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JOURNAL ARTICLES
Dynamics of thin filopodia during sea urchin gastrulation
J. Miller, S.E. Fraser, D. McClay
Development 1995 121: 2501-2511;

Summary

At gastrulation in the sea urchin embryo, a dramatic rearrangement of cells establishes the three germ layers of the organism. Experiments have revealed a number of cell interactions at this stage that transfer patterning information from cell to cell. Of particular significance, primary mesenchyme cells, which are responsible for production of the embryonic skeleton, have been shown to obtain extensive positional information from the embryonic ectoderm. In the present study, high resolution Nomarski imaging reveals the presence of very thin filopodia (02-0.4 micron in diameter) extending from primary mesenchyme cells as well as from ectodermal and secondary mesenchyme cells. These thin filopodia sometimes extend to more than 80 microns in length and show average growth and retraction rates of nearly 10 microns/minute. The filopodia are highly dynamic, rapidly changing from extension to resorption; frequently, the resorption changes to resumption of assembly. The behavior, location and timing of active thin filopodial movements does not correlate with cell locomotion; instead, there is a strong correlation suggesting their involvement in cell-cell interactions associated with signaling and patterning at gastrulation. Nickel-treatment, which is known to create a patterning defect in skeletogenesis due to alterations in the ectoderm, alters the normal position-dependent differences in the thin filopodia. The effect is present in recombinant embryos in which the ectoderm alone was treated with nickel, and is absent in recombinant embryos in which only the primary mesenchyme cells were treated, suggesting that the filopodial length is substratum dependent rather than being primary mesenchyme cell autonomous. The thin filopodia provide a means by which cells can contact others several cell diameters away, suggesting that some of the signaling previously thought to be mediated by diffusible signals may instead by the result of direct receptor-ligand interactions between cell membranes.

Reference

    1. Armstrong N.,
    2. Hardin J.,
    3. McClay D. R.
    (1993) Cell-cell interactions regulate skeleton formation in the sea urchin embryo. Development 119, 833–840
    OpenUrlAbstract/FREE Full Text
    1. Armstrong N.,
    2. McClay D. R.
    (1994) Skeletal pattern is specified autonomously by the primary mesenchyme cells in sea urchin embryos. Dev. Biol 162, 329–338
    OpenUrlCrossRefPubMedWeb of Science
    1. Caudy M.,
    2. Bentley D.
    (1986) Pioneer growth cone steering along a series of neuronal and non-neuronal cues of different affinities. J. Neurosci 6, 1781–1795
    OpenUrlAbstract
    1. Davenport R. W.,
    2. Dou P.,
    3. Rehder V.,
    4. Kater S. B.
    (1993) A sensory role for neuronal growth cone filopodia. Nature 361, 721–724
    OpenUrlCrossRefPubMed
    1. Ettensohn C. A.,
    2. McClay D. R.
    (1986) The regulation of primary mesenchyme cell migration in the sea urchin embryo: transplantations of cells and latex beads. Dev. Biol 117, 380–391
    OpenUrlCrossRefPubMedWeb of Science
    1. Ettensohn C. A.,
    2. McClay D. R.
    (1988) Cell lineage conversion in the sea urchin embryo. Dev. Biol 125, 396–409
    OpenUrlCrossRefPubMedWeb of Science
    1. Ettensohn C. A.
    (1990) Cell interactions in the sea urchin embryo studied by fluorescence photoablation. Science 248, 1115–1118
    OpenUrlAbstract/FREE Full Text
    1. Ettensohn C. A.
    (1990) The regulation of primary mesenchyme cell patterning. Dev. Biol 140, 261–271
    OpenUrlCrossRefPubMed
    1. Gibbins J. R.,
    2. Tilney L. G.,
    3. Porter K. R.
    (1969) Microtubules in the formation and development of the primary mesenchyme in Arbacia punctulata. I. The distribution of microtubules. J. Cell Biol 41, 201–226
    OpenUrlAbstract/FREE Full Text
    1. Gustafson T.,
    2. Wolpert L.
    (1961) Studies on the cellular basis of morphogenesis in the sea urchin embryo; directed movements of primary mesenchyme cells in normal and vegetalized larvae. Exp. Cell Res 24, 64–79
    OpenUrlCrossRefPubMedWeb of Science
    1. Gustafson T.
    (1963) Cellular mechanisms in the morphogenesis of the seaurchin embryo. Cell contacts within the ectoderm and between mesenchyme and ectoderm cells. Exp. Cell Res 32, 570–589
    OpenUrlCrossRefPubMed
    1. Gustafson T.,
    2. Wolpert L.
    (1967) Cellular movement and contact in sea urchin morphogenesis. Biol. Rev 42, 442–498
    OpenUrlPubMed
    1. Hardin J. D.,
    2. Cheng L. Y.
    (1986) The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev. Biol 115, 490–501
    OpenUrlCrossRefWeb of Science
    1. Hardin J. D.
    (1987) Archenteron elongation in the sea urchin embryo is a microtubule-independent process. Dev. Biol 121, 253–262
    OpenUrlCrossRefPubMed
    1. Hardin J.
    (1988) The role of secondary mesenchyme cells during sea urchin gastrulation studied by laser ablation. Development 103, 317–324
    OpenUrlAbstract
    1. Hardin J.,
    2. Coffman J. A.,
    3. Black S. D.,
    4. McClay D. R.
    (1992) Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development 116, 671–685
    OpenUrlAbstract
    1. Hardin J.,
    2. McClay D. R.
    (1990) Target recognition by the archenteron during sea urchin gastrulation. Dev. Biol 142, 86–102
    OpenUrlCrossRefPubMedWeb of Science
    1. Karp G. C.,
    2. Solursh M.
    (1985) Dynamic activity of the filopodia of sea urchin embryonic cells and their role in directed migration of the primary mesenchyme in vitro. Dev. Biol 112, 276–283
    OpenUrlCrossRefPubMed
    1. Leaf D. S.,
    2. Anstrom J. A.,
    3. Chin J. E.,
    4. Harkey M. A.,
    5. Raff R. A.
    (1987) Antibodies to a fusion protein identify a cDNA clone encoding msp130, a primary mesenchyme-specific cell surface protein of the sea urchin embryo. Dev. Biol 121, 29–40
    OpenUrlCrossRefPubMedWeb of Science
    1. Lemmon V.,
    2. Burden S. M.,
    3. Payne H. R.,
    4. Elmslie G. W.,
    5. Hlavin S.
    (1992) Neurite growth on different substrates: permissive versus instructive influences and the role of adhesive strength. J. Neurosci 12, 818–826
    OpenUrlAbstract
    1. Marsh L.,
    2. Letourneau P. C.
    (1984) Growth of neurites without filopodial or lamellapodial activity in the presence of cytochalasin B. J. Cell Biol 99, 2041–2047
    OpenUrlAbstract/FREE Full Text
    1. McClay D. R.,
    2. Armstrong N. A.,
    3. Hardin J.
    (1992) Pattern formation during gastrulation in the sea urchin embryo. Development 1992, 33–41
    1. Myers P. Z.,
    2. Bastiani M. J.
    (1993) Growth cone dynamics during the migration of an identified commisural growth cone. J. Neurosci 13, 127–143
    OpenUrlAbstract
    1. Oakley R. A.,
    2. Tosney K. W.
    (1993) Contact-mediated mechanisms of motor axon segmentation. J. Neurosci 13, 3773–3792
    OpenUrlAbstract
    1. Sheetz M. P.,
    2. Baumrind N. L.,
    3. Wayne D. B.,
    4. Pearlman A. L.
    (1990) Concentrations of membrane antigens by forward transport and trapping in neuronal growth cones. Cell 61, 231–241
    OpenUrlCrossRefPubMedWeb of Science
    1. Sheetz M. P.,
    2. Wayne D. B.,
    3. Pearlman A. L.
    (1992) Extension of filopodia by motor-dependent actin assembly. Cell Motil.Cytoskeleton 22, 160–169
    OpenUrlCrossRefPubMedWeb of Science
    1. Taghert P. H.,
    2. Bastiani M. J.,
    3. Ho R. K.,
    4. Goodman C. S.
    (1982) Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to lucifer yellow. Dev. Biol 94, 391–399
    OpenUrlCrossRefPubMedWeb of Science
    1. Wessel G. M.,
    2. McClay D. R.
    (1987) Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix. Dev. Biol 121, 149–165
    OpenUrlCrossRefPubMed
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JOURNAL ARTICLES
Dynamics of thin filopodia during sea urchin gastrulation
J. Miller, S.E. Fraser, D. McClay
Development 1995 121: 2501-2511;
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