The head and neck arise during development as the result of a complex series of cellular and molecular interactions that begin in the fertilized egg. In this article, the role of an important class of molecules, growth factors, is examined in two main steps of the developmental sequence: the initial induction of mesoderm and the later induction of jaw cartilage and bone. The article focuses particularly on the roles of members of the transforming growth factor-beta (TGF-β), fibroblast growth factor (FGF), and epithelial growth factor (EGF) families in these processes and current models of growth factor involvement. Possible experiments for the future are discussed.
References
1.
Adamson, E.D.: Developmental Activities of the Epidermal Growth Factor Receptor. Current Topics in Developmental Biology24:1-29 (1990).
2.
Akhurst, R.J., S.A. Lehnert, A. Faissner, and E. Duffie: TGF Beta in Murine Morphogenetic Processes: The Early Embryo and Cardiogenesis. Development108:645-656 (1990).
3.
Albano, R.M., S.F. Godsave, D. Huylebroek, K. Van Nimmen, H.V. Isaacs, J.M.W. Slack, and J.C. Smith: A Mesoderm-Inducing Factor Produced by WEHI-3 Murine Myelomonocytic Leukemia Cells Is Activin A. Development110:43-443 (1990).
4.
Amaya, E., T.J. Musci, and M.W. Kirschner: Expression of a Dominant Negative Mutant of the FGF Receptor Disrupts Mesoderm Formation in Xenopus Embryos. Cell66:257-270 (1991).
5.
Bee, J. and P. Thorogood: The Role of Tissue Interactions in the Skeletogenic Differentiation of Avian Neural Crest Cells. Dev. Biol. 78:47-62 (1980).
6.
Blanchard, M.-G. and N. Josso: Source of the Anti-Mullerian Hormone Synthesized by the Fetal Testis: Mullerian-Inhibiting Activity of Fetal Bovine Sertoli Cells in Tissue Culture. Pediatr. Res. 8:968-971 (1974).
7.
Bonewald, L.F. and G.R. Mundy: Role of Transforming Growth Factor Beta in Bone Remodeling: A review. Conn. Tiss. Res. 23:201-208 (1989).
8.
Boyd, F.T., S. Cheifetz, J. Andres, M. Laiho, and J. Massague: Transforming Growth Factor-β Receptors and Binding Proteoglycans. J. Cell Sci. (Suppl.)13:131-138 (1990).
9.
Bradamante, Z. and B.K. Hall: The Role of Epithelial Collagen and Proteoglycan in the Interaction of Osteogenesis by Avian Neural Crest Cells. Anat. Rec. 197:305-315 (1980).
10.
Carpenter, G. and S. Cohen: Epidermal Growth Factor. J. Biol. Chem. 265:7709-7712 (1990).
11.
Chan, W.Y. and P.P.L. Tam: A Morphological and Experimental Study of the Mesencephalic Neural Crest Cells in the Mouse Embryo using Wheat Germ Agglutinin-Gold Conjugate as the Cell Marker. Development102:427-442 (1988).
12.
Christian, J.L., B.J. Gavin, A.P. McMahon, and R.T. Moon: Isolation of cDNAs Partially Encoding Four Xenopus Wnt-1/int-1-Related Proteins and Characterization of Their Transient Expression During Embryonic Development. Devel. Biol. 143:230-234 (1991).
13.
Christian, J.L., D.J. Olson, and R.T. Moon: Xwnt-8 Modifies the Character of Mesoderm Induced by b-FGF in Isolated Xenopus Ectoderm. EMBO J. (1992, In Press).
14.
Coffin-Collins, P.A. and B.K. Hall: 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 (1989).
15.
Cohen, S.: Isolation of a Mouse Submaxillary Gland Protein Accelerating Incisor Eruption and Eyelid Opening in the Newborn Animal. J. Biol. Chem. 237:1555-1562 (1962).
16.
Cooke, J.: Mesoderm-Inducing Factors and Spemann's Organizer Phenomenon in Amphibian Development. Development107:229-241 (1989).
17.
Cooke, J.: Inducing Factors and Mechanism of Body Pattern Formation in Vertebrate Embryos. Curr. Top. Dev. Biol. 25:45-75 (1991).
18.
Cooke, J. and A. Wong: Growth-Factor-Related Proteins That Are Inducers in Early Amphibian Development May Mediate Similar Steps in Amniote (Bird) Embryogenesis. ( 1991).
19.
Cooke, J., J.C. Smith, E.J. Smith, and M. Yaqoob: The Organization of Mesodermal Pattern in Xenopus laevis: Experiments using a Xenopus Mesoderm-Inducing Factor. Development101:893-908 (1987).
20.
Cross, M. and T.M. Dexter: Growth Factors in Development, Transformation and Tumorigenesis. Cell64:271-280 (1991).
21.
Dale, L., G. Matthews, L. Tabe, and A. Colman: Developmental Expression of the Protein Product of Vgl, a Localized Maternal mRNA in the Frog Xenopus laevis. EMBO J. 8:1057-1065 (1989).
22.
Delli-Bovi, P., A.M. Curatola, F.G. Kern, A. Greco, M. Ittman, and C. Basilico: An Oncogene Isolated by Transfection of Kaposi's Sarcoma DNA Encodes a Growth Factor That Is a Member of the FGF Family. Cell50:729-737 (1987).
23.
Dickson, C., P. Acland, R. Smith, M. Dixon, R. Deed, D. MacAllan, W. Walther, F. Fuller-Pace, P. Kiefer, and G. Peters: Characterization of int-2: A Member of the Fiborblast Growth Factor Family. J. Cell Sci. (Suppl.)13:87-96 (1990).
24.
Durkin, M.E., S. Chakravarti, B.B. Bartos, S-H. Liu, R.L. Friedman, and A.E. Chung: Amino Acid Sequence and Domain Structure of Enactin. Homology with Epidermal Growth Factor Precursor and Low Density Lipoprotein Receptor. J. Cell Biol. 107:2749-2756 (1988 ).
25.
Folkman, J. and M. Klagsbrun: Angiogenic Factors. Science235:442-447 (1987).
26.
Folkman, J., M. Klagsbrun, J. Sasse, M. Wadzinski, D. Ingber, and I. Vlodavsky: A Heparain-Binding Angiogenic Protein-Basic Fiborblast Growth Factor Is Stored within Basement Membrane. Am. J. Pathol. 130:393-400 (1988).
27.
Gatherer, D., P. Ten Dijke, D.T. Baird, and R.J. Ackhurst: Expression of TGF-β Isoforms During First Trimester Human Embryogenesis. Development110:445-460 (1990).
28.
Gillespie, L.L., G.D. Paterno, and J.M.W. Slack: Analysis of Competence: Receptors for Fibroblast Growth Factor in Early Xenopus Embryos. Development106:203-208 (1989).
29.
Goldfarb, M.: The Fibroblast Growth Factor Family. Cell Growth and Differentiation1:439-445 (1990).
30.
Gospodarowicz, D.: Localization of a Fibroblast Growth Factor and Its Effect Alone and with Hydrocortisone on 3T3 Cells Growth. Nature249:123-127 (1974).
31.
Gospodarowicz, D.: Fibroblast Growth Factor and Its Involvement in Developmental Processes. Curr. Top. Dev. Biol. 24:57-93 (1990).
32.
Gospodarowicz, D., J. Weseman, and J. Moran: Presence in Brain of a Mitogenic Agent Promoting Proliferation of Myoblasts in Low Density Culture. Nature256:216-219 (1975).
33.
Gospodarowicz, D., N. Ferrara, L. Schweigerer, and G. Neufeld: Structural Characterization and Bilogical Functions of Fibroblast Growth Factor. Endocr. Rev. 8:95-114( 1987).
34.
Green, J.A., G. Howes, K. Symes, J. Cooke, and J.C. Smith: The Biological Effects of XTC-MIF: Quantitative Comparison with Xenopus bFGF. Development108:173-183 (1990).
35.
Gurdon, J.B.: The Localization of an Inductive Response. Development105:27-33 (1989).
36.
Hall, B.K.: Initiation of Osteogenesis by Mandibular Mesenchyme of the Embryonic Chick in Response to Mandibular and Non-Mandibular Epithelia. Arch. Oral Biol. 23:1157-1161 (1978).
37.
Hall, B.K.: Viability and Proliferation of Epithelia and the Initiation of Osteogenesis within Mandibular Ectomesenchyme in the Embryonic Chick. J. Embryol Exp. Morph. 56:71-89 (1980a).
38.
Hall, B.K.: Tissue Interactions and Initiation of Osteogenesis and Chondrogenesis in the Neural Crest Derived Mandibular Skelton of the Embryonic Mouse as Seen in Isolated Murine Tissues and in Recombinations of Murine and Avian Tissues. J. Embryol. Exp. Morph. 58:251-264 (1980b).
39.
Hall, B.K.: The Induction of Neural Crest-Derived Cartilage and Bone by Embryonic Epithelia: An Analysis of the Mode of Action of an Epithelial-Mesenchyme Interaction, J. Embryol. Exp. Morph. 64:305-320 (1981).
40.
Hall, B.K.: Tissue Interactions in the Development and Evolution of the Vertebrate Head. In: Developmental and Evolutionary Aspects of the Neural Crest, pp. 215-259. (P. F. A. Maderson, Ed.) John Wiley & Sons, New York (1987a).
41.
Hall, B.K.: Sodium Fluoride as an Initiator of Osteogenesis from Embryonic Mesenchyme In Vitro. Bone8:111-116 (1987b).
42.
Hall, B.K.: The Embryonic Development of Bone. Am. Sci. 76:174-181 (1988).
43.
Hall, B.K.: What is Bone Growth? In: Fundamentals of Bone Growth: Methodology and Applications. Proc. of the 3rd International Conference, pp. 605-612. (A. D. Dixon, B. G. Sarnat, and D. A. N. Hoyte, Eds.) CRC Press, Boca Raton, Fla. (1991a).
44.
Hall, B.K.: Cell-Cell Interactions in Craniofacial Growth and Development. In: The Biological Mechanisms of Tooth Movement and Craniofacial Adaptation (1991b, In Press).*
45.
Hall, B.K. and P.A. Coffin-Collins: Reciprocal Interactions Between Epithelium, Mesenchyme and Epidermal Growth Factor (EGF) in the Regulation of Mandibular Mitotic activity in the Embryonic Chick. J. Craniofac. Gen. Dev. Biol. 10:241-261 (1990).
46.
Hall, B.K. and S. Horstadius: The Neural Crest. Oxford University Press, London (1988).
47.
Hall, B.K. and R.J. Van Exan: Induction of Bone by Epithelial Cell Products. J. Embryol. Exp. Morph. 69:37-46 (1982).
48.
Haub, O. and M. Goldfarb: Expression of the Fibroblast Growth Factor-5 Gene in the Mouse Embryo. Development112:397-406 (1991).
49.
Hauschka, P.V., T.L. Chen, and A.E. Mavrakos: Polypeptide Growth Factors in Bone Matrix. Ciba Found. Symp. 136:207-225 (1988).
50.
Heath, J.K. and C.M. Isacke: PC13 Embryonal Carcinoma-Derived Growth Factor EMBO J. 3:2957-2962 (1984).
51.
Heath, J.K., G.D. Patemo, A.C. Lindon, and D.R. Edwards: Expression of Multiple Heparin-Binding Growth Factor Species by Murine Embryonal Carcinoma and Embryonic Stem Cells. Development107:113-122 (1989).
52.
Hebert, J.M., M. Boyle, and G.R. Martin: mRNA Localization Studies Suggest That Murine FGF-5 Plays a Role in Gastrulation. Development112:407-415 (1991).
53.
Heine, U.I., E.F. Munoz, K.C. Flanders, L.R. Ellingsworth, H.-Y.P. Lam, N.L. Thompson, A.B. Roberts, and M.B. Sporn: Role of Transforming Growth Factor-β in the Development of the Mouse Embryo. J. Cell Biol. 105:2861-2876 (1987 ).
54.
Johnson, M.C.: A Radioautographic Study of the Migration and Fate of Cranial Neural Crest Cells in the Chick Embryo. Anat. Res. 156:143-156 (1966).
55.
Jones, E.A. and H.R. Woodland: The Development of Animal Cap Cells in Xenopus: A Measure of the Start of Animal Cap Competence to Form Mesoderm. Development101:557-563 (1987).
56.
Kawamura, M. and M.R. Urist: Growth Factors, Mitogens, Cytokines and Bone Morphogenetic Protein in Induced Chondrogenesis in Tissue Culture. Dev. Biol. 130:435-442 (1988).
57.
Kanzaki, T., A. Olofsson, A. Moren, C. Wernstedt, U. Hellman, K. Miyazono, L. Claesson-Welsh, and C.-H. Heldin: TGF-β1 Binding Protein: A Component of the Large Latent Complex of TGF-β1 with Multiple Repeat Sequences. Cell61:1051-1061 (1990).
58.
Kimelman, D. and M. Kirschner: Synergistic Induction of Mesoderm by FGF and TGF-β and the Identification of an mRNA Encoding for FGF in the Early Xenopus Embryo. Cell51:869-877 (1987).
59.
Kimelman, D. and A. Maas: Induction of Dorsal and Ventral Mesoderm by Ectopically Expressed Xenopus Basic Fibroblast Growth Factor. Development ( 1992, In Press).
60.
Kimelman, D., J.A. Abraham, T. Haaparanta, T.M. Palisi, and M.W. Kirschner: The Presence of Fibroblast Growth Factor in the Frog Egg: Its Role as a Natural Mesoderm Inducer. Science242:1053-1056 (1988).
61.
Kondaiah, P., M.J. Sands, J.M. Smith, A. Fields, A.B. Roberts, M.B. Sporn, and D.A. Melton: Identification of a Novel Transforming Growth Factor β (TGF-β5) mRNA in Xenopus laevis. J. Biol. Chem. 265:1089-1093 (1990).
62.
Krusius, T., K.R. Gehlsen, and E. Ruoslahti: A Fibroblast Chondroitin Sulfate Proteoglycan Core Protein Contains Lectin-like and Growth Factor-like Sequences. J. Biol. Chem. 262:13120-13125 (1987).
63.
Langille, R.M. and M. Solursh: Formation of Chondrous and Osseus Tissues in Micromass Cultures of Rat Frontonasal and Mandibular Ectomesenchyme. Differentiation44:197-206 (1990).
64.
Langille, R.M. and A. Sakai: Effects of Retinoic Acid and TGF-β on Rat Mandibular and Frontonasal Mesenchyme In Vitro. Anat. Rec. 229:50A (1991 ).
65.
Langille, R.M., D.F. Paulsen, and M. Solursch: Differential Effects of Physiological Concentrations of Retinoic Acid In Vitro on Chondrogenesis and Myogenesis in Chick Craniofacial Mesenchyme. Differentiation40:84-92 (1989).
66.
Le Douarin, N.M.: The Neural Crest. Cambridge University Press, Cambridge, England (1982).
67.
Ling, N., S.-Y. Ying, N. Ueno, F. Esch, L. Denoroy, and R. Guillemin: Isolation and Partial Characterization of a M, 32,000 Protein with Inhibin Activity from Porcine Follicular Fluid. Proc. Natl. Acad. Sci. U.S.A.82:7217-7221 (1985 ).
68.
Lyons, K., J.L. Graycar, A. Lee, S. Hashmi, P.B. Lindquist, E.Y. Chen, B.L.M. Hogan, and R. Derynck: Vgr-1, a Mammalian Gene Related to Xenopus Vg-1, Is a Member of the Transformation Growth Factor β Gene Superfamily. Proc. Natl. Acad. Sci. U.S.A.86:4554-4558 (1989 ).
69.
Lyons, K.M., R.W. Pelton, and B.L. Hogan: Organo-genesis and Pattern Formation in the Mouse: RNA Distribution Patterns Suggest a Role for Bone Morphogenetic Protein-2A (BMP-2A). Development109:833-844 (1990).
Matrisian, L.M. and B.L.M. Hogan: Growth Factor-Regulated Proteases and Extracellular Matrix Remodelling during Mammalian Development. Curr. Top. Dev. Biol. 24:219-259 (1990).
72.
Melton, D.A.: Pattern Formation During Animal Development. Science252:234-241 (1991).
73.
Mercola, M. and C.D. Stiles: Growth Factor Superfamilies and Mammalian Embryogenesis. Development102:451-460 (1988).
74.
Millan, F.A., F. Denhez, P. Kondaiah, and R.J. Akhurst: Embryonic Gene Expression Patterns of TGF (β1, β2 and β3 Suggest Differential Developmental Functions In Vivo. Development111:131-144 (1991).
75.
Mina, M., E.J. Kollar, A.B. Joann, and D.H. Rohrbach: Interaction between the Neural Crest and Extracellular Matrix Proteins in Craniofacial Skeletogenesis. Crit. Rev. Oral Biol. Med. 1(2):79-87 (1990).
76.
Mitrani, E., T. Ziv, G. Thomsen, Y. Shimoni, D.A. Melton, and A. Bril: Activin Can Induce the Formation of Axial Structures and Is Expressed in the Hypoblast of the Chick. Cell63:495-501 (1990a).
77.
Mitrani, E., Y. Gruenbaum, H. Shohat, and T. Ziv: Fibroblast Growth Factor During Mesoderm Induction in the Early Chick Embryo. Development109:387-393 (1990b).
78.
Mummery, C.L. and A.J.M. Van den Einjden-Van Raaij: Growth Factors and Their Receptors in Differentiation and Early Murine Development. Cell Differ. Dev. 30:1-18 (1990).
79.
Mummery, C.L., T.A.E. Van Achterberg, A.J.M. Van den Eijnden-Raaij, L. Van Haaster, A. Willemse, S.W. De Laat, and A.H. Peirsma: Visceral-Endoderm-like Cell Lines Induce Differentiation of Murine P19 Embryonal Carcinoma Cells. Differentiation46:51-60 (1991).
80.
Musci, T.J., E. Amaya, and M.W. Kirschner: Regulation of the Fibroblast Growth Factor Receptor in Early Xenopus Embryos. Proc. Natl. Acad. Sci. U.S.A. 87:8365-8369 (1990).
81.
Nichols, D.H.: Formation and Distribution of Neural Crest Mesenchyme to the First Pharyngeal Arch Region of the Mouse Embryo. Am. J. Anat. 176:221-231 (1986).
82.
Nieukoop, P.D.: The Formation of the Mesoderm in Urodelean Amphibians. I. Induction by the Endoderm. Wilhelm Roux's Archives162:341-373 (1969).
83.
Nilsen-Hamilton, M.: Transforming Growth Factor-β and Its Actions on Cellular Growth and Differentiation. In: Current Topics in Developmental Biology, Vol. 24, pp. 95-128. (M. Nilsen-Hamilton, Ed.) San Diego: Academic Press (1990).
84.
Noden, D.M.: Interactions between Cephalic Neural Crest and Mesodermal Populations. In: Developmental and Evolutionary Aspects of the Neural Crest, pp. 89-119. (P. F. A. Maderson, Ed.) John Wiley & Sons, New York ( 1987).
85.
Osumi-Yamashita, N. and E. Kazuhiro: Mammalian Cranial Neural Crest Cells and Facial Development. Dev. Growth Differ. 32(5):451-459 (1990).
86.
Panatoyou, G., P. End, M. Aumailly, R. Timpi, and J. Engel: Domains of Laminin with Growth-Factor Activity. Cell56:93-101 (1989).
87.
Paralkar, V.M., S. Vukicevic, and A.H. Reddi: Transforming Growth Factor β Type 1 Binds to Collagen IV of Basement Membrane Matrix: Implications for Development ( 1991).
88.
Partanen, A.-M.: Epidermal Growth Factor and Transforming Growth Factor-a in the Development of Epithelial-Mesenchymal Organs of the Mouse. Curr. Top. Dev. Biol. 24:31-55 (1990).
89.
Paterno, G.D., L. Gillespie, M.S. Dixon, J.M.W. Slack, and J.K. Heath: Mesoderm-inducing Properties of Int-2 and kFGF: Two Oncogene-encoded Growth Factors Related to FGF. Development106:79-83 (1989).
90.
Pelton, R.W., S. Nomura, H.L. Moses, and B.L.M. Hogan: Expression of Transforming Growth Factor β2 RNA during Murine Embryogenesis. Development106:759-767 (1989).
91.
Pondel, M.D. and M.L. King: Localized Maternal mRNA Related to Transforming Growth Factor β mRNA Is Concentrated in a Cytokeratin-Enriched Fraction from Xenopus Oocytes. Proc. Natl. Acad. Sci. U.S.A. 85:7612-7616 (1988).
92.
Richman, J.M. and Z. Crosby: Differential Growth of Facial Primordia in Chick Embryos: Responses of Facial Mesenchyme to Basic Fibroblast Growth Factor (BFGF) and Serum in Micromass Culture. Development109:341-348 (1990).
93.
Rifkin, D.B. and D. Moscatelli: Recent Developments in the Cell Biology of Basic Fibroblast Growth Factor. J. Cell Biol. 109:1-6 (1989).
94.
Rizzino, A.: Transforming Growth Factor-β: Multiple Effects on Cell Differentiation and Extracellular Matrices. Dev. Biol. 130:411-422 (1988).
95.
Roberts, A.B., F. Rosa, N.S. Roche, J.E. Coligan, M. Garfield, M.L. Rebbert, P. Kondaiah, D. Danielpour, J.H. Kehrl, S.M. Wahl, I.B. Dawid, and M.B. Sporn: Isolation and Characterization of TGF-B2 and TGF-B5 from Medium Conditioned by Xenopus XTC Cells. Growth Factors2:135-147 (1990).
96.
Rosa, F., A.B. Roberts, D. Danielpour, L.L. Dart, M.B. Sporn, and I.B. Dawid: Mesoderm Induction in Amphibians: The Role of TGF-B2-like Factors. Science239:783-785 (1988).
97.
Ruiz i Altaba, A. and D.A. Melton: Interaction between Peptide Growth Factors and Homeobox Genes in the Establishment of Antero-Posterio Plarity in Frog Embryos. Nature341:33-38 (1989).
98.
Ruoslahti, E. and M.D. Pierschbacher: Arg-Gly-Asp: A Versatile Cell Recognition Signal. Cell44:517-519 (1986).
99.
Sakai, A. and R.M. Langille: Effects of Retinoic Acid and TGF-β on Chondrogenesis in Chick Mandibular and Frontonasal Mesenchymal Cells In Vitro. Anat. Rec. 229:78A (1991).
100.
Sanders, E.J. and S. Prasad: Possible Roles for TGF-β1 in the Gastrulating Chick Embryo. J. Cell Sci. 99:617-626 (1991).
101.
Sasaki, M., S. Kato, K. Kohno, G.R. Martin, and Y. Amada: Sequence of the cDNA Encoding the Laminin B1 Chain Reveals a Multidomain Protein Containing Cysteine-Rich Repeats. Proc. Natl. Acad. Sci. U.S.A.84:935-939 (1987).
102.
Saxen, L.: Neural Induction. Int. J. Dev. Biol. 33:21-48 (1989).
103.
Schmid, P., D. Cox, G. Bilbe, R. Maier, and G.K. McMaster: Differential Expression of TGF β1, β2 and β3 Genes during Mouse Embryogenesis. Development111:117-130 (1991).
104.
Slack, J.M.W.: Growth Factors as Inducing Agents in Early Xenopus Development. J. Cell Sci. (Suppl.)13:119-130 (1990).
105.
Slack, J.M.W. and H.V. Isaacs: Presence of Basic Fibroblast Growth Factor in the Early Xenopus Embryo. Development105:147-153 (1989).
106.
Slack, J.M.W., B.G. Darlington, J.K. Heath, and S.F. Godsave: Mesoderm Induction in Early Xenopus Embryos by Heparin-Binding Growth Factors. Nature326:197-200 (1987).
107.
Slack, J.M.W., B.G. Darlington, L.L. Gillespei, S.F. Godsave, H.V. Isaacs, and G.D. Paterno: The Role of Fibroblast Growth Factor in Early Xenopus Development. Development (Suppl.) 00:141-148 (1989).
108.
Slager, H.G., K.A. Lawson, A.J.M. Van den Eijnden-Van Raaij, S.W. DeLaat, and C.L. Mummery: Differential Localization of TGF-β2 in Mouse Preimplantation and Early Postimplantation Development. Dev. Biol. 145:205-218 (1991).
109.
Smith, J.C.: A Mesoderm-inducing Factor Is Produced by a Xenopus Cell Line. Development99:3-14 (1987).
110.
Smith, J.C.: Mesoderm Induction and Mesoderm-Inducing Factors in Early Amphibian Development. Development105:665-677 (1989a).
111.
Smith, J.C.: Induction and Early Amphibian Development. Curr. Opin. Cell Biol. 1:1061-1070 (1989b).
112.
Smith, J.C., M. Yaqoob, and K. Symes: Purification, Partial Characterization and Biological Effects of the XTC Mesoderm-inducing Factor. Development103:591-600 (1988).
113.
Smith, J.C., B.M.J. Price, K. Van Nimmen, D. Huylebroeck: Identification of a Potent Xenopus Mesoderm-inducing Factor as a Homologue of Activin A. Nature34:729-731 (1990).
114.
Smith, M.M. and B.K. Hall: Development and Evolutionary Origins of Vertebrate Skeletogenic and Odontogenic Tissues. Biol. Rev. 65:277-373 (1990).
115.
Smith, W.C. and R.M. Harland: Injected Xwnt-8 RNA Acts Early in Xenopus Embryos to Promote Formation of a Vegetal Dorsaling Center. Cell67:753-765 (1991).
116.
Sokol, S. and D.A. Melton: Pre-Existent Pattern in Xenopus Animal Pole Cells Revealed by Induction with Activin. Nature351:409-411 (1991).
117.
Sokol, S., J.L. Christian, R.T. Moon, and D.A. Melton: Injected Wnt RNA Induces a Complete Body Axis in Xenopus Embryos. Cell67:741-752 (1991).
118.
Spemann, H. and H. Mangold: Uber Induktion von Embryonenanlagen durch Implantation artfremder Organisatoren. Wilhelm Roux's Archiv. 100:599-638 (1924).
119.
Spencer, F.A., F.M. Hoffmann, and W.M. Gelbart: Decapentaplegic: A Gene Complex Affecting Morphogenesis in Drosophila melanogaster. Cell28:451-461 (1982).
120.
Sporn, M.B. and A.B. Roberts: Transforming Growth Factor Beta: New Chemical Forms and New Biological Roles. Biofactors1:89-93 (1988).
121.
Tan, S.S. and G.M. Morris-Kay: Analysis of Cranial Neural Crest Migration and Early Fates in Postimplantation Rat Chimeras. J. Embryol. Exp. Morph. 98:21-58 (1986).
122.
Tannahill, D. and D.A. Melton: Localized Synthesis of the Vgl Protein during Early Xenopus Development. Development106:775-785 (1989).
123.
Thomsen, G., T. Woolf, M. Whitman, S. Sokol, J. Vaughan, W. Vale, and D.A. Melton: Activins Are Expressed Early in Xenopus Embryogenesis and Can Induce Axial Mesoderm and Anterior Structures. Cell63:485-493 (1990).
124.
Tosney, K.W.: The Segregation and Early Migration of Cranial Neural Crest Cells in the Avian Embryo. Dev. Biol. 89:13-24 (1982).
125.
Tyler, M.S. and B.K. Hall: Epithelial Influences on Skeletogenesis in the Mandible of the Embryonic Chick. Anat. Rec. 118:229-240 (1977).
126.
Tyler, M.S. and D.P. McCobb: The Genesis of Membrane Bone in the Embryonic Chick Maxilla: Epithelial-Mesenchymal Tissue Recombination Studies. J. Embryol. Exp. Morph. 56:269-281 (1980).
127.
Van den Eijnden-Van Raaij, A.J.M., T.A.E. Van Achterberg, C. M. M. Van der Kruijssen, A.H. Peirsma, D. Huylebroeck, S.W. De Laat, and C.L. Mummery: Differentiation of Aggregated Murine P19 Embryonal Carcinoma Cells Is Induced by a Novel Visceral Endoderm-Specific FGF-Like Factor and Inhibited by Activin A. Mechan. Dev. 33:157-166 (1991).
128.
Wedden, S.E., M.R. Lewin-Smith, and C. Tickel: The Patterns of Chondrogenesis of Cells from Facial Primordia of Chick Embryos in Micromass Culture. Dev. Biol. 117:71-82 (1986).
129.
Wedden, S.E., J.R. Ralphs, and C. Tickle: Pattern Formation in the Facial Primordia. Development103:(Suppl.) 31-40 (1988).
130.
Weeks, D.L. and D.A. Melton: A Maternal mRNA Localized to the Vegetal Hemisphere in Xenopus Eggs Codes for a Growth Factor Related to TGF-β. Cell51:861-867 (1987).
131.
Westermann, R., C. Grothe, and K. Unsicker: Basic Fibroblast Growth Factor (bFGF), a Multifunctional Growth Factor for Neuroectodermal Cells. J. Cell Sci. (Suppl.)13:97-117 (1990).
132.
Whitman, M. and D.A. Melton: Growth Factors in Early Embryogenesis. Annu. Rev. Cell Biol. 5:93-117 (1989).
133.
Wilkinson, D.G., G. Peters, C. Dickson, and A.P. McMahon: Expression of the FGF-Related Proto-Oncogene int-2 during Gastrulation and Neurulation in the Mouse. EMBO J. 7:691-695 (1988).
134.
Wozney, J.M., V. Rosen, M. Byme, A.J. Celeste, I. Moutsatsos, and E.A. Wang: Growth Factors Influencing Bone Development. J. Cell Sci. (Suppl.) 13:149-156 (1990).
135.
Yamaguchi, Y., D.M. Mann, and E. Ruoslahti: Negative Regulation of Transforming Growth Factor-β by the Proteoglycan Decorin. Nature346:281-284 (1990).
136.
Yisraeli, J.K. and D.A. Melton: The Maternal mRNA Vgl is Correctly Localized Following Injection IntoXenopus Oocytes. Nature336:592-595 (1988).
137.
Zhan, X., B. Bates, X. Hu, and M. Goldfard: The Human FGF-5 Oncogene Encodes a Novel Protein Related to Fibroblast Growth Factors. Mol. Cell. Biol. 8:3487-3495 (1988 ).
