In vivo Analysis of Convergent Cell Movements in The Germ Ring of Fundulus
Carbon marking shows that the cells of the germ ring (GR) converge toward and enter the embryonic shield (ES). Interestingly, marks closer to the ES move faster. Cells lateral to the ES (in the prospective proximal yolk sac) also move into the ES.
Analysis of video tapes made of converging cells with DIC optics leads to the following conclusions. All cells of the GR engage in translocation almost all the time and their net directionality is always toward the ES, which they eventually join, contributing to its steady augmentation. But no cells move in a direct line toward the ES. All meander considerably. Their mean net rate during one 80 min period was 1.4 µm/min ± 0.36 and their mean total rate was 1.9 µm/min ± 0.35. GR cells that are near the ES move toward it at a higher net rate than those farther away. In consequence, their net trajectories are significantly longer. Since total cell movement and amount of motile quiescence are the same near and far, the greater net trajectory of the nearer cells must be due to less meandering. This suggests that there are exogenous factors that promote directionality toward the ES and that they operate more efficiently close to it. Cells in the prospective yolk sac adjacent to the ES also show net movement toward the ES. However, this movement is much less efficient than in the GR proper. Directional forces are apparently stronger in the marginal region of the blastoderm, namely the germ ring.
Converging deep cells in the GR move by both filolamellipodia and, much less frequently, by blebs. There is very little individual cell movement, and, at any moment, almost all cells are in contact with other cells in moving cell clusters. This is by far the dominant mode of movement. Clusters vary constantly in size, continually aggregating with other cells and other clusters and splitting, but always showing net movement toward the ES. Both moving cell clusters and individual filolamellipodial cells show protrusive activity solely on their free borders, which ceases whenever their surface makes contact with another cell surface. Clearly, they show contact paralysis or contact inhibition of cell movement. Nevertheless, they move and do so directionally to boot. The reason for this, we think, is that they are almost always members of moving cell clusters. As such, much of their movement is passive. Movement of clusters toward the ES is presumably due to directional factors in their environment which favor protrusive activity at their proximal margins. Both kinds of cells show intercalation or invasive activity frequently during convergence. But, consistent with their contact-inhibiting properties, filolamellipodial cells intercalate only when neighboring cells have separated enough to provide free space into which they can move. Cells that move by blebbing locomotion are not contact inhibiting and do not require free space for intercalation. Cells continue to divide during convergence at an apparently steady rate—e.g., 12% of cells observed during one 80 minute period. Although this temporarily arrests their movement, the daughter cells soon join in the mass convergent movement, usually in 2 min or less after completion of cytokinesis.
KeywordsCell Movement Cell Cluster Contact Inhibition Deep Cell Yolk Syncytial Layer
Unable to display preview. Download preview PDF.
- Ballard, W.W. 1973. Morphogenetic movements in Salmo gairdneri Richardson. J. Exp.Zool. 184:381–426.Google Scholar
- Erickson, C.A. 1985. Morphogenesis of the neural crest, p. 481–543. In:Developmental Biology: A Comprehensive Synthesis. Vol. 2, The Cellular Basis of Morphogenesis. L.W. Browder (Ed.). Plenum Press, New York.Google Scholar
- 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
- Keller, R.E., J. Shih, and P. Wilson. 1991. Cell motility and regional interactions controlling amphibian gastrulation. p. 101–120. In: Gastrulation: Movements, Patterns, and Molecules. R. Keller, W.H. Clark, Jr., F. Griffin (Eds.). Plenum Press, New York.Google Scholar
- Kolega, J. 1981.The movement of cell clusters in vitro: Morphology and directionality. J. Cell Set 49:15–22.Google Scholar
- Pasteels, J. 1936. Etudes sur la gastrulation des vertébrés méroblastiques. I. Téléostéens. Arch. Biol. 47:205–308.Google Scholar
- Trinkaus, J.P. 1967. Procurement, maintenance and use of Fundulus eggs. p. 113–122. In: Methods in Developmental Biology. F.H. Wilt and N.K. Wessells (Eds.). Crowell, New York.Google Scholar
- Trinkaus, J.P. 1980. Formation of protrusions of the cell surface during tissue cell movement, p. 887–906. In: Tumor Cell Surfaces and Malignancy. R.O. Hynes and C.F. Fox (Eds.). Alan R. Liss, New York.Google Scholar
- Trinkaus, J.P. 1984a. Cells into Organs, The Forces that Shape the Embryo, p. 543. Prentice-Hall, Englewood Cliffs, N.J.Google Scholar
- Trinkaus, J.P. 1984b. Mechanism of Fundulus epiboly—A current view. Am. Zool 24:673–688.Google Scholar
- Trinkaus, J.P. 1988b. Directional cell movement during early development of the teleost Blennius pholis. II. Transformation of the cells of epithelial clusters into dendritic melanocytes, their dissociation from each other, and their migration to and invasion of the pectoral fin buds. J. Exp. Zool. 248:55–72.PubMedCrossRefGoogle Scholar
- Trinkaus, J.P., M. Trinkaus, and R.D. Fink. 1992. On the convergent cell movements of gastrulation in Fundulus. J. Exp. Zool, In press.Google Scholar
- Wood, A. and L.P.M. Timmermans. 1988. Teleost epiboly: a reassessment of deep cell movement in the germ ring. Development 102:575–585.Google Scholar