 3:14-19
35. O'Grady P, Liu Q, Huang SS, Huang JS 1992 Transforming growth factor β (TGF-β) type V receptor has a TGF-β stimulated serine/threonine-specific autophosphorylation activity. J Biol Chem 267:21033-21037
36. Graycar JL, Miller DA, Arrcik BA, Lyons RM, Moses HL, Derynck R 1989 Human transforming growth factor β3: recombinant expression, purification, and biological activities in comparison with transforming growth factors β1 and β2. Mol Endocrinol 3:1977-1986
37. tenDijke P, Iwata KK, Goddard C, Pieler C, Canalis E, McCarthy TL, Centrella M 1990 Recombinant transforming growth factor type β3: biological activities and receptor binding properties in isolated bone cells. Mol Cell Biol 10:4473-4479
38. 2+ channel that is regulated by TGF-β. Science 257:91-94
39. Rizzino A 1987 Appearance of high affinity receptors for type β transforming growth factor during differentiation of murine embryonal carcinoma cells. Cancer Res 47:4386-4390
40. Ewton DZ, Spizz G, Olson EN, Florini JR 1988 Decrease in transforming growth factor-β binding and action during differentiation in muscle cells. J Biol Chem 263:4029-4032
41. Kypriaou N, Isaacs J 1988 Identification of a cellular receptor for transforming growth factor-β in rat ventral prostate and its negative regulation by androgens. Endocrinology 123:2124-2131
42. Cochet C, Feige JJ, Chambaz EM 1988 Bovine adrenocortical cells exhibit high affinity transforming growth factor-β receptors which are regulated by adrenocorticotropin. J Biol Chem 263:5707-5713
43. Gruppuso PA 1989 Expression of hepatic transforming growth factor receptors during late gestation in the fetal rat. Endocrinology 125:3037-3043
44. Hu J-S, Olson EN 1990 Functional receptors for transforming growth factor-β are retained by biochemically differentiated C2 myocytes in growth factor deficient medium containing EGTA, but down-regulated during terminal differentiation. J Biol Chem 265:7914-7919
45. Centrella M, McCarthy TL, Canalis E 1991 Glucocorticoid regulation of transforming growth factor β1 (TGF-β1) activity and binding in osteoblast-enriched cultures from fetal rat bone. Mol Cell Biol 11:4490-4496
46. Gazit D, Ebner R, Kahn AJ, Derynck R 1993 Modulation of expression and cell surface binding of members of the transforming growth factor-β superfamily during retinoic acid-indcued osteoblastic differentiation of multipotential mesenchymal cells. Mol Endocrinol 7:189-198
47. Mulder KM, Segarini PR, Morris SL, Ziman JM, Choi HG 1993 Role of receptor complexes in resistance or sensitivity to growth inhibition by TGF-β in intestinal epithelial cell clones. J Cell Physiol 154:2-174
48. Dennis PA, Rifkin DB 1991 Cellular activation of latent transforming growth factor β requires binding to the cation-independent mannose-6-phosphate/insulin-like growth factor type II receptor. Proc Natl Acad Sci USA 88:580-584
49. Czech MP 1989 Signal transmission by the insulin-like growth factors. Cell 59:235-238
50. Wakefield LM, Smith DM, Flanders KC, Sporn MB 1988 Latent transforming growth factor-β from human platelets: a high molecular weight complex containing precursor sequences. J Biol Chem 263:7646-7654
51. Huang SS, O'Grady P, Huang JS 1988 Human transforming growth factor β:α2-macroglobulin complex is a latent form of transforming growth factor β. J Biol Chem 263:1535-1541
52. Lomri A, Marie PJ 1990 Bone cell responsiveness to transforming growth factor β, parathyroid hormone, and prostaglandin E2 in normal and postmenopausal osteoporotic women. J Bone Miner Res 5:1149-1155
53. Kells AF, Shwartz HS, Bascom CC, Hoover RL 1992 Identification and analysis of transforming growth factor β receptors on primary osteoblast-enriched cultures derived from adult human bone. Connect Tissue Res 27:197-209
54. 2O2 in normal mouse osteoblastic cells (MC3T3-E1), but not in their ras-transformants. Biochem Biophys Res Commun 187:1418-1425
55. Hunter T, Pines J 1991 Cyclins and cancer. Cell 66:1071-1074
56. Koff A, Ohtsuki M, Polyak K, Roberts JM, Massague J 1993 Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-β. Science 260:536-539
57. Burmester JK, Qian SW, Roberts AB, Huang A, Amatayakul-Chantler S, Suardet L, Odartchenko N, Madri JA, Sporn MB 1993 Characterization of distinct functional domains of transforming growth factor β. Proc Natl Acad Sci USA 90:8628-8632
58. Centrella M, Casinghino S, Ignotz R, McCarthy TL 1992 Multiple regulatory effects by transforming growth factor type β (TGF-β1) on type I collagen levels in osteoblast-enriched cultures from fetal rat bone. Endocrinology 131:2863-2872
59. Strong DD, Beachler AL, Wergedal JE, Linkhart TA 1991 Insulin-like growth factor II and transforming growth factor β regulate collagen expression in human osteoblastlike cells in vitro. J Bone Miner Res 6:15-23
60. Wrana JL, Kubota T, Zhang Q, Overall CM, Aubin JE, Butler WT, Sodek J 1991 Regulation of transformation-sensitive secreted protein (SSPI/osteopontin) expression by transforming growth factor-β. Comparisons with expression of SPARC (secreted acidic cysteine-rich protein). Biochem J 273:523-531
61. 3. Metabolism 41:42-48
62. Bonewald LF, Kester MB, Schwartz Z, Swain LD, Khare A, Johnson TL, Leach RJ, Boyan BD 1992 Effects of combining transforming growth factor β and 1,25-dihydroxyvitamin D3 on differentiation of human osteosarcoma (MG-63). J Biol Chem 267:8943-8949
63. Centrella M, McCarthy TL, Kusmik WF, Canalis E 1992 Isoform specific regulation of platelet-derived growth factor activity and binding in osteoblast-enriched cultures from fetal rat bone. J Clin Invest 89:1076-1084
64. Rydziel S, Ladd C, McCarthy TL, Centrella M, Canalis E 1992 Determination and expression of platelet-derived growth factor AA in bone cell cultures. Endocrinology 130:1916-1922
65. Ber R, Kubota T, Sodek J, Aubin JE 1991 Effects of transforming growth factor-β on normal clonal bone cell populations. Biochem Cell Biol 69:132-140
66. Takigawa M, Kinoshita A, Enomoto M, Asada A, Sozuki F 1991 Effects of various growth and differentiation factors on expression of parathyroid hormone receptors on rabbit costal chondrocytes in culture. Endocrinology 129:868-876
67. Seitz PK, Zhu BT, Cooper CW 1992 Effects of transforming growth factor beta on parathyroid hormone receptor binding and cAMP formation in rat osteosarcoma cells. J Bone Miner Res 7: 541-546
68. Schneider H-G, Michelangeli VP, Frampton RJ, Grogan JL, Ikeda K, Martin TJ, Findlay DM 1992 Transforming growth factor-β modulates receptor binding of calciotropic hormones and G protein-mediated adenylate cyclase responses in osteoblast-like cells. Endocrinology 131:1383-1389
69. Hughes FJ, Aubin JE, Heershe JN 1992 Differential chemotactic responses of different populations of fetal rat calvarial cells to platelet-derived growth factor and transforming growth factor β. Bone Mineral 19:63-74
70. Hiyamizu TF, Sessions SK, Wanel N, Bryant SV 1991 Effects of localized application of transforming growth factor β 1 on developing chick limbs. Dev Biol 145:164-173
71. Yamaguchi Y, Mann DM, Ruoshlati E 1990 Negative regulation of transforming growth factor-β by the proteoglycan decorin. Nature 346:281-284
72. Centrella M, McCarthy TL, Rosenberg LC, Regulation of cell growth and transforming growth factor β (TGF-β) responsiveness by proteoglycans in osteoblast-enriched cultures from fetal rat bone. Program of the Fifth International Congress on Cell Biology, Madrid, Spain, 1992
73. Raisz LG 1992 Mechanisms and regulation of bone resorption by osteoclastic cells. In: Coe FL, Fauvus MJ (eds) Disorders of Bone and Mineral Metabolism. Raven Press Ltd, New York, pp 287-311
74. Metcalf D 1989 The molecular control of cell division, differentiation commitment and maturation in haemopoietic cells. Nature 339:27-30
75. Horowitz M, Brown M, Insogna K, Coleman D, Centrella M, Phillips J, Weir E 1990 PTHrp and PTH induce the secretion of IL-6 by a clonal osteosarcoma cell line. In: Powanda MC, Oppenheim JJ, Kluger MJ, Dinarello CA, (eds) Molecular and Cellular Biology of Cytokines. Alan R Liss Inc, New York, pp 471-476
76. Horowitz M, Phillips J, Centrella M 1992 TGF-β regulates IL-6 secretion by osteoblasts. In: Cohn DV, Gennari C, Tashjian Jr AH (eds) Calcium Regulating Hormones and Bone Metabolism: Basic and Clinical Aspects. Elsevier Science Publishers, Amsterdam, pp 275-280
77. Marusic A, Kalinowski JF, Harrison JR, Centrella M, Raisz LG, Lorenzo JA 1991 Effects of transforming growth factor β and interleukin 1α on prostaglandin synthesis in serum-deprived osteoblastic cells. J Immunol 146:2633-2638
78. Shinar DM, Rodan GA 1990 Biphasic effects of transforming growth factor-β on the production of osteoclast-like cells in mouse bone marrow cultures: the role of prostaglandins in the generation of these cells. Endocrinology 126:3153-3158
79. Hattersley G, Chambers TJ 1991 Effects of transforming growth factor β1 on the regulation of osteoclastic development and function. J Bone Miner Res 6:165-172
80. Ruscetti FW, Dubois C, Falk LA, Jacobsen SE, Sing G, Longo DL, Wiltrout RH, Keller JR 1991 In vivo and in vitro effects of TGF-β1 on normal and neoplastic haemopoiesis. Ciba Found Symp 157:212-227
81. Petkovich PM, Wrana JL, Grigoriadis AE, Heersche JNM, Sodek J 1988 1,25-Dihydroxyvitamin D3 increases epidermal growth factor receptors and transforming growth factor β-like activity in a bone-derived cell line. J Biol Chem 2:13424-13428
82. Finkelman RD, Linkhart TA, Mohan S Lau KH, Baylink DJ, Bell NH 1991 Vitamin D deficiency causes a selective reduction in deposition of transforming growth factor β in rat bone: possible mechanism for impaired osteoinduction. Proc Natl Acad Sci USA 88:3657-3660
83. Komm BS, Terpening CM, Benz DJ, Graeme KA, Gallegos A, Korc M, Greene GL, O'Malley BW, Haussler MR 1988 Estrogen binding receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science 241:81-84
84. Oursler MJ, Cortese C, Keeling P, Anderson MA, Bonde SK, Riggs BL, Speisberg TC 1991 Modulation of transforming growth factor-β production in normal human osteoblast-like cells by 17 β-estradiol and parathyroid hormone. Endocrinology 129:3313-3320
85. Finkelman RD, Bell NH, Strong DD, Demers LM, Baylink DJ 1992 Ovariectomy selectively reduces the concentration of transforming growth factor β in rat bone: implications for estrogen deficiency-associated bone loss. Proc Natl Acad Sci USA 89: 12190-12193
86. Benz DJ, Haussler MR, Thomas MA, Speelman B, Komm BS 1991 High affinity androgen binding and androgenic regulation of α1(I)-procollagen and transforming growth factor-β steady state messenger ribonucleic acid levels in human osteoblast-like osteosarcoma cells. Endocrinology 128:2723-2730
87. Yang NN, Hardikar S, Kim J, Sato M 1993 Ralixofene, and "anti-estrogen", stimulates the effects of estrogen on inhibiting bone resorption through regulating TGF-β3 expression in bone. J Bone Miner Res 8:5118 (abstract)
88. Heath JK, Rodan SB, Yoon K, Rodan GA 1989 Rat calvarial cell lines immortalized with SV-40 large T antigen: constitutive and retinoic acid-inducible expression of osteoblastic features. Endocrinology 124:3060-3068
89. A chain. Proc Natl Acad Sci USA 85: 2434-2438
90. Thomsen G, Woolf T, Whitman M, Sokol S, Vaughan J, Vale W, Melton DA 1990 Activins are expressed early in Xenopus embryogenesis and can induce axial mesodem and anterior structures. Cell 63:485-493
91. Mitrani E, Ziv T, Thomsen G, Shimoni Y, Melton DA, Bril A 1990 Activin can induce the formation of axial structures and is expressed in the hypoblast of the chick. Cell 63:495-501
92. Roberts VJ, Sawchenko PE, Vale W 1991 Expression of inhibin/ activin subunit messenger ribonucleic acids during rat embryogenesis. Endocrinology 128:3122-3129
93. Ogawa Y, Schmidt DK, Nathan RM, Armstrong RM, Miller KL, Sawamura SJ, Ziman JM, Erickson KL, deLeon ER, Rosen DM, Seyedin SM, Glaser CB, Chang R-J, Corrigan AZ, Vale WW 1992 Bovine bone activin enhances bone morphogenetic protein-induced ectopic bone formation. J Biol Chem 267:14233-14237
94. Hashimoto M, Shoda A, Inoue S, Yamada R, Kondo T, Sakurai T, Ueno N, Muratmatsu M 1992 Functional regulation of osteoblastic cells by the interaction of activin-A with follistatin. J Biol Chem 267:4999-5004
95. Celeste AJ, Ianazzi JA, Taylor RC, Hewick RM, Rosen V, Wang EA, Wozney JM 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
96. Sampath TK, Coughlin JE, Whetstone RM, Banach D, Corbett C, Ridge RJ, Ozkaynak E, Oppermann H, Rueger DC 1990 Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-β superfamily. J Biol Chem 265:13198-13205
97. Yamaguchi A, Katagiri T, Ikeda T, Wozney JM, Rosen V, Wang EA, Kahn AJ, Suda T, Yoshiki S 1991 recombinant human bone morphogenetic protein-2 stimulates osteoblastic maturation and inhibits myogenic differentiation in vitro. J Cell Biol 113:681-687
98. Hiraki Y, Inoue H, Shigeno C, Sanma Y, Bentz H, Rosen DM, Asada A, 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
99. Chen TL, Bates RL, Dudley A, Hammonds RG Jr Amento EP 1991 Bone morphogenetic protein-2b stimulation of growth and osteogenic phenotypes in rat osteoblast-like cells: comparison with TGF-β1. J Bone Miner Res 6:1387-1393
100. Thies RS, Bauduy M, Ashton BA, Kurtzberg L, Wozney JM, Rosen V 1992 Recombinant human bone morphogenetic protein-2 induces osteoblastic differentiation in W-20-17 stromal cells. Endocrinology 130:1318-1324
101. Carrington JL, Reddi AH 1990 Temporal changes in the response of chick limb bud mesodermal cells to transforming growth factor β-type 1. Exp Cell Res 186:368-373
102. Luyten FP, Yu YM, Yanagishita M, Vukicevic S, Hammonds RG, Reddi AH 1992 Natural bovine osteogenin and recombinant human bone morphogenetic protein-2B are equipotent in the maintenance of proteoglycans in bovine articular cartilage explant cultures. J Biol Chem 267:3691-3695
103. Carrington JL, Chen P, Yanagishita M, Reddi AH 1991 Osteogenin (bone morphogenetic protein-3) stimulates cartilage formation by chick limb bud cells in vitro. Dev Biol 146:406-415
104. Chen P, Carrington JL, Hammonds RG, Reddi AH 1991 Stimulation of chondrogenesis in limb bud mesoderm cells by recombinant bone morphogenetic protein 2B (BMP-2B) and modulation by transforming growth factor β1 and β2. Exp Cell Res 195: 509-515
105. Chen P, Carrington JL, Paralkar VM, Pierce GF, Reddi AH 1992 Chick limb bud mesodermal cell chondrogenesis: inhibition by isoforms of platelet-derived growth factor and reversal by recombinant bone morphogenetic protein. Exp Cell Res 200:110-117
106. Niswander L, Martin GR 1993 FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361:68-71
107. Kingsley DM, Bland AE, Grubber JM, Merker PC, Russell LB, Copeland NG, Jenkins NA 1992 The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGF β superfamily. Cell 71:399-410
108. Cunningham NS, Paralkar V, Reddi AH 1992 Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor β1 mRNA expression. Proc Natl Acad Sci USA 89:11740-11744
109. Kawaguchi H, Kurokawa T, Hoshino Y, Kawahara H, Ogata E, Matsumoto T 1992 Immunohistochemical demonstration of bone morphogenetic protein-2 and transforming growth factor-β in the ossification of the posterior longitudinal ligament of the cervical spine. Spine 17:533-36
110. Lyons CM, Lyons KM, Lapan PM, Wright CV, Hogan BL 1992 DVR-4 (bone morphogenetic protein-4) as a posterior ventralizing factor in Xenopus mesoderm induction. Development 115:639-647
111. Lyons KM, Jones CM, Hogan BL 1992 The TGF-β related DVR gene family in mammalian development. Ciba Found Symp 165:219-230
112. Wang EA, Rosen V, D'Allesandro JS, Bauduy M, Cordes P, Harada T, Israel DI, Hewick RM, Kerns KM, Lapan P, Luxenberg DP, McQuaid D, Moutsatsos DC, Nove J, Wozney JM 1990 Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220-2224
113. Bentz H, Thompson AY, Armstrong R, Chang R-J, Piez KA, Rosen DM 1991 Transforming growth factor-β2 enhances the osteo-inductive activity of a bovine bone-derived fraction containing bone morphogenetic protein-2 and 3. Matrix 11:269-275
114. Noda M, Camilliere JJ 1989 In vivo stimulation of bone formation by transforming growth factor-β. Endocrinology 124:2291-2294
115. Marcelli C, Yates AJ, Mundy GR 1990 In vivo effects of human recombinant transforming growth factor β on bone turnover in normal mice. J Bone Miner Res 5:1087-1096
116. Beck LS, Ammann AJ, Aufdemorte TB, Deguzman L, Xu Y, Lee WP, McFatridge LA, Chen TL 1991 In vivo induction of bone by recombinant human transforming growth factor β1. J Bone Miner Res 6:961-968
117. Yasko AW, Lane JM, Fellinger EJ, Rosen V, Wozney JM, Wang EA 1992 The healing of segmental bone defects, induced by recombinant human bone morphogenetic protein (rhBMP-2). J Bone Joint Surg 74-A:659-670
118. Johnson EE, Urist MR, Finerman GAM 1992 Resistant nonunions and partial or complete segmental defects of long bones. Treatment with implants of a composite of human bone morphogenetic protein (BMP) and autolyzed, antigen-extracted, allogeneic (AAA) bone. Clin Orthop 277:229-237
119. Ripamonti U, Ma S-S, Cunningham NS, Yeates L, Reddi AH 1993 Reconstruction of the bone-bone marrow organ by osteogenin, a bone morphogenetic protein, and demineralized bone matrix in calvarial defects of adult primates. Plast Reconstr Surg 91:27-36
120. Khouri RK, Koudsi B, Reddi H 1991 Tissue transformation into bone in vivo. A potential practical application. JAMA 266:1953-1955
121. Horisaka Y, Okamoto Y, Matsumoto N, Yoshimura Y, Kawada J, Yamashita K, Tomomichi T 1991 Subperiosteal implantation of bone morphogenetic protein adsorbed to hydroxyapatite. Clin Orthop 268:303-312
122. Ono I, Ohura T, Murata M, Yamaguchi H, Ohnuma Y, Kuboki Y 1992 A study on bone induction in hydroxyapatite combined with bone morphogenetic protein. Plast Reconstr Surg 90:870-879
123. Ripamonti U, Ma S-S, van den Heever B, Reddi AH 1992 Osteogenin, a bone morphogenetic protein, adsorbed on porous hydroxyapatite substrata, induces rapid bone differentiation in calvarial defects of adult primates. Plast Reconstr Surg 90:382-393
124. Sato T, Kawamura M, Sato K, Iwata H, Miura T 1991 Bone morphogenesis of rabbit bone morphogenetic protein bound hydroxyapatite-fibrin composite. Clin Orthop 263:254-262
125. Doll BA, Towle HJ, Hollinger JO, Reddi AH 1990 The osteogenic potential of two composite graft systems using osteogenin. J Periodont 61:745-750
126. Katoh T, Sato K, Kawamura M, Iwata H, Miura T 1993 Osteogenesis in scintered bone combined with bovine bone morphogenetic protein. Clin Orthop 287:266-275
127. Miyamota S, Takaoka K, Okada T, Yoshikawa H, Hashimoto J, Suzuki S, Ono K 1992 Evaluation of polylactic acid homopolymers as carriers for bone morphogenetic protein. Clin Orthop 278: 274-285