The Arrangement of Early Inductive Signals in Relation to Gastrulation; Results from Frog and Chick

  • Jonathan Cooke
Part of the Bodega Marine Laboratory Marine Science Series book series (BMSS)


Nieuwkoop and his students first showed clearly that specification of presumptive mesodermal territories in the amphibian embryo, and of their overall orientation, takes place by agency of signals deriving from the yolky vegetal zone (Nieuwkoop 1977, review). This process begins during (possibly early) blastula stages, and is progressive so that by onset of gastrulation, when the first movements begin to produce rearrangement in the induced territories, there is a significant geographical pattern and differential time schedule to these movements, as well as a pattern of differentiation capacities in the tissue when cultured in isolation (Keller et al. 1985; Dale and Slack 1987b). This pattern relates to the subsequent axes of organization of the body. Geographical regionalization on a finer scale is most advanced in a relatively narrow (ca. 90°) sector around the future dorsal midline, and is related to deep vs. superficial position within the blastula wall as well as to cells’ distances from initial sources of induction, i.e., to ‘height’ in the marginal zone towards the animal pole. As described by Keller and his associates (op. cit. and Keller 1986; Wilson et al. 1989) the role of this sector in gastrulation and neurulation and its capacities when developing in isolation entitle it to the designation ‘morphogenetic organ’.


Marginal Zone Xenopus Laevis Xenopus Embryo Neural Induction Animal Pole 
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  1. Boucaut, J.C., T. Darribère, H. Boulekbache, and J.-P. Thiery. 1984. Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature 307:364–367.PubMedCrossRefGoogle Scholar
  2. Cooke, J. 1972. Properties of the primary organization field in the embryo of Xenopus laevis. I. Cell autonomy and behavior at the site of the organizer. J. Embryol. Exp. Morphol 28:13–26.PubMedGoogle Scholar
  3. Cooke, J. 1983. Evidence for specific feedback signals underlying pattern control during vertebrate embryogenesis. J. Embryol. Exp. Morphol. 76:95–114.PubMedGoogle Scholar
  4. Cooke, J. 1985. The system specifying body position in the early development of Xenopus, and its response to perturbations. J. Embryol. Exp. Morphol. 89 (Suppl.):69–87.PubMedGoogle Scholar
  5. Cooke, J. 1987. Dynamics of the control of body pattern in the development of Xenopus laevis. IV. Timing and pattern in the development of twinned bodies after re-orientation of eggs in gravity. Development 99:417–427.PubMedGoogle Scholar
  6. Cooke, J. 1989a. The early amphibian embryo: Evidence for activating and for modulating or self-limiting components in a signalling system that underlies pattern formation, p. 145–158. In: Cell to Cell Signalling. A. Goldbeter (Ed.). Academic Press, New York.Google Scholar
  7. Cooke, J. 1989b. Mesoderm-inducing factors and Spemann’s organiser phenomenon in amphibian development. Development 107:229–241.PubMedGoogle Scholar
  8. Cooke, J. 1989c. Xenopus mesoderm induction: Evidence for early size control and partial autonomy for pattern development by onset of gastrulation. Development 106:519–529.PubMedGoogle Scholar
  9. Cooke, J. and E.J. Smith. 1988. The restrictive effect of early exposure to lithium upon body pattern in Xenopus development, studied by quantitative anatomy and immunofluorescence. Development 102:85–99.PubMedGoogle Scholar
  10. Cooke, J. and J.C. Smith. 1989. Gastrulation and larval pattern in Xenopus after blastocoelic injection of a Xenopus-derived inducing factor: Experiments testing models for the normal organisation of mesoderm. Dev. Biol. 131:383–400.PubMedCrossRefGoogle Scholar
  11. Cooke, J. and J.C. Smith. 1990. Measurement of developmental time by cells of early embryos. Cell 10:891–894.CrossRefGoogle Scholar
  12. Cooke, J., J.C. Smith, E.J. Smith, and M. Yaqoob. 1987. The organisation of mesodermal pattern in Xenopus laevis: Experiments using a Xenopus mesoderm-inducing factor. Development 101:893–908.PubMedGoogle Scholar
  13. Cooke, J., K. Symes, and E.J. Smith. 1989. Potentiation by the lithium ion of morphogenetic responses to a Xenopus inducing factor. Development 105:549–588.PubMedGoogle Scholar
  14. Cooke, J. and J.A. Webber. 1985. Dynamics of the control of body pattern in the development of Xenopus laevis. I. Timing and pattern in the development of dorso-anterior and of posterior blastomere pairs, isolated at the 4-cell stage. J. Embryol. Exp. Morphol. 88:85–112.PubMedGoogle Scholar
  15. Cooke, J. and E.C. Zeeman. 1976. A clock and wavefront model for the control of the number of repeated structures during animal morphogenesis. J. Theor. Biol. 58:455–476.PubMedCrossRefGoogle Scholar
  16. Dale, L. and J.M.W. Slack. 1987a. Fate map for the 32-cell stage of Xenopus laevis. Development 99:197–210.Google Scholar
  17. Dale, L. and J.M.W. Slack. 1987b. Regional specification within the mesoderm of early embryos of Xenopus laevis. Development 100:279–295.PubMedGoogle Scholar
  18. Dixon, J.E. and C.R. Kintner. 1989. Cellular contacts required for neural induction in Xenopus embryos: Evidence for two signals. Development 106:749–757.PubMedGoogle Scholar
  19. Gerhart, J., T. Doniach, and R. Stewart. 1991. Organizing the Xenopus Organizer, p. 57–78. In: Gastrulation: Movements, Patterns, and Molecules. R. Keller, W.H. Clark, Jr., F. Griffin (Eds.). Plenum Press, New York.Google Scholar
  20. Gierer, A. and H. Meinhardt. 1972. A theory of biological pattern formation. Kybernetik 12:30–39.PubMedCrossRefGoogle Scholar
  21. Gimlich, R.L. 1986. Acquisition of developmental autonomy in the equatorial region of the Xenopus embryo. Dev. Biol. 115:340–352.PubMedCrossRefGoogle Scholar
  22. Gimlich, R.L. and J. Gerhart. 1984. Early cellular interactions promote embryonic axis formation in Xenopus laevis. Dev. Biol. 104:117–130.CrossRefGoogle Scholar
  23. Green, J.B.A., G. Howes, K. Symes, J. Cooke, and J.C. Smith. 1990. The biological effects of XTC-MIF: Quantitative comparison with Xenopus. Development 108:173–183.PubMedGoogle Scholar
  24. Green, J.B.A. and J.C. Smith. 1990. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature 347:391–394.PubMedCrossRefGoogle Scholar
  25. Gurdon, J.B., S. Fairman, T.J. Mohun, and S. Brennan. 1985. Activation of muscle-specific actin genes in Xenopus development by an induction between animal and vegetal cells of a blastula. Cell 41:913–922.PubMedCrossRefGoogle Scholar
  26. Keller, R.E. 1976. Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep region. Dev. Biol. 51:118–137.PubMedCrossRefGoogle Scholar
  27. Keller, R.E. 1980. The cellular basis of epiboly: An SEM study of deep cell rearrangement during gastrulation in Xenopus laevis. J. Embryol. Exp. Morphol. 60:201–234.PubMedGoogle Scholar
  28. Keller, R.E. 1986. The cellular basis of amphibian gastrulation. p. 241–328. In: The Cellular Basis of Morphogenesis. L. B. (Ed.). Plenum Press, New York.CrossRefGoogle Scholar
  29. Keller, R.E., M. Danilchik, R.L. Gimlich, and J. Shih. 1985. The function and mechanism of convergent extension during gastrulation of Xenopus laevis. J. Embryol. Exp. Morphol. 89 (Suppl.): 185–209.PubMedGoogle Scholar
  30. Kimelman, D., J.A. Abraham, T. Haaparanta, T.M. Palisi, and M.W. Kirschner. 1988. The presence of fibroblast growth factor in the frog egg, its role as a natural mesoderm inducer. Science 242:1053–1056.PubMedCrossRefGoogle Scholar
  31. Kochav, S., M. Ginsburg, and H. Eyal-Giladi. 1980. From cleavage to primitive streak formation: A complementary normal table and a new look at the first stages of the development of the chick. II. Microscopic anatomy and cell population dynamics. Dev. Biol. 79:296–308.PubMedCrossRefGoogle Scholar
  32. London, C., R. Akers, and C. Phillips. 1988. Expression of Epi-1, an epidermis-specific marker in Xenopus laevis embryos, is specified prior to gastrulation. Dev. Biol. 129:380–389.PubMedCrossRefGoogle Scholar
  33. Meinhardt, H. 1982. Models of Biological Pattern Formation. Academic Press, London.Google Scholar
  34. Mitrani, E. and Y. Shimoni. 1990. Induction by soluble factors of organised axial structures in chick epiblasts. Science 247:1092–1094.PubMedCrossRefGoogle Scholar
  35. New, D.A.T. 1955. A new technique for the cultivation of the chick embryo in vitro. J. Embryol. Exp. Morph. 3:326–331.Google Scholar
  36. Nieuwkoop, P.D. 1977. Origin and establishment of embryonic polar axes in amphibian development. Curr. Top. Dev. 11:115–132.CrossRefGoogle Scholar
  37. Nieuwkoop, P.D. and J. Faber. 1967. Normal table of Xenopus laevis (Daudin). 2nd edition. North Holland, Amsterdam.Google Scholar
  38. Rosa, F.M. 1989. Mix. 1, a homeobox RNA inducible by mesoderm inducers, is expressed mostly in the presumptive endodermal cells of Xenopus embryos. Cell 57:965–974.PubMedCrossRefGoogle Scholar
  39. Ruiz-Altaba, A. 1990. Neural expression of the Xenopus homeobox gene Xhox3: Evidence for a patterning neural signal that spreads through ectoderm. Development 108:595–604.Google Scholar
  40. Ruiz-Altaba, A. and D.A. Melton. 1989a. Bimodal and graded expression of the Xenopus homeobox gene Xhox3 during embryonic development. Development 106:173–183.Google Scholar
  41. Ruiz-Altaba, A. and D.A. Melton. 1989b. Interaction between peptide growth factors and homeobox genes in the establishment of antero-posterior polarity in frog embryos. Nature 341:33–38.CrossRefGoogle Scholar
  42. Sharpe, C.R., A. Fritz, E.M. De Robertis, and J.B. Gurdon. 1987. A homoebox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction. Cell 50:749–758.PubMedCrossRefGoogle Scholar
  43. Slack, J.M.W. and D. Forman. 1980. An interaction between dorsal and ventral regions of the marginal zone in amphibian embryos. J. Embryol. Exp. Morphol. 56:283–299.PubMedGoogle Scholar
  44. Slack, J.M.W., B.G. Darlington, L.L. Gillespie, S.F. Godsave, H.V. Isaacs, and G.D. Paterno. 1989. The role of fibroblast growth factor in early Xenopus development. Development 107 (Suppl.): 141–148.PubMedGoogle Scholar
  45. Slack, J.M.W., B.G. Darlington, J.K. Heath, and S.F. Godsave. 1987. Mesoderm induction in early Xenopus embryos by heparin binding growth factors. Nature 326:197–200.PubMedCrossRefGoogle Scholar
  46. Smith, J.C, B.M.J. Price, K. Van Nimmen, and D. Huylebroeck. 1990a. Identification of a potent Xenopus mesoderm-inducing factor, as a homologue of activin A. Nature 354:729–731.CrossRefGoogle Scholar
  47. Smith, J.C. and J.M.W. Slack. 1983. Dorsalization and neural induction: Properties of the organizer in Xenopus laevis. J. Embryol. Exp. Morphol. 78:299–317.PubMedGoogle Scholar
  48. Smith, J.C., K. Symes, R.O. Hynes, and D.W. DeSimone. 1990b. Mesoderm induction and the control of gastrulation in Xenopus laevis: The roles of fibronectin and integrins. Development 108:229–238.PubMedGoogle Scholar
  49. Smith, J.C., M. Yaqoob, and K. Symes. 1988. Purification, partial characterisation and biological effects of the XTC mesoderm-inducing factor. Development 103:591–600.PubMedGoogle Scholar
  50. Sokol, S., A.A. Wong, and D.A. Melton. 1990. A mouse macrophage factor induces head structure and organises a body axis in Xenopus. Science 249:561–564.CrossRefGoogle Scholar
  51. Spemann, H. and H. Mangold. 1924. Uber Induktion von Embryonenanlagen durch Implantation Artfremder Organisatoren. Wilhelm Roux’s Arch. Dev. Biol. 100:599–638.Google Scholar
  52. Stern, CD. and D.R. Canning. 1990. Origin of cells giving rise to mesoderm and endoderm in chick embryo. Nature 343:273–275.PubMedCrossRefGoogle Scholar
  53. Stewart, R.M. and J.C. Gerhart. 1990. The anterior extent of dorsal development of the Xenopus embryonic axis depends on the quantity of organizer in the later blastula. Development 109:363–372.PubMedGoogle Scholar
  54. Symes, K. and J.C. Smith. 1987. Gastrulation movements provide an early marker of mesoderm induction in Xenopus laevis. Development 101:339–350.Google Scholar
  55. Vale, W., J. River, J. Vaughan, R. McClintock, A. Corrigan, W. Woo, D. Karr, and J. Spiess. 1986. Purification and characterisation of a FSH-releasing protein from porcine ovarian follicular fluid. Nature 321:776–779.PubMedCrossRefGoogle Scholar
  56. Van-Obberghen-Schilling, E., N.S. Roche, K.C Flanders, M.B. Sporn, and A.B. Roberts. 1988. Transforming growth factor β1 Positively regulates its own expression in normal and transformed cells. J. Biol. Chem. 263:7741–7746.PubMedGoogle Scholar
  57. Warner, A. and J.B. Gurdon. 1987. Functional gap junctions are not required for muscle gene activation by induction in Xenopus embryos. J. Cell Biol. 104:557–564.PubMedCrossRefGoogle Scholar
  58. Wilson, P.A., G. Oster, and R. Keller. 1989. Cell rearrangement and segmentation in Xenopus: Direct observation of cultured explants. Development 105:155–166.PubMedGoogle Scholar
  59. Wolpert, L. 1971. Positional information and pattern formation. Curr. Top. Dev. 6:183–223.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Jonathan Cooke
    • 1
  1. 1.Laboratory of EmbryogenesisNational Institute for Medical ResearchLondonUK

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