Gastrulation pp 147-168 | Cite as

Mesoderm Cell Migration in the Xenopus Gastrula

  • Rudolf Winklbauer
  • Andreas Selchow
  • Martina Nagel
  • Cornelia Stoltz
  • Brigitte Angres
Part of the Bodega Marine Laboratory Marine Science Series book series (BMSS)


We analyze the migration of the prospective head mesoderm (HM) across the blastocoel roof (BCR) during gastrulation of the Xenopus embryo. Cell spreading and the concomitant appearance of cytoplasmic lamellae depend on the interaction of HM cells with fibronectin (FN) fibrils, which cover the inner surface of the BCR. Isolated HM cells only extend short-lived filiform protrusions on non-adheasive substrates, but form lamelliform protrusions (usually two lamellae appear simultaneously at opposite ends of a cell) on a FN substrate. Isolated bipolar HM cells move in a step-wise mode of translocation, with in-built changes of the direction of migration. This ineffective mode of migration is altered when HM cells move as part of a larger aggregate, as occurs in the embryo, where the HM forms a coherent cell mass. A Ca++-dependent cell-cell adhesion molecule, U-cadherin, mediates aggregate formation, which is one prerequisite for highly persistent migration. The second requirement is that the mesoderm aggregate moves on a proper substrate. The extracellular matrix of the inner BCR surface can be deposited on a plastic substrate. This conditioned substrate contains directional cues which guide the mesoderm to its target region. The migrating mesoderm becomes visibly polarized on conditioned substrate. Cells appear unipolar and extend protrusions in the direction of migration only, thus underlapping neighboring cells anteriorly. This shingle arrangement of HM cells is also observed in the embryo. We conclude that both cadherin-mediated cell-cell contact and aggregate formation, and a substrate containing guiding cues are required for the unipolar extension of locomotory protrusions, oriented underlapping of neighboring cells, and efficient, persistent, and directional migration of HM cells.


Mesoderm Cell Amphibian Embryo Cytoplasmic Protrusion Protrusion Formation Head Mesoderm 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Angres, B., A. Muller, and P. Hausen. 1991. Differential expression of two cadherins in Xenopus laevis. Development. 111:829–844.PubMedGoogle Scholar
  2. Boucaut, J.-C. and T. Darribère. 1983a. Fibronectin in early amphibian embryos: Migrating mesodermal cells contact fibronectin established prior to gastrulation. Cell Tissue Res. 234:135–145.CrossRefGoogle Scholar
  3. Boucaut, J.-C. and T. Darribère. 1983b. Presence of fibronectin during early embryogenesis in the amphibian Pleurodeles waltlii. Cell Differ. 12:77–83.CrossRefGoogle Scholar
  4. Boucaut, J.-C, T. Darribère, H. Boulekbache, and J.-P. Thiery. 1984a. Prevention of gastrulation but not neurulation by antibodies to fibronectin in amphibian embryos. Nature 307:364–367.PubMedCrossRefGoogle Scholar
  5. Boucaut, J.-C, T. Darribère, T.J. Poole, H. Aoyama, KM. Yamada, and J.-P. Thiery. 1984b. Biologically active synthetic peptides as probes of embryonic development: A competitive peptide inhibitor of fibronectin function inhibits gastrulation in amphibian embryos and neural crest cell migration in avian embryos. J. Cell Biol. 99:1822–1830.PubMedCrossRefGoogle Scholar
  6. Boucaut, J.-C, T. Darribère, D.-L. Shi, H. Boulekbache, KM. Yamada, and J.-P. Thiery. 1985. Evidence for the role of fibronectin in amphibian gastrulation. J. Embryol.Exp. Morphol. 89 (Suppl.):211–227.PubMedGoogle Scholar
  7. Boucaut, J.-C, T. Darribdre, D. Shi, J.-F. Riou, K.E. Johnosn, and M. Delarue. 1991. Amphibian Gastrulation: The Molecular Bases of Mesodermal Cell Migration in Urodele Embryos, p. 169–184. In: Gastrulation: Movements, Patterns, and Molecules. R. Keller, W.H. Clark, Jr., F. Griffin (Eds.). Plenum Press, New York.Google Scholar
  8. Carter, S.B. 1965. Principles of cell motility: The direction of cell movement and cancer invasion. Nature 208:1183–1187.PubMedCrossRefGoogle Scholar
  9. Darribère, T., H. Boulekbache, D.-L. Shi, and J.-C Boucaut. 1985. Immunoelectron microscopic study of fibronectin in gastrulating amphibian embryos. Cell TissueRes. 239:75–80.CrossRefGoogle Scholar
  10. Darribère, T., K Guida, H. Larjava, KE. Johnson, KM. Yamada, J.-P. Thiery, and J.-C Boucaut. 1990. In vivo analyses of integrin Bl subunit function in fibronectin matrix assembly. J. Cell Biol. 110:1813–1823.PubMedCrossRefGoogle Scholar
  11. Darribère, T., K.M. Yamada, K.E. Johnson, and J.-C Boucaut. 1988. The 140-kDa fibronectin receptor complex is required for mesodermal cell adhesion during gastrulation in the amphibian Pleurodeles waltlii. Dev. Biol. 126:182–194.PubMedCrossRefGoogle Scholar
  12. Dipasquale, A. 1975. Locomotory activity of epithelial cells in culture. Exp. Cell Res. 94:191–215.PubMedCrossRefGoogle Scholar
  13. Horibata, K. and A.W. Harris. 1970. Mouse myelomas and lymphomas in culture. Exp. Cell Res. 60:61–77.PubMedCrossRefGoogle Scholar
  14. Keller, R.E. 1986. The cellular basis of amphibian gastrulation. p. 241–327. In: Developmental Biology: A Comprehensive Synthesis. Vol.2. The Cellular Basis of Morphogenesis. L.W. Browder (Ed.). Plenum Press, New York.Google Scholar
  15. Keller, R.E., M. Danilchik, R. 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
  16. Keller, R.E. and G.C. Schoenwolf. 1977. An SEM study of cellular morphology, contact and arrangement as related to gastrulation in Xenopus laevis. Wilhelm Roux’s Arch.Dev. Biol. 182:165–186.CrossRefGoogle Scholar
  17. Keller, R.E. and J. Hardin. 1987. Cell behaviour during active cell rearrangement: Evidence and speculations. J. Cell Sci. Suppl. 8:369–393.PubMedGoogle Scholar
  18. Keller, R. and R. Winklbauer. 1990. The role of the extracellular matrix in amphibian gastrulation. Sem. Dev. Bio. 1:25:33.Google Scholar
  19. Kolega, J. 1981. The movement of cell clusters in vitro: Morphology and directionality. J. Cell Sci. 49:15–32.PubMedGoogle Scholar
  20. König, G. 1988. A method for mounting specimens for scanning electron microscopy. Trends Genet. 4:270.PubMedGoogle Scholar
  21. König, G. 1990. Untersuchungen zur Determination der planaren Zellpolaritdt in denepidermalen Cilienzellen von Embryonen des südafrikanischen KrallenfroschesXenopus laevis. Thesis, Universität Tübingen.Google Scholar
  22. Kubota, H.Y. and A. J. Durston. 1978. Cinematographical study of cell migration in the opened gastrula of Ambystoma mexicanum. J. Embryol. Exp. Morphol. 44:71–80.PubMedGoogle Scholar
  23. Nakatsuji, N. 1975. Studies on the gastrulation of amphibian embryos: Cell movement during gastrulation in Xenopus laevis embryos. Wilhelm Roux’s Arch. Dev. Biol. 178:1–14.CrossRefGoogle Scholar
  24. Nakatsuji, N. and K.E. Johnson. 1982. Cell locomotion in vitro by Xenopus laevis gastrula mesoderm cells. Cell Motil. 2:149–161.PubMedGoogle Scholar
  25. Nakatsuji, N. and K.E. Johnson. 1983a. Comparative study of extracellular fibrils on the ectodermal layer in gastrulae of five amphibian species. J. Cell Sci. 59:61–70.PubMedGoogle Scholar
  26. Nakatsuji, N. and K.E. Johnson. 1983b. Conditioning of a culture substratum by the ectodermal layer promotes attachment and oriented locomotion by amphibian gastrula mesodermal cells. J. Cell Sci. 59:43–60.PubMedGoogle Scholar
  27. Nakatsuji, N, M.A. Smolira, and C.C. Wylie. 1985. Fibronectin visualized by scanning electron microscopy immunocytochemistry on the substratum for cell migration in Xenopus laevis. Dev. Biol. 107:264–268.PubMedCrossRefGoogle Scholar
  28. Nieuwkoop, P.D. and J. Faber. 1967. Normal Table of Xenopus laevis (Daudin). 2nd edition. North-Holland, Amsterdam.Google Scholar
  29. Riou, J.-F., D.-L. Shi, M. Chiquet, and J.-C. Boucaut. 1990. Exogenous tenascin inhibits mesodermal cell migration during amphibian gastrulation. Dev. Biol. 137:305–317.PubMedCrossRefGoogle Scholar
  30. Shi, D.-L., T. Darribere, K.E. Johnson, and J.-C. Boucaut. 1989. Initiation of mesodermal cell migration and spreading relative to gastrulation in the urodele amphibian Pleurodeles waltl. Development 105:351–363.Google Scholar
  31. Takeichi, M. 1988. The cadherins: Cell-cell adhesion molecules controlling animal morphogenesis. Development 102:639–655.PubMedGoogle Scholar
  32. Weiss, P. 1961. Guiding principles in cell locomotion and cell aggregation. Exp. Cell Res. 8 (Suppl.):260–281.CrossRefGoogle Scholar
  33. Winklbauer, R. 1986. Cell proliferation in the ectoderm of the Xenopus embryo: Development of substratum requirements for cytokinesis. Dev. Biol. 118:70–81.PubMedCrossRefGoogle Scholar
  34. Winklbauer, R. 1988. Differential interaction of Xenopus embryonic cells with fibronectin in vitro. Dev. Biol. 130:175–183.PubMedCrossRefGoogle Scholar
  35. Winklbauer, R. 1990. Mesoderm cell migration during Xenopus gastrulation. Dev. Biol. 142:155–168.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Rudolf Winklbauer
    • 1
  • Andreas Selchow
    • 1
  • Martina Nagel
    • 1
  • Cornelia Stoltz
    • 1
  • Brigitte Angres
    • 1
  1. 1.Max Planck Institut fur EntwicklungsbiologieTubingenFederal Republic of Germany

Personalised recommendations