Early Embryonic Induction: The Ectodermal Target Cells

  • Horst Grunz
Part of the NATO ASI Series book series (NSSA, volume 77)


Spemann’s and Hilde Mangold’s famous transplantation experiment[1] showed that in amphibians competent ectoderm (presumptive epidermis) could be triggered to differentiate into neural tissues by the upper blastopore lip of early amphibian gastrulae. Spemann entitled this area with inducing activity as the organisator (organizer), because it organizes the formation of the central nervous system. In the following decades the interest of embryologists has been focused on the question, which factors located in the upper blastopore lip are responsible for the process of primary embryonic induction. Morphogenetic factors, which induce in competent ectoderm the formation of endodermal, mesodermal and neural derivatives, could be isolated from different sources[2–13]. A vegetalizing factor could be isolated in highly purified form from chicken embryos[14,15]. It is now generally accepted that these factors, which in contrast to growth factors can be entitled as determination factors, are protein in nature.


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  1. 1.
    H. Spemann and H. Mangold, Uber Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren, Arch.Entw.Mech. Org., 100: 599–638 (1924).Google Scholar
  2. 2.
    S. Toivonen and T. Kuusi, Implantationsversuche mit in verschiedener Weise vorbehandelten abnormen Induktoren bei Triton, Ann.Soc.Zool.-bot.fenn.Vanamo, 13: 1–19 (1948).Google Scholar
  3. 3.
    T. Yamada, Regional differentiation of the isolated ectoderm of the Triturus gastrula induced through a protein extract, Embryologia, 1: 1–20 (1950).CrossRefGoogle Scholar
  4. 4.
    T. Yamada, Induction of specific differentiation by samples of proteins and nucleoproteins in the isolated ectoderm of Triturus gastrulae, Experientia, 14: 81–87 (1958).CrossRefGoogle Scholar
  5. 5.
    T. Kuusi, Uber die chemische Natur der Induktionsstoffe im Implantationsversuch bei Triton, Experientia, 7: 299–300 (1951a).CrossRefGoogle Scholar
  6. 6.
    T. Kuusi, Uber die chemische Natur der Induktionsstoffe mit besonderer Berücksichtigung der Rolle der Proteine und der Nucleinsäuren. Diss., Helsinki, Ann.Soz.Zool.-bot.fenn.Vanamo 14: 1–98, (1951b).Google Scholar
  7. 7.
    H. Tiedemann and H. Tiedemann, Versuche zur chemischen Kennzeichnung von embryonalen Induktionsstoffen, Hoppe-Seyler’s Z.Physiol.Chem., 306: 7–32 (1956).CrossRefGoogle Scholar
  8. 8.
    H. Tiedemann and H. Tiedemann, Zur Gewinnung von Induktionsstoffen aus Hühnerembryonen, Experientia, 8: 320 (1957).CrossRefGoogle Scholar
  9. 9.
    H. -H. Chuang, Effects of alcohol and heat treatment on inductive ability, Acta.Biol.Exp.Sinica, 8: 3–4 (1963).Google Scholar
  10. 10.
    I. Faulhaber, Anreicherung des vegetalisierenden Induktionsfaktors aus der Gastrula des Krallenfrosches (Xenopus laevis) und Abgrenzung des Molekulargewichtbereiches durch Gradientenzentrifugation, Hoppe-Seyler’s Z.Physiol.Chem., 351: 588–594 (1970).CrossRefGoogle Scholar
  11. 11.
    I. Faulhaber and L. Lyra, Ein Vergleich der Induktionsfähigkeit von Hüllenmaterial der Dotterplättchen-und Microsomenfraktion aus Furchungs-sowie Gastrula-und Neurulastadien des Krallenfrosches Xenopus laevis, Wilhelm Roux ’ Archives, 176: 151–157 (1974).Google Scholar
  12. 12.
    J. Kawakami, S. Noda, K. Kurihara, and K. Okuma, Vegetalizing factor extracted from the fish swimbladder and tested on presumptive ectoderm of Triturus embryos, Wilhelm Roux ’ Archives 182: 1–7 (1977).Google Scholar
  13. 13.
    A. Hoperskaya, Induction: The main principle of melanagenesis in early development, Differentiation, 20: 104–116 (1981).CrossRefGoogle Scholar
  14. 14.
    J. Born, H. P. Geithe, H. Tiedemann, H. Tiedemann, and U. Kocher-Becker, Isolation of a vegetalizing inducing factor, Z.Physiol.Chem., 353: 1075–1084 (1972).CrossRefGoogle Scholar
  15. 15.
    H. P. Geithe, M. Asashima, H. Born, H. Tiedemann, and H. Tiedemann, Isolation of a homogeneous morphogenetic factor, inducing mesoderm and endoderm derived tissues in Triturus ectoderm, Exptl.Cell Res., 94: 447–449 (1975).CrossRefGoogle Scholar
  16. 16.
    P. D. Nieuwkoop and C. J. Weijer, Neural induction, a two-way process, Medical Biology, 56: 366–371.Google Scholar
  17. 17.
    W. Vogt, Weitere Versuche mit vitaler Farbmarkierung und farbiger Transplantation zur Analyse der Primitiventwicklung von Triton, Verh.anat.Ges., (Anat.Anz.suppl.), 57: 30–38 (1923).Google Scholar
  18. 18.
    P. Weiss, Discussion, in: “A Symposium on the Chemical Basis of Development”, W. D. McElroy and B. Glass, eds., The John Hopkins Press, Baltimore, pp. 259–260 (1958).Google Scholar
  19. 19.
    L. Saxên and S. Toivonen, Primary Embryonic induction, Lagos Press, Academic Press, (1962).Google Scholar
  20. 20.
    Nakamura and S. Toivonen, eds., Organizer: A milestone of a half-century from Spemann, Elsevier/North-Holland Biomedical Press, Amsterdam, Oxford, New York, (1978).Google Scholar
  21. 21.
    P. D. Nieuwkoop, The formation of the mesoderm in urodelean amphibians. I. Induction by the endoderm, Wilhelm Roux ’ Archives, 162: 341–373 (1969).Google Scholar
  22. 22.
    O. Nakamura, H. Takasaki, and A. Nagata, Further studies on the prospective fate of blastomeres at the 32 cell stage of Xenopus laevis embryos, Medical Biology, 56: 355–360 (1978).Google Scholar
  23. 23.
    H. Grunz, Differentiation of the four animal and the four vegetal blastomeres of the eight-cell-stage of Triturus alpestris, Wilhelm Roux ’ Archives, 181: 267–277 (1977).Google Scholar
  24. 24.
    J. Holtfreter, Studien zur Ermittlung der Gestaltungsfaktoren in der Organentwicklung der Amphibien, Wilhelm Roux’ Archives, 139: 227–273.Google Scholar
  25. 25.
    H. Grunz, The ultrastructure of amphibian ectoderm treated with an inductor or actinomycin D, Wilhelm Roux ’ Archives, 173: 283–293 (1973).Google Scholar
  26. 26.
    H. Grunz, A. -M. Multier-Lajous, R. Herbst, and G. Arkenberg, The differentiation of isolated amphibian ectoderm with or without treatment with an inductor. A scanning electron microscop study, Wilhelm RouxArchives, 178: 277–284 (1975).Google Scholar
  27. 27.
    H. Mangold, Transplantationsversuche zur Frage der Spezifität und der Bildung der Keimblätter, Wilhelm RouxArchives, 100: 198–301 (1923).Google Scholar
  28. 28.
    J. Holtfreter, Nachweis der Induktionsfähigkeit abgetöteter Keimteile. Isolations-und Transplantationsversuche, Wilhelm Roux ’ Archives, 128: 584–633 (1933).Google Scholar
  29. 29.
    U. Becker, H. Tiedemann, and H. Tiedemann, Versuche zur Determination von embryonalen Amphibiengewebe durch Induktionsstoffe in Lösung, Z.Naturf., 14b: 608–609 (1959).Google Scholar
  30. 30.
    T. Yamada and K. Takata, A technique for testing macromolecular samples in solution for morphogenetic effects on the isolated ectoderm of the amphibian gastrula, Develop.Biol., 3: 411–423 (1961).CrossRefGoogle Scholar
  31. 31.
    H. Grunz, Einfluß von Inhibitoren der RNS-und Protein-synthese und Induktoren auf die Zellaffinität von Amphibiengewebe, Wilhelm RouxArchives, 169: 41–55 (1972).Google Scholar
  32. 32.
    J. Holtfreter and V. Hamburger, Embryogenesis: Progressive differentiation. Amphibians, in: “Analysis of Development”, B. H. Willier, P. A. Weiss, and V. Hamburger, eds., Saunders, Philadelphia and London, pp. 230–296 (1955).Google Scholar
  33. 33.
    A. Leikola, The mesodermal and neural competence of isolated gastrula ectoderm studied by heterogenous inductors, Ann. Zool.Soc.Vanamo, 25: 2–50 (1963).Google Scholar
  34. 34.
    P. D. Nieuwkoop, Neural competence of the gastrula ectoderm in Ambystoma mexicanum. An attempt at quantitative analysis of morphogenesis, Acta Embryol.Morph.Exp., 2: 13–53 (1958).Google Scholar
  35. 35.
    H. -H. Chuang, Untersuchungen über die Reaktionsfähigkeit des Ektoderms mittels sublethaler Cytolyse, J.Acad.Sinica, 4: 151–186 (1955).Google Scholar
  36. 36.
    H. Grunz, Experimentelle Untersuchungen über die Kompetenzverhältnisse früher Entwicklungsstadien des Amphibein-Ektoderms, Wilhelm RouxArchives, 160: 344–347 (1968).Google Scholar
  37. 37.
    H. Grunz, Abhängigkeit der Kompetenz des Amphibien-Ektoderms von der Proteinsynthese, Wilhelm RouxArchives, 165: 91–102 (1970).Google Scholar
  38. 38.
    L. G. Barth, Neural differentiation without organizer, J.Exp. Zool., 87: 371–383 (1941).Google Scholar
  39. 39.
    L. G. Barth and L. J. Barth, The sodium dependence of embryonic induction, Develop.Biol., 20: 236–262 (1969).CrossRefGoogle Scholar
  40. 40.
    S. Karasaki, On the mechanism of the dorsalization in the ectoderm of Triturus gastrulae caused by precytolytic treatments. I. Cytolytical and morphogenetic effects of various injurious agents, Embryologia, 3: 317–334 (1957).CrossRefGoogle Scholar
  41. 41.
    S. LUvtrup, U. Landström, and H. L,Svtrup-Rein, Polarities, cell differentiation and primary induction in the amphibian embryo, Biological Reviews, 53: 1 (1978).CrossRefGoogle Scholar
  42. 42.
    S. LSvtrup, Epigenetic mechanisms in the early amphibian embryo. Cell differentiation and morphogenetic elements, Biological Reviews, 58: 91–130 (1983).CrossRefGoogle Scholar
  43. 43.
    H. L. Wahn, L. E. Lightbody, and T. T. Tchen, Induction of neural differentiation in cultures of amphibian undetermined presumptive epidermis by cyclic AMP derivatives, Science, 188: 366–369 (1975).CrossRefGoogle Scholar
  44. 44.
    G. V. Lopashov, Die Entwicklungsleistungen des Gastrulaektoderms in Abhängigkeit von Veränderungen der Masse, Biol.Zbl., 55: 606–615 (1935).Google Scholar
  45. 45.
    W. B. Muchmore, Differentiation of the trunk mesoderm in Amblystoma maculatum. II. Relation of the size of presumptive somite explants to subsequent differentiation, J.Exp.Zool.; 134: 293–310 (1957).CrossRefGoogle Scholar
  46. 46.
    E. M. Deuchar, Effect of the cell number on the type and stability of differentiation in Amphibian ectoderm, Exp.Cell Res., 59: 341–343 (1969).CrossRefGoogle Scholar
  47. 47.
    H. Grunz, Change of the differentiation pattern of amphibian ectoderm after the increase of the initial cell mass, Wilhelm RouxArchives, 187: 49–57 (1979).Google Scholar
  48. 48.
    H. Grunz and H. Tiedemann, Influence of cyclic nucleotides on amphibian ectoderm, Wilhelm Roux ’ Archives, 181: 261–265 (1977).Google Scholar
  49. 49.
    G. Siegel, H. Grunz, and H. Tiedemann, (in preparation).Google Scholar
  50. 50.
    Waddington, Needham, Brachet, Studies on the nature of the amphibian organization centre. III. The activation of the evocator, Proc.Roy.Soc., London, 120: 173–198 (1936).Google Scholar
  51. 51.
    Y. Masui, Alteration of the differentiation of gastrula ectoderm under influence of lithium chloride, Mem.Konan Univ., Sci.Ser., 4: 79–102 (1960).Google Scholar
  52. 52.
    D. 0. E. Gebhardt and P. D. Nieuwkoop, The influence of lithium on the competence of the ectoderm in Ambystoma mexicanum, J.Embryol.Exp.Morph., 12: 317–331 (1964).Google Scholar
  53. 53.
    J. Holtfreter, Der Einfluß thermischer, mechanischer und chemischer Eingriffe auf die Induzierfähigkeit von Triton-Keimteilen, Wilhelm RouxArchives, 132: 225–306 (1934).Google Scholar
  54. 54.
    H. Tiedemann, U. Becker, and H. Tiedemann, Uber die primären Schritte bei der embryonalen Induktion, Embryologia, 6: 204218 (1961).Google Scholar
  55. 55.
    A. G. Johnen, Experimental studies about the temporal relationships in the induction process. I. Experiments on Amblystoma mexicanum, Proc.Acad.Sci.Amst.Ser.C., 59: 554–561 (1956).Google Scholar
  56. 56.
    A. G. Johnen, Experimental studies about the temporal relationships in the inducing process. II. Experiments on Triturus vulgaris, Proc.Acad.Sci.Amst.Ser.C., 59: 652–660 (1956).Google Scholar
  57. 57.
    H. Grunz, Change in the differentiation pattern of Xenopus laevis ectoderm by variation of the incubation time and concentration of vegetalizing factor, Wilhelm RouxArchives, 192: 130–137 (1983).Google Scholar
  58. 58.
    K. -J. Asahi, J. Born, and H. Tiedemann, Formation of mesodermal pattern by secondary inducing interactions, Wilhelm RouxArchives, 187: 231–244 (1979).Google Scholar
  59. 59.
    M. Minuth and H. Grunz, The formation of mesodermal derivatives after induction with vegetalizing factor depends on secondary cell interactions, Cell differentiation, 9: 229–238 (1980).CrossRefGoogle Scholar
  60. 60.
    M. P. Chuang-Tseng, H. H. Chuang, C. Sandri, and K. Akert, Gap junctions and impulse propagation in embryonic epithelium of amphibia, Cell Tissue Res., 225: 249–258 (1982).CrossRefGoogle Scholar
  61. 61.
    U. Kocher-Becker, H. Tiedemann, and H. Tiedemann, Exovagination of newt endoderm: Cell affinities altered by the mesodermal inducing factor, Science, 147: 167–169 (1965).CrossRefGoogle Scholar
  62. 62.
    H. Grunz and J. Staubach, Changes of the cell surface charge of amphibian ectoderm after induction, Wilhelm RouxArchives, 186: 77–80 (1979).Google Scholar
  63. 63.
    H. Grunz, Mechanisms of competence of early embryonic tissues, Ontogenez, 9: (5), 427–437 (1978).Google Scholar
  64. 64.
    S. Toivonen and J. Wartiovaara, Mechanism of cell interaction during primary embryonic induction studied in transfilter experiments, Differentiation, 5: 61–66 (1976).CrossRefGoogle Scholar
  65. 65.
    S. Toivonen, D. Tarin, L. Saxén, P. J. Tarin, and J. Wartiovaara Transfilter studies on neural induction in the newt, Differentiation, 4: 1–7 (1975).CrossRefGoogle Scholar
  66. 66.
    S. Toivonen, D. Tarin, and L. Saxén, The transmission of morpho-genetic signals from amphibian mesoderm to ectoderm in primary induction, Differentiation, 5: 49–55 (1976).CrossRefGoogle Scholar
  67. 67.
    H. Grunz and J. Staubach, Cell contacts between chorda-mesoderm and the overlaying neuroectoderm (presumptive central nervous system) during the period of primary embryonic induction in amphibians, Differentiation, 14: 59–65 (1979).CrossRefGoogle Scholar
  68. 68.
    Hildegard Tiedemann and J. Born, Biological activity of vegetalizing and neuralizing inducing factors after binding to BAC-Cellulose and CNBr-Sepharose, Wilhelm RouxArchives, 184: 285–299.Google Scholar
  69. 69.
    J. Born, H. Grunz, H. Tiedemann, and H. Tiedemann, Biological activity of the vegetalizing factor: Decrease after coupling to polysaccharide matrix and enzymatic recovery of active factor, Wilhelm RouxArchives, 189: 47–56 (1980).Google Scholar
  70. 70.
    H. Tiedemann, Signals of cell determination in embryogenesis,in: “Colloquim-Moosbach”, Biochemistry of Differentiation and Morphogenesis, Springer-Verlag, Berlin, Heidelberg, p.33 (1982).Google Scholar
  71. 71.
    J. Y. Fan, J. -L. Carpentier, P. Gorden, E. van Obberghen, N. M. Grunfeld, and L. Orci, Receptor-mediated endocytosis of insulin: Role of microvilli, coated pits, and coated vesicles, Proc.Natl.Acad.Sci. USA, 79: 7788–7791 (1982).CrossRefGoogle Scholar
  72. 72.
    J. L. Goldstein, R. G. W. Anderson, and M. S. Brown, Coated pits, coated vesicles, and receptor mediated endocytosis, Nature, 279: 679–682 (1979).CrossRefGoogle Scholar
  73. 73.
    J. Kartenbeck, E. Schmid, H. Müller, and W. F. Werner, Immunological identification and localization of clathrin and coated vesicles in cultured cells and in tissues, Exp.Cell Res., 133: 191–211 (1981).CrossRefGoogle Scholar
  74. 74.
    K. Takata, K. Y. Yamamoto, and R. Ozawa, Use of lectins as probes for analyzing embryonic induction, Wilhelm RouxArchives, 190: 92–96 (1981).Google Scholar
  75. 75.
    A. M. Duprat, L. Gualandris, and P. Rouge, Neural induction and the structure of the target cell surface, J.Embryol.Exp. Morphol., 70: 171–187 (1982).Google Scholar
  76. 76.
    M. Asashima and H. Grunz, Effects of inducers on inner and outer gastrula ectoderm layers of Xenopus laevis, Differentiation, 23: 206–212 (1983).CrossRefGoogle Scholar
  77. 77.
    H. L. Harris and S. E. Zalik, The presence of an endogenous lectin in early embryos of Xenopus laevis, Wilhelm RouxArchives, 191: 208–210 (1982).Google Scholar
  78. /8.
    P. I. Townes and J. Holtfreter, Directed movements and selective adhesion of embryonic amphibian cells, J.Exp.Zool., 128: 5120 (1955).Google Scholar
  79. 79.
    H. Grunz, Hemmung der Reaggregation dissoziierter Amphibienzellen durch Inhibitoren der RNS- und Proteinsynthese, Wilhelm RouxArchives, 163: 184–196 (1969).Google Scholar
  80. 80.
    H. Tiedemann, J. Born, H. Tiedemann, Mechanism of cell differentiation. Affinity of a morphogenetic factor to DNA, Wilhelm RouxArchives, 171: 160–169 (1972).Google Scholar
  81. 81.
    R. A. Roth and D. J. Cassell, Insulin receptor: Evidence that it is a protein kinase, Science, 219: 299–301 (1983).CrossRefGoogle Scholar
  82. 82.
    J. M. Bishop, Enemies within: the genesis of retrovirus oncogenes, Cell, 23: 5–6 (1981).CrossRefGoogle Scholar
  83. 83.
    R. A. Rubin and H. S. Earp, Dimethyl sulfoxide stimulates tyrosine residue phosphorylation of rat liver epidermal growth factor receptor, Science, 219: 60–63 (1983)CrossRefGoogle Scholar

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© Plenum Press, New York 1984

Authors and Affiliations

  • Horst Grunz
    • 1
  1. 1.Universität Essen (FB 9 - Zoophysiologie)Essen 1Germany

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