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JOURNAL ARTICLES
An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis
E.M. Williams-Masson, A.N. Malik, J. Hardin
Development 1997 124: 2889-2901;

Summary

The epiboly of the Caenorhabditis elegans hypodermis involves the bilateral spreading of a thin epithelial sheet from the dorsal side around the embryo to meet at the ventral midline in a process known as ventral enclosure. We present evidence that ventral enclosure occurs in two major steps. The initial migration of the hypodermis is led by a quartet of cells, which exhibit protrusive activity at their medial tips and are required to pull the hypodermis around the equator of the embryo. These cells display actin-rich filopodia and treatment with cytochalasin D immediately halts ventral enclosure, as does laser inactivation of all four cells. Once the quartet of cells has migrated around the equator of the embryo and approaches the ventral midline, the remainder of the leading edge becomes visible on the ventral surface and exhibits a localization of actin microfilaments along the free edges of the cells, forming an actin ring. Cytochalasin D and laser inactivation block ventral enclosure at this later stage as well and, based upon phalloidin staining, we propose that the second half of enclosure is dependent upon a purse string mechanism, in which the actin ring contracts and pulls together the edges of the hypodermal sheet at the ventral midline. The ventral cells then form junctions with their contralateral neighbors to complete ventral enclosure.

REFERENCES

    1. Avery L.,
    2. Horvitz H. R.
    (1989) Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3, 473–485
    OpenUrlCrossRefPubMedWeb of Science
    1. Bement W. M.,
    2. Forscher P.,
    3. Mooseker M. S.
    (1993) A novel cytoskeletal structure involved in purse string wound closure and cell polarity maintenance. J. Cell Biol 121, 565–578
    OpenUrlAbstract/FREE Full Text
    1. Betchaku T.,
    2. Trinkaus J. P.
    (1978) Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of Fundulus before and during epiboly. J. Exp. Zool 206, 381–426
    OpenUrlCrossRefPubMedWeb of Science
    1. Costa M.,
    2. Draper B. W.,
    3. Priess J. R.
    (1997) The role of actin filaments in patterning the Caenorhabditis elegans cuticle. Dev. Biol 184, 373–384
    OpenUrlCrossRefPubMed
    1. Downie J. R.,
    2. Pegrum S. M.
    (1971) Organisation of the chick blastoderm edge. J. Embryol. Exp. Morph 26, 623–635
    OpenUrlPubMed
    1. Fleig R.,
    2. Sander K.
    (1988) Honeybee morphogenesis: embryonic cell movements that shape the larval body. Development 103, 525–534
    OpenUrlAbstract
    1. Gabbiani G.,
    2. Chaponnier C.,
    3. Huttner I.
    (1978) Cytoplasmic filaments and gap junctions in epithelial cells and myofibroblasts during wound healing. J. Cell Biol 76, 561–568
    OpenUrlAbstract/FREE Full Text
    1. Hergott G. J.,
    2. Sandig M.,
    3. Kalnins V. I.
    (1989) Cytoskeleton organization of migrating retinal pigment epithelial cells during wound healing in organ culture. Cell Motil. Cytoskeleton 13, 83–93
    OpenUrlCrossRefPubMedWeb of Science
    1. Keller R. E.,
    2. Trinkaus J. P.
    (1987) Rearrangement of enveloping layer cells without disruption of the epithelial permeability barrier as a factor in Fundulus epiboly. Dev. Biol 120, 12–24
    OpenUrlCrossRefPubMed
    1. Kramer J.
    (1994) Genetic analysis of extracellular matrix in C. elegans. Ann. Rev. Genetics 28, 95–116
    OpenUrlPubMed
    1. Martin P.,
    2. Lewis J.
    (1992) Actin cables and epidermal movement in embryonic wound healing. Nature 360, 179–183
    OpenUrlCrossRefPubMed
    1. McCormack S. A.,
    2. Viar M. J.,
    3. Johnson L. R.
    (1992) Migration of IEC-6 cells: a model for mucosal healing. Am. J. Physiol 263, 426–435
    OpenUrl
    1. Nusrat A.,
    2. Delp C.,
    3. Madara J. L.
    (1992) Intestinal epithelial restitution. Characterization of a cell culture model and mapping of cytoskeletal elements in migrating cells. J. Clin. Invest 89, 1501–1511
    1. Podbilewicz B.,
    2. White J. G.
    (1994) Cell fusions in the developing epithelia of C. elegans. Dev. Biol 161, 408–424
    OpenUrlCrossRefPubMedWeb of Science
    1. Priess J. R.,
    2. Hirsh D. I.
    (1986) Caenorhabditis elegans morphogenesis: The role of the cytoskeleton in elongation of the embryo. Dev. Biol 117, 156–173
    OpenUrlCrossRefPubMedWeb of Science
    1. Radice G. P.
    (1980) The spreading of epithelial cells during wound closure in Xenopus larvae. Dev. Biol 76, 26–46
    OpenUrlCrossRefPubMed
    1. Ris H.
    (1985) The cytoplasmic filament system in critical-point dried whole mounts and plastic-embedded sections. J. Cell Biol 100, 1474–1487
    OpenUrlAbstract/FREE Full Text
    1. Shelton C. A.,
    2. Bowerman B.
    (1996) Time-dependent responses to glp-1 -mediated inductions in early C. elegans embryos. Development 122, 2043–2050
    OpenUrlAbstract
    1. Sulston J. E.,
    2. Schierenberg E.,
    3. White J. G.,
    4. Thomson J. N.
    (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol 100, 64–119
    OpenUrlCrossRefPubMedWeb of Science
    1. Sulston J. E.,
    2. White J. G.
    (1980) Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev. Biol 78, 577–597
    OpenUrlCrossRefPubMedWeb of Science
    1. Takeuchi S.
    (1979) Wound healing in the cornea of the chick embryo IV. Promotion of the migratory activity of isolated corneal epithelium in culture by the application of tension. Dev. Biol 70, 232–240
    OpenUrlCrossRefPubMed
    1. Takeuchi S.
    (1983) Wound healing in the cornea of the chick embryo V. An observation and quantitative assessment of the cell shapes in isolated corneal epithelium during spreading in vitro. Cell Tissue Res 229, 109–127
    OpenUrlPubMed
    1. Young P. E.,
    2. Richman A. M.,
    3. Ketchum A. S.,
    4. Kiehart D. P.
    (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev 7, 29–41
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis
E.M. Williams-Masson, A.N. Malik, J. Hardin
Development 1997 124: 2889-2901;
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