Gastrulation pp 313-327 | Cite as

The Role of Cell Adhesion During Gastrulation in The Sea Urchin

  • David R. McClay
Part of the Bodega Marine Laboratory Marine Science Series book series (BMSS)


For those who are interested in morphogenetic movements, the gastrula has long been a favorite embryonic stage for study. Gastrulation occurs early in morphogenesis so that the movements are rather simple to describe, though even then the descriptions can be long and detailed [Gustafson and Wolpert 1967; Gerhart and Keller 1986]. The general wisdom has been that since gastrulation is a time when there are relatively few cell types in the embryo, one ought to be able to explain how various morphogenetic movements occur in the emergence of pattern. Often there is an attempt to simplify, though in actuality, simplicity need not be a component of any movement. In fact, if one begins to study a single morphogenetic movement in some detail, that movement begins to appear more and more complicated, especially when one considers gene expression, changing adhesions, shifting cell positions, cell motility, net directionality of cell movements, etc. The morphogenetic event soon becomes bewilderingly complicated. And if one then projects to the complex anatomy that eventually carries the organism through its somatic lifetime, the complexity seems even more impressive. Yet at the same time we are persuaded that there must be some simplicity in the rules that govern pattern because, to use the same argument that led immunologists to look for simplicity in the immunoglobulin gene, there is not enough genomic space for each cell to be given its own complete set of instructions that are qualitatively different from those of any other cell.


Adhesion Molecule Cell Interaction Endoderm Cell Vegetal Pole Morphogenetic Movement 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adelson, D.L. and T. Humphreys. 1988. Sea urchin morphogenesis and cell-hyalin adhesion are perturbed by a monoclonal antibody specific for hyalin. Development 104:391–402.PubMedGoogle Scholar
  2. Alliegro, M.C., C.A. Burdsal, and D.R. McClay. 1990. In vitro biological activities of echinonectin. Biochemistry 29:2135–2141.PubMedCrossRefGoogle Scholar
  3. Alliegro, M.C., C.A. Ettensohn, C.A. Burdsal, H.P. Erickson, and D.R. McClay. 1988. Echinonectin: A new embryonic substrate adhesion protein. J. Cell Biol. 107:2319–2327.PubMedCrossRefGoogle Scholar
  4. Austin, J. and J. Kimble. 1989. Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58:565–571.PubMedCrossRefGoogle Scholar
  5. Bernacki, S.H. and D.R. McClay. 1989. Embryonic cellular organization: Differential restrictions of fates as revealed by cell aggregates and lineage markers. J. Exp. Zool. 251:203–216.PubMedCrossRefGoogle Scholar
  6. Bixby, J.L., R.S. Pratt, J. Lilien, and L.F. Reichardt. 1987. Neurite outgrowth on muscle cell surfaces involves extracellular matrix receptors as well as Ca2+-dependent and-independent cell adhesion molecules. Proc. Natl. Acad. Sci. USA 84:2555–2559.PubMedCrossRefGoogle Scholar
  7. Buck, C.A and A.F. Horowitz. 1987. Cell surface receptors for extracellular matrix molecules. Annu. Rev. Cell Biol. 3:179–205.PubMedCrossRefGoogle Scholar
  8. Burdsal, C.A., M.C. Alliegro, and D.R. McClay. 1991. Tissue-specific, temporal changes in cell adhesion to echinonectin within the mesoderm and ectoderm lineages of the sea urchin embryo. Dev. Biol. 144:327–334.PubMedCrossRefGoogle Scholar
  9. Burridge, K, K. Fath, T. Kelly, G. Nuckolls, and C. Turner. 1988. Focal adhesions: Transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487–526.PubMedCrossRefGoogle Scholar
  10. Burridge, K., L. Molony, and T. Kelly. 1987. Adhesion plaques: Sites of transmembrane interaction between the extracellular matrix and the actin cytoskeleton. J. Cell Sci.Suppl. 8:211–229.PubMedGoogle Scholar
  11. Cervello, M. and V. Matranga. 1989. Evidence of a precursor-product relationship between vitellogenin and toposome, a glycoprotein complex mediating cell adhesion. Cell Differ. Dev. 26:67–76.PubMedCrossRefGoogle Scholar
  12. Cooke, J. 1989. Mesoderm-inducing factors and Spemann's organiser phenomenon in amphibian development. Development. 107:229–241.PubMedGoogle Scholar
  13. Dan, K. and T. Ono. 1952. Cyto-embryological studies of sea urchins. I. The means of fixation of the mutual position among the blastomeres of sea urchin larvae. Biol.Bull102:58–73CrossRefGoogle Scholar
  14. Edelman, G.M. 1985. Cell adhesion and the molecular process of morphogenesis. Annu.Rev. Biochem. 54:135–169.PubMedCrossRefGoogle Scholar
  15. Ettensohn, C.A. 1985. Gastrulation in the sea urchin is accompanied by the rearrangement of invaginating epithelial cells. Dev. Biol. 112:383–390.PubMedCrossRefGoogle Scholar
  16. Fehon, R.G., P.J. Kooh, I. Rebay, C.L. Regan, T. Xu, AT. Muskavitch, and S. Artavanis-Tsakonas. 1990. Molecular interactions between the protein products of the neurogenic loci notch and delta, two EGF-Homologous genes in Drosophila.Cell 61:523–534.PubMedCrossRefGoogle Scholar
  17. Fink, R.D. and D.R. McClay. 1985 Three cell recognition changes accompany the ingression of sea urchin primary mesenchyme cells. Dev. Biol. 107:66–74.PubMedCrossRefGoogle Scholar
  18. Gerhart, J. and R. Keller. 1986. Region-specific cell activities in amphibian gastrulation. Annu. Rev. Cell Biol. 2:201–229.PubMedCrossRefGoogle Scholar
  19. Giudice, G. and V. Mutolo. 1970. Reaggregation of dissociated cells of sea urchin embryos. Adu. Morphog. 10:115–158.Google Scholar
  20. Gustafson, T. and L. Wolpert. 1967. Cellular movement and contact in sea urchin morphogenesis. Biol. Rev. Camb. Philos. Soc. 42:442–498.PubMedCrossRefGoogle Scholar
  21. Hall, G. and V. Vacquier. 1982. The apical lamina of the sea urchin embryo: Major glycoproteins associated with the hyaline layer. Dev. Biol. 89:160–178.CrossRefGoogle Scholar
  22. Hardin, J. 1988. The role of secondary mesenchyme cells during sea urchin gastrulation studied by laser ablation. Development 103:317–324.PubMedGoogle Scholar
  23. Hardin, J. 1989. Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev. Biol. 136:430–445.PubMedCrossRefGoogle Scholar
  24. Hardin, J. and D.R. McClay. 1990. Target recognition by the archenteron during sea urchin gastrulation. Dev. Biol. 142:86–102.PubMedCrossRefGoogle Scholar
  25. Harris, A. 1973. Behavior of cultured cells on substrata of variable adhesiveness. Exp.Cell Res. 77:285–296.PubMedCrossRefGoogle Scholar
  26. Herbst, C. 1900. Ober das Auseinandergehen von Furchungszellen und Gewebezellen in kalkfreiem Medium. Wilhelm Roux’ Arch. Entwicklungsmech Org. 9:424–463.Google Scholar
  27. Holtfreter, J. 1943. A study of the mechanics of gastrulation. Part I. J. Exp. Zool. 94:261–318.CrossRefGoogle Scholar
  28. Hynes, R.O. 1987. Integrins: A family of cell surface receptors. Cell 48:549–554.PubMedCrossRefGoogle Scholar
  29. Jessell, T.M., M.A. Hynes and J. Dodd. 1990. Carbohydrates and carbohydrate-binding proteins in the nervous system. Annu. Rev. Neurosci. 13:227–256.PubMedCrossRefGoogle Scholar
  30. Kane, R.E. 1973. Hyalin release during normal sea urchin development and its replacement after removal at fertilization. Exp. Cell Res. 81:301–311.PubMedCrossRefGoogle Scholar
  31. Kane, R.E. and R.E. Stephens. 1969. A comparative study of the isolation of the cortex and the role of the calcium-insoluble protein in several species of sea urchin egg. J. Cell Biol. 41:133–144.PubMedCrossRefGoogle Scholar
  32. Lee, G.F., E.W. Fanning, M.P. Small, and M.B. Hille. 1989. Developmentally regulated proteolytic processing of a yolk glycoprotein complex in embryos of the sea urchin, Strongylocentrotus purpuratus. Cell Differ. 26:5–18.CrossRefGoogle Scholar
  33. Lotz, M.M., C.A. Burdsal, H.P. Erickson, and D.R. McClay. 1989. Cell adhesion to fibronectin and tenascin: Quantitative measurements of initial binding and subsequent strengthening response. J. Cell Biol. 109:1795–1805.PubMedCrossRefGoogle Scholar
  34. McCarthy, R.A., K. Beck, and M.M. Burger. 1987 Laminin is structurally conserved in the sea urchin basal lamina. EMBO J. 6:1587–1593.PubMedGoogle Scholar
  35. McCarthy, R.A. and M.M. Burger. 1987 In vivo embryonic expression of laminin and its involvement in cell shape change in the sea urchin Sphaerechinus granulans.Development 101:659–671.Google Scholar
  36. McCarthy, R.A. and M. Spiegel. 1983. Protein composition of the hyaline layer of sea urchin embryos and reaggregating cells. Cell Differ. 13:93–102.PubMedCrossRefGoogle Scholar
  37. McClay, D.R., M.C. Alliegro, and S.D. Black. 1990a. The ontogenetic appearance of extracellular matrix during sea urchin development, p. 1–15. In: Organization andAssembly of Plant and Animal Extracellular Matrix. S. Adair and R. Mecham (Eds.). Academic Press, New York.Google Scholar
  38. McClay, D.R., M.C. Alliegro, and J.D. Hardin. 1990b. Cell interactions as epigenetic signals in morphogenesis of the sea urchin embryo, p. 70–87. In: The Cellular andMolecular Basis of Pattern Formation. D. Stocum and T. Karr (Eds.). Oxford University Press, Oxford.Google Scholar
  39. McClay, D.R. and A.F. Chambers. 1978. Identification of four classes of cell surface antigens appearing at gastrulation in sea urchin embryos. Dev. Biol. 63:179–186.PubMedCrossRefGoogle Scholar
  40. McClay, D.R., A.F. Chambers, and R.G. Warren. 1977. Specificity of cell-cell interactions in sea urchin embryos. Appearance of new cell-surface determinants at gastrulation. Dev. Biol. 56:343–355.PubMedCrossRefGoogle Scholar
  41. McClay, D.R., J.C. Coffman, and J.D. Hardin. 1990c. Epigenetic signals at gastrulation in the sea urchin. UCLA Symp. Mol. Cell. Biol. 125:251–256.Google Scholar
  42. McClay, D.R. and R.D. Fink. 1982. Sea urchin hyalin: Appearance and function in development. Dev. Biol. 92:285–293.PubMedCrossRefGoogle Scholar
  43. McClay, D.R. and R.E. Hausman. 1975. Specificity of cell adhesion: Differences between normal and hybrid sea urchin cells. Dev. Biol. 47:454–460.PubMedCrossRefGoogle Scholar
  44. McClay, D.R. and V. Matranga. 1986. On the role of calcium in the adhesion of embryonic sea urchin cells. Exp. Cell Res. 165:152–164.PubMedCrossRefGoogle Scholar
  45. McClay, D.R., G.M. Wessel and R.B. Marchase. 1981. Intercellular recognition: Quantitation of initial binding events. Proc. Natl. Acad. Sci. USA 78:4975–4979.PubMedCrossRefGoogle Scholar
  46. Moscona, A. 1956. Development of heterotypic combinations of dissociated embryonic chick cells. Proc. Soc. Exp. Biol. Med. 92:410–419.PubMedGoogle Scholar
  47. Moscona, A. and H. Moscona. 1952. Dissociation and aggregation of cells from organ rudiments of the early chick embryos. J. Anat. 86:287–301.PubMedGoogle Scholar
  48. Nelson, S.H. and D.R. McClay. 1988. Cell polarity in sea urchin embryos: Reorientation of cells occurs quickly in aggregates. Dev. Biol. 127:235–247.PubMedCrossRefGoogle Scholar
  49. Noll, H., M. Cervelo, T. Humphreys, B. Kuwasaki, and D. Adelson. 1985. Characterization of toposomes from sea urchin blastula cells: A cell organelle mediating cell adhesion and expressing positional information. Proc. Natl. Acad.Sci. USA82:8062–8066.PubMedCrossRefGoogle Scholar
  50. Noll, H, V. Matranga, D. Cascino, and L. Vittorelli. 1979. Reconstitution of membranes and embryonic development in dissociated blastula cells of the sea urchin by reinsertion of aggregation-promoting membrane proteins extracted with butanol. Proc. Natl. Acad. Sci. USA 72:288–292.CrossRefGoogle Scholar
  51. Nose, A, A. Nagafuchi, and M. Takeichi. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993–1001.PubMedCrossRefGoogle Scholar
  52. Rutishauser, U. 1989. Membrane apposition as a regulating parameter in cell-cell interactions, p. 137–150. In: The Assembly of the Nervous System. L. Landmesser (Ed.). Alan R. Liss, New York.Google Scholar
  53. Sheffield, J.B. and AA Moscona. 1989. Electron microscopic analysis of aggregation of embryonic cells: The structure and differentiation of aggregates of neural retina cells. Dev. Biol. 23:36–61.CrossRefGoogle Scholar
  54. Smith, J.C., J. Cooke, J.B.A. Green, G. Howes, and K. Symes. 1989. Inducing factors and the control of mesodermal pattern in Xenopus laevis. Development Suppl. 8:149–159.Google Scholar
  55. Spiegel, E., M. Burger, and M. Spiegel. 1980. Fibronectin in the developing sea urchin embryo. J. Cell Biol. 87:309–313.PubMedCrossRefGoogle Scholar
  56. Spiegel, E., M.M. Burger, and M. Spiegel. 1983. Fibronectin and laminin in the extracellular matrix and basement membrane of sea urchin embryos. Exp. Cell Res. 144:47–55.PubMedCrossRefGoogle Scholar
  57. Spiegel, M. and E. Spiegel. 1975. The reaggregation of dissociated embryonic sea urchin cells. Am. Zool. 15:583–606.Google Scholar
  58. Spray, D.C., M. Fujita, J.C. Saez, H. Choi, T. Watanabe, E. Hertzberg, L.C. Rosenberg, L.M. Reid. 1987. Proteoglycans and glycosaminoglycans induce gap junction synthesis and function in primary liver cultures. J. Cell Biol. 105:541–551.PubMedCrossRefGoogle Scholar
  59. Springer, T.A, M.L. Dustin, T.K. Kishimoto, and S.D. Marlin. 1987. LFA-1, CD2, and LFA-3 molecules: Cell adhesion receptors of the immune system. Annu. Rev.Immunol. 5:223–252.PubMedCrossRefGoogle Scholar
  60. Steinberg, M. 1970. Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J. Exp. Zool. 173:395–434.PubMedCrossRefGoogle Scholar
  61. Stephens, R.E. and R.E. Kane. 1970. Some properties of hyalin. J. Cell Biol. 44:611–617.PubMedCrossRefGoogle Scholar
  62. Takeichi, M. 1988. The cadherins: Cell-cell adhesion molecules controlling animal morphogenesis. Development 102:639–655.PubMedGoogle Scholar
  63. Takeichi, M., T. Atsumi, C. Yoshida, K. Uno, and T.S. Okada. 1981. Selective adhesion of embryonal carcinoma cells and differentiated cells by Ca2 + - dependent sites. Dev. Biol. 87:340–350.PubMedCrossRefGoogle Scholar
  64. Townes, P.L. and J. Holtfreter. 1955. Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128:53–120.CrossRefGoogle Scholar
  65. Trinkaus, J.P. 1984. Cells into Organs. Prentice-Hall, Englewood Cliffs, New Jersey.Google Scholar
  66. Wessel, G.M., R.B. Marchase, and D.R. McClay. 1984. Ontogeny of the basal lamina in the sea urchin embryo. Dev. Biol. 103:235–245.PubMedCrossRefGoogle Scholar
  67. Wessel, G.M. and D.R. McClay. 1987. Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix. Dev. Biol. 121:149–165.PubMedCrossRefGoogle Scholar
  68. Xu, T., I. Rebay, R.J. Fleming, T.N. Scottgale, and S. Artavanis-Tsakonas. 1990. The Notch locus and the genetic circuitry involved in early Drosophila neurogenesis. Genes Dev. 4:464–475.PubMedCrossRefGoogle Scholar
  69. Yamada, KM. and S.K. Akiyama. 1984. The interactions of cells with extracellular matrix components, p. 77–148. In: Cell Membranes, vol. 2. E. Elson, W. Frazier, and L. Glaser (Eds.). Plenum Press, New York.Google Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • David R. McClay
    • 1
  1. 1.Department of ZoologyDuke UniversityDurhamUSA

Personalised recommendations