Convergence of the BMP and EGF signaling pathways on Smad1 in the regulation of chondrogenesis

International Journal of Developmental Biology

Volumn 43, Issue 8, 1999, Pages 795-807

  Nonaka, Kazuaki ^a   Shum, Lillian ^a   Takahashi, Ichiro ^a   Takahashi, Katsu ^a   Ikura, Tsuyoshi ^a   Dashner, Ralph ^a   Nuckolls, Glen H ^a   Slavkin, Harold C ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

Mandible; Micromass culture; Organ culture; Sox9; Type II collagen

Indexed keywords

ALCIAN BLUE; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR; COLLAGEN TYPE 2; EPIDERMAL GROWTH FACTOR; SMAD PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CHICKEN; CHONDROGENESIS; CONTROLLED STUDY; ECTOPIC TISSUE; EMBRYO; EMBRYO DEVELOPMENT; IMMUNOCYTOCHEMISTRY; MANDIBLE; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; CARTILAGE, ARTICULAR; CELL NUCLEUS; CHICK EMBRYO; CHONDROGENESIS; COLLAGEN; DNA PRIMERS; DNA-BINDING PROTEINS; EPIDERMAL GROWTH FACTOR; GENE EXPRESSION; HIGH MOBILITY GROUP PROTEINS; IN SITU HYBRIDIZATION; MANDIBLE; MICE; MOLECULAR SEQUENCE DATA; ORGAN CULTURE TECHNIQUES; RECEPTORS, CELL SURFACE; RECEPTORS, GROWTH FACTOR; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD1 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA; AVES; AVIAN RETROVIRUS; GALLUS GALLUS; UNIDENTIFIED RETROVIRUS;

EID: 0033374802     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (81)

1. ALONSO, S., MINTY, A., BOURLET, Y. and BUCKINGHAM, M. (1986). Comparison of three actin-coding sequences in the mouse: evolutionary relationships between the actin genes of warm-blooded vertebrates. J. Mol. Evol. 23: 11-22.
2. BARLOW, A.J. and FRANCIS-WEST, P.H. (1997). Ectopic application of recombinant BMP-2 and BMP-4 can change patterning of developing chick facial primordia. Development 124: 391-398.
3. BARLOW, A.J., BOGARDI, J.P., LADHER, R. and FRANCIS-WEST, P.H. (1999). Expression of chick Barx-1 and its differential regulation by FGF-8 and BMP signaling in the maxillary primordia. Dev. Dyn. 214: 291-302.
4. BENNETT, J.H., HUNT, P. and THOROGOOD, P. (1995). Bone morphogenetic protein-2 and -4 expression during murine orofacial development. Arch. Oral Biol. 40: 847-854.
5. BERNIER, S.M. and GOLTZMAN, D. (1992). Effect of protein and steroidal osteotropic agents on differentiation and epidermal growth factor-mediated growth of the CFK1 osseous cell line. J. Cell Physiol. 752: 317-327.
6. BI, W., DENG, J.M., ZHANG, A., BEHRINGER R.R. and DE CROMBRUGGHE, B. (1999). Sox9 is required for cartilage formation. Nature Genet. 22: 85-89.
7. BOONSTRA, J., RIJKEN, P., HUMBEL, B., CREMERS, F., VERKLEIJ, A. and VAN BERGEN EN HENEGOUWEN, P. (1995). The epidermal growth factor. Cell Biol. Int. 79: 413-430.
8. BUCKLAND, R.A., COLLINSON, J.M., GRAHAM, E., DAVIDSON, D.R. and HILL, R.E. (1998). Antagonistic effects of FGF4 on BMP induction of apoptosis and chondrogenesis in the chick limb bud. Mech. Dev. 71: 143-150.
9. COFFIN-COLLINS, P.A. and HALL, B.K. (1989). Chondrogenesis of mandibular mesenchyme from the embryonic chick is inhibited by mandibular epithelium and by epidermal growth factor. Int. J. Dev. Biol. 33: 297-311.
10. DANIELS, K. and SOLURSH, M. (1991). Modulation of chondrogenesis by the cytoskeleton and extracellular matrix. J. Cell Sci. 100: 249-254.
11. DEALY, C.N., SCRANTON, V. and CHENG, H.C. (1998). Roles of transforming growth factor-alpha and epidermal growth factor in chick limb development. Dev. Biol. 202: 43-55.
12. DERYNCK, R., ZHANG, Y. and FENG, X.H. (1998). Smads: transcriptional activators of TGF-beta responses. Cell 95: 737-740.
13. EKANAYAKE, S. and HALL, B.K. (1997). The in vivo and in vitro effects of bone morphogenetic protein-2 on the development of the chick mandible. Int. J. Dev. Biol. 47: 67-81.
14. FRANCIS-WEST, P.H., TATLA, T. and BRICKELL, P.M. (1994). Expression patterns of the bone morphogenetic protein genes Bmp-4 and Bmp-2 in the developing chick face suggest a role in outgrowth of the primordia. Dev. Dyn. 201: 168-178.
15. GANAN, Y., MACIAS, D., DUTERQUE-COQUILLAUD, M., ROS, M.A. and HURLÉ, J.M. (1996). Role of TGF beta s and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122: 2349-2357.
16. GANNON, F.H., KAPLAN, F.S., OLMSTED, E., FINKEL, G.G., ZASLOFF, M.A. and SHORE, E. (1997). Bone morphogenetic protein 2/4 in early fibromatous lesions of fibrodysplasia ossificans progressiva. Hum. Pathol. 28: 339-343.
17. GOSPODAROWICZ, D. and MESCHER, A.L. (1977). A comparison of the responses of cultured myoblasts and chondrocytes to fibroblast and epidermal growth factors. J. Cell Physiol. 93: 117-127.
18. HALL, B.K. and COFFIN-COLLINS, P.A. (1990). Reciprocal interactions between epithelium, mesenchyme, and epidermal growth factor (EGF) in the regulation of mandibular mitotic activity in the embryonic chick. J. Craniofac. Genet. Dev. Biol. 70: 241-261.
19. HALL, B.K. and MIYAKE, T. (1995). Divide, accumulate, differentiate: cell condensation in skeletal development revisited. Int. J. Dev. Biol. 39: 881-893.
20. HAMBURGER, V. and HAMILTON, H.L. (1992). A series of normal stages in the development of the chick embryo. Dev. Dyn. 195: 231-272.
21. HARADA, S., NAKAYAMA, K., OSHIMA H. and RODAN, G.A. (1998). Activation of Sox9 response element by constitutively active type IBMP receptors via a SMADs dependent pathway. Bone 23: S239.
22. HAZAN, R.B. and NORTON, L. (1998). The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 273: 9078-9084.
23. HELMS, J.A., KIM, C. H., HU, D., MINKOFF, R., THALLER, C. and EICHELE, G. (1997). Sonic hedgehog participates in craniofacial morphogenesis and is down-regulated by teratogenic doses of retinoic acid. Dev. Biol. 187: 25-35.
24. HILL, D.J. and LOGAN, A. (1992). Peptide growth factors and their interactions during chondrogenesis. Prog. Growth Factor Res. 4: 45-68.
25. HOGAN, B.L. (1996). Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6: 432-438.
26. JOHTOH, N. and UMEZAWA, K. (1992). Inhibition of EGF-induced cytoskeletal change in A431 cells by inhibitors of phosphatidylinositol turnover. Drug Exp. Clin. Res. 18: 1-7.
27. JONES, K.L. (1997). Smith's recognizable patterns of human malformations (5th edition). W.B. Saunders, Philadelphia.
28. KATO, Y., HIRAKI, Y., INOUE, H., KINOSHITA, M., YUTANI, Y. and SUZUKI, F (1983). Differential and synergistic actions of somatomedin-like growth factors, fibroblast growth factor and epidermal growth factor in rabbit costal chondrocytes. Eur. J. Biochem. 129: 685-690.
29. KAWABATA, M., IMAMURA, T. and MIYAZONO, K. (1998). Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Review 9: 49-61.
30. KRETZSCHMAR, M., LIU, F., HATA, A., DOODY, J. and MASSAGUE, J. (1997). The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11: 984-995.
31. LANCHONEY, T.F., OLMSTED, E.A., SHORE, E.M., GANNON, F.A., ROSEN, V., ZASLOFF, M.A. and KAPLAN, F.S. (1998). Characterization of bone morphogenetic protein 4 receptor in fibrodysplasia ossificans progressiva. Clin. Orthop. 346: 38-45.
32. LEFEBVRE, V. and DE CROMBRUGGHE, B. (1998). Toward understanding SOX9 function in chondrocyte differentiation. Matrix Biol. 16: 529-540.
33. MACIAS-SILVA, M., HOODLESS, P.A., TANG, S.J., BUCHWALD, M. and WRANA, J.L. (1998). Specific activation of Smadl signaling pathways by the BMP7 type I receptor, ALK2. J Biol Chem. 273: 25628-36.
34. MEANS, A.L. and GUDAS, L.J. (1996). FGF-2, BMP-2, and BMP-4 regulate retinoid binding proteins and receptors in 3T3 cells. Cell Growth Differ. 7: 989-996.
35. METSARANTA, M., TOMAN, D., DE CROMBRUGGHE, B. and VUORIO, E. (1991). Mouse type II collagen gene. Complete nucleotide sequence, exon structure, and alternative splicing. J. Biol. Chem. 266: 16862-16869.
36. MIETTINEN, P.J., CHIN, J.R., SHUM, L., SLAVKIN, H.C., SHULER, C.F., DERYNCK, R. and WERB, Z. (1999). Epidermal growth factor receptor function is necessary for normal craniofacial development and palate closure. Nature Genet. 22: 69-73.
37. MIZOGUCHI, I., NAKAMURA, M., TAKAHASHI, I., SASANO, Y., KAGAYAMA, M. and MITANI, H. (1993). Presence of chondroid bone on rat mandibular condyle cartilage. An immunohistochemical study. Anat. Embryol. 187: 9-15.
38. MORGAN, B.A. and FEKETE, D.M. (1996). Manipulating Gene Expression with Replication-Competent Retroviruses. Methods Cell Sci. 57: 185-218.
39. NAH, H.D. and UPHOLT, W.B. (1991). Type II collagen mRNA containing an alternatively spliced exon predominates in the chick limb prior to chondrogenesis. J. Biol. Chem. 266: 23446-23452.
40. NEUBÜSER, A., PETERS, H., BALLING, R. and MARTIN, G.R. (1997). Antagonistic interactions between FGF and BMP signaling pathways: a mechanism for positioning the sites of tooth formation. Cell 90: 247-255.
41. NG, L.J., WHEATLEY, S., MUSCAT, G.E., CONWAY-CAMPBELL, J., BOWLES, J., WRIGHT, E., BELL, D.M., TAM, P.P., CHEAH, K.S. and KOOPMAN, P. (1997). Sox9 binds DNA, activates transcription and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 183: 108-121.
42. NISHIMURA, R., KATO, Y., CHEN, D., HARRIS, S.E., MUNDY, G.R. and YONEDA, T. (1998). Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J. Biol. Chem. 273: 1872-1879.
43. NISWANDER, L. and MARTIN, G.R. (1993). FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361: 68-71.
44. NUCKOLLS, G.H., SLAVKIN, H.C. and SHUM, L. (1998). Bone morphogenetic protein signaling in limb and craniofacial development. In Proceedings of the Biological Mechanisms of Tooth Eruption, Resorption and Replacement by Implants (Ed. Z. Davidowitch), Harvard Society for the Advancement of Orthodontics, EBSCO Media, Birmingham, Alabama, pp. 39-47.
45. OLSEN, B.R. (1996). Role of cartilage collagens in formation of the skeleton. Ann. NY Acad. Sci. 705: 124-130.
46. PAULSEN, D.F., LANGILLE, R.M., DRESS, V. and SOLURSH, M. (1988). Selective stimulation of in vitro limb-bud chondrogenesis by retinoic acid. Differentiation 39: 123-130.
47. PETERS, H. and BALLING, R. (1999). Teeth. Where and how to make them. Trends Genet. 5: 59-65.
48. REDDI, A.M. (1998). Role of morphogenetic proteins in skeletal tissue engineering and regeneration. Nature Biotechnol. 16: 247-252.
49. RIBAULT, D., KHATIB, A.M., PANASYUK, A., BARBARA, A., BOUIZAR, Z. and MITROVIC, R.D. (1997). Mitogenic and metabolic actions of epidermal growth factor on rat articular chondrocytes: modulation by fetal calf serum, transforming growth factor-beta, and tyrphostin. Arch. Biochem. Biophys. 337: 149-158.
50. RIESE, D.J. and STERN, D.F. (1998). Specificity within the EGF family/ErbB receptor family signaling network. BioEssays 20: 41-48.
51. ROSEN, B. and BEDDINGTON, R.S.P. (1993). Whole-mount in situ hybridization in the mouse embryo: gene expression in three dimensions. Trends Genet. 9: 162-167.
52. SASANO, Y., MIZOGUCHI, I., KAGAYAMA, M., SHUM, L., BRINGAS, P. Jr. and SLAVKIN, H.C. (1992). Distribution of type I collagen, type II collagen and PNA binding glycoconjugates during chondrogenesis of three distinct embryonic cartilages. Anat. Embryol. 186: 205-213.
53. SHAFRITZ, A.B., SHORE, E.M., GANNON, F.H., ZASLOFF, M.A., TAUB, R., MUENKE, M. and KAPLAN, F.S. (1996). Overexpression of an osteogenic morphogen infibrodysplasiaossificansprogressiva. New Engl. J. Med. 335: 555-561.
54. SHUM, L., SAKAKURA, Y., BRINGAS, P., LUO, W., SNEAD, M.L., MAYO, M., CROHIN, C., MILLAR, S., WERB, Z., BUCKELY, S., HALL, F.L., WARBURTON, D. and SLAVKIN, H.C. (1993). EGF abrogation induced fusilli-form dysmorphogenesis of Meckel's cartilage during embryonic mouse mandibular morphogenesis in vitro. Development 118: 903-917.
55. SLAVKIN, H.C., CHAI, Y., HU, C.C., MILLAR-GROFF, S. and BRINGAS, Jr., P. (1994). Intrinsic molecular determinants of tooth development from specification to root formation. A review. In Biological Mechanisms of Tooth Eruption, Resorption and Replacement by Implants (Ed. Z. Davidovitch), EBSCO Media, Birmingham, Alabama, pp. 263-272.
56. SOUTHERLAND, S.S. and LUCAS, P.L. (1995). A novel method for the serum-free plating of stage-14 chick limb bud cells. Methods Cell Sci. 17: 17-23.
57. STOTT, N.S., LEE, Y.S. and CHUONG, C.M. (1998). Retroviral gene transfer in chondrogenic limb bud micromass cultures. Biotechniques 24: 660-666.
58. TAKAHASHI, K., NUCKOLLS, G.H., TANAKA, O., SEMBA, I., TAKAHASHI, I., DASHNER, R., SHUM, L. and SLAVKIN, H.C. (1998). Adenovirus mediated ectopic expression of Msx2 in even-numbered rhombomeres induces apoptotic elimination of cranial neural crest cells en ovo. Development 125: 1627-1635.
59. TAMAKI, K., SOUCHELNYTSKYI, S., ITOH, S., NAKAO, A., SAMPATH, K., HELDIN, C.H. and TEN DIJKE, P. (1998). Intracellular signaling of osteogenic protein-1 through Smad5 activation. J. Cell Physiol. 177: 355-363.
60. TERKELTAUB, R.A., JOHNSON, K., ROHNOW, D., GOOMER, R., BURTON, D. and DEFTOS, L.J. (1998). Bone morphogenetic proteins and bFGF exert opposing regulatory effects on PTHrP expression and inorganic pyrophosphate elaboration in immortalized murine endochondral hypertrophic chondrocytes (MCT cells). J. Bone Miner. Res. 13: 931-941.
61. THEILER, K. (1989). The house mouse: atlas of embryonic development. Springer-Verlag, New York.
62. TUCKER, A.S. and SHARPE, P.T. (1999). Molecular genetics of tooth morphogenesis and patterning: the right shape in the right place. J. Dent. Res. 78: 826-834.
63. TUCKER, A.S., AL KHAMIS, A. and SHARPE, P.T. (1998a). Interactions between Bmp-4 and Msx-1 act to restrict gene expression to odontogenic mesenchyme. Dev. Dyn. 212: 533-539.
64. TUCKER, A.S., MATTHEWS, K.L. and SHARPE, P.T. (1998b). Transformation of tooth type induced by inhibition of BMP signaling. Science 282: 1136-1138.
65. URIST, M.R. (1965). Bone: formation by autoinduction. Science 150: 893-899.
66. UWANOGHO, D., REX, M., CARTWRIGHT, E.J., PEARL, G., HEALY, C., SCOTTING, P.J. and SHARPE, P.T. (1995). Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech. Dev. 49: 23-36.
67. VAINIO, S., KARAVANOVA, I., JOWETT, A. and THESLEFF, I. (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75: 45-58.
68. VIVIEN, D., GALERA, P., LEBRUN, E., LOYAU, G. and PUJOL, J.P. (1990). Differential effects of transforming growth factor-beta and epidermal growth factor on the cell cycle of cultured rabbit articular chondrocytes. J. Cell Physiol. 143: 534-545.
69. VORTKAMP, A. (1997). Defining the skeletal elements. Curr. Biol. 7: 104-107.
70. WALL, N.A. and HOGAN, B.L. (1995). Expression of bone morphogenetic protein-4 (BMP-4), bone morphogenetic protein-7 (BMP-7), fibroblast growth factor-8 (FGF-8) and sonic hedgehog (SHH) during branchial arch development in the chick. Mech. Dev. 53: 383-392.
71. WANG, Y.H, UPHOLT, W.B. SHARPE, P.T., KOLLAR, E.J. and MINA, M. (1998). Odontogenic epithelium induces similar molecular responses in chick and mouse mandibular mesenchyme. Dev Dyn. 213: 386-397.
72. WATANABE, Y., DUPREZ, D., MONSORO-BURQ, A.H., VINCENT, C. and LE DOUARIN, N.M. (1998). Two domains in vertebral development: antagonistic regulation by SHH and BMP4 proteins. Development 125: 2631-2639.
73. WILSON, P.A., LAGNA, G., SUZUKI, A. and HEMMATI-BRIVANLOU, A. (1997). Concentration-dependent patterning of the Xenopus ectoderm by BMP4 and its signal transducer Smad1. Development 124: 3177-3184.
74. WOZNEY, J.M. (1998). The bone morphogenetic protein family: multifunctional cellular regulators in the embryo and adult. Eur. J. Oral Sci. 106 (Suppl. 1): 160-166.
75. 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.
76. WRIGHT, E., HARGRAVE, M.R., CHRISTIANSEN, J., COOPER, L., KUN, J., EVANS, T., GANGADHARAN, U., GREENFIELD, A. and KOOPMAN, P. (1995). The Sry-related gene Sox-9 is expressed during chondrogenesis in mouse embryos. Nature Genet. 9: 15-20.
77. XU, R.H., AULT, K.T., KIM, J., PARK, M.J., HWANG, Y.S., PENG, Y., SREDNI, D. and KUNG, H.F. (1999). Opposite effects of FGF and BMP-4 on embryonic blood formation: roles of PV.1 and GATA-2. Dev. Biol. 208: 352-361.
78. YAMAMOTO, N., AKIYAMA, S., KATAGIRI, T., NAMIKI, M., KUFOKAWA, T. and SUDA, T. (1997). Smad1 and smad5 act downstream of intracellular signalings of BMP-2 that inhibits myogenic differentiation and induces osteoblast differentiation in C2C12 myoblasts. Biochem. Biophys. Res. Commun. 238: 574-580.
79. YAMANE, A., MAYO, M.L., BRINGAS, P., JR., CHEN, L., HUYNH, M., THAI, K., SHUM, L. and SLAVKIN, H.C. (1997). TGF-alpha, EGF and their cognate EGF receptor are co-expressed with desmin during embryonic, fetal and neonatal myogenesis in mouse tongue development. Dev. Dyn. 209: 1-14.
80. ZHAO, Q., EBERSPAECHER, H., LEFEBVRE, V. and DE CROMBRUGGHE, B. (1997). Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209: 377-386.
81. ZOU, H., WIESER, R., MASSAGUE, J. and NISWANDER, L. (1997). Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11: 2191-2203.