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JOURNAL ARTICLES
Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis
R. Sharma-Kishore, J.G. White, E. Southgate, B. Podbilewicz
Development 1999 126: 691-699;

Summary

The genes involved in the inductive interactions that specify cell fates in the vulva of Caenorhabditis elegans are known in some detail. However, little is known about the morphogenesis of this organ. Using a combination of cell biological and anatomical approaches, we have determined a complete morphogenetic pathway of cellular events that lead to the formation of the vulva. These events include reproducible cell divisions, migrations, remodeling of adherens junctions, cell fusions and muscle attachments. In the course of these events, an epithelial channel comprising a stack of 7 toroidal cells is formed that connects the internal epithelium of the uterus with the external body epithelium, forming the vulva. Vulval muscles attach to the epithelial channel and the whole structure everts during the final molt. The mature vulva has rotational, two-fold symmetry. Using laser microsurgery, we found that the two halves of the vulva develop autonomously.

Reference

    1. Baird S. E.,
    2. Fitch D. A.,
    3. Kassem I. A. A.,
    4. Emmons S. W.
    (1991) Pattern formation in the nematode epidermis: determination of the arrangement of peripheral sense organs in the C. elegans male tail. Development 113, 515–526
    OpenUrlAbstract
    1. Banerjee U.,
    2. Zipursky S. L.
    (1990) The role of cell-cell interactions in the development of the Drosophila visual system. Neuron 4, 177–187
    OpenUrlCrossRefPubMedWeb of Science
    1. Bettinger J. C.,
    2. Euling S.,
    3. Rougvie A. E.
    (1997) The terminal differentiation factor LIN-29 is required for proper vulval morphogenesis and egg laying in Caenorhabditis elegans. Development 124, 4333–4342
    OpenUrlAbstract
    1. Brenner S.
    (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71–94
    OpenUrlAbstract/FREE Full Text
    1. Cross J. C.,
    2. Werb Z.,
    3. Fisher S. J.
    (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508–1518
    OpenUrlAbstract/FREE Full Text
    1. Eizinger A.,
    2. Sommer R. J.
    (1997) The homeotic gene lin-39 and the evolution of nematode epidermal cell fates. Science 278, 452–454
    OpenUrlAbstract/FREE Full Text
    1. Finney M.,
    2. Ruvkun G.
    (1990) The unc −86 gene product couples cell lineage and cell identity in C. elegans. Cell 63, 895–905
    OpenUrlCrossRefPubMedWeb of Science
    1. Francis G. R.,
    2. Waterston R. H.
    (1991) Muscle cell attachment in Caenorhabditis elegans. J. Cell Biol 114, 465–479
    OpenUrlAbstract/FREE Full Text
    1. Freeman M.
    (1997) Cell determination strategies in the Drosophila eye. Development 124, 261–370
    OpenUrlAbstract
    1. Grawe F.,
    2. Wodarz A.,
    3. Lee B.,
    4. Knust E.,
    5. Skaer H.
    (1996) The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122, 951–959
    OpenUrlAbstract
    1. Greenwald I.,
    2. Rubin G. M.
    (1992) Making a difference: the role of cell-cell interactions in establishing separate identities for equivalent cells. Cell 68, 271–281
    OpenUrlCrossRefPubMedWeb of Science
    1. Greenwald I. S.,
    2. Sternberg P. W.,
    3. Horvitz H. R.
    (1983) The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34, 434–444
    OpenUrl
    1. Hardin J.
    (1989) Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev. Biol 136, 430–445
    OpenUrlCrossRefPubMed
    1. Herman R. K.,
    2. Hedgecock E. M.
    (1990) Limitations of the size of the vulval primordium of Caenorhabditis elegans by lin −15 expression in surrounding hyopodermis. Nature 348, 169–171
    OpenUrlCrossRefPubMed
    1. Herman T.,
    2. Horvitz H. R.
    (1997) Mutations that perturb vulval invagination in C. elegans. Cold Spring Harb. Symp. Quant. Biol 62, 353–359
    OpenUrlAbstract/FREE Full Text
    1. Hernandez L. D.,
    2. Hoffman L. R.,
    3. Wolfsberg T. G.,
    4. White J. M.
    (1996) Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol 12, 627–661
    OpenUrlCrossRefPubMedWeb of Science
    1. Horvitz H. R.,
    2. Sternberg P. W.
    (1991) Multiple intercellular signalling systems control the development of the Caenorhabditis elegans vulva. Nature 351, 535–541
    OpenUrlCrossRefPubMed
    1. Huang T. W.,
    2. Green A. D.,
    3. Beattie C. W.,
    4. Das Gupta T. K.
    (1993) Monocyte-macrophage lineage of giant cell tumor of bone. Cancer 71, 1751–1760
    OpenUrlCrossRefPubMed
    1. Kimble J.
    (1981) Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegans. Dev. Biol 87, 286–300
    OpenUrlCrossRefPubMedWeb of Science
    1. Kornfeld K.
    (1997) Vulval development in Caenorhabditis elegans. Trends Genet 13, 55–61
    OpenUrlCrossRefPubMedWeb of Science
    1. Maloof J. N.,
    2. Kenyon C.
    (1998) The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development 125, 181–190
    OpenUrlAbstract
    1. Newman A. P.,
    2. White J. G.,
    3. Sternberg P. W.
    (1996) Morphogenesis of the C. elegans hermaphrodite uterus. Development 122, 3617–3626
    OpenUrlAbstract
    1. Podbilewicz B.
    (1996) ADM-1, a protein with metalloprotease-and disintegrin-like domains, is expressed in syncytial organs, sperm and sheath cells of sensory organs in C. elegans. Mol. Biol. Cell 7, 1877–1893
    OpenUrlAbstract/FREE Full Text
    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. Reddi A. H.
    (1994) Bone and cartilage differentiation. Curr. Opin. Genet. Dev 4, 737–744
    OpenUrlCrossRefPubMed
    1. Saxen L.,
    2. Sariola H.
    (1987) Early organogenesis of the kidney. Pediatr. Nephrol 1, 385–392
    OpenUrlCrossRefPubMedWeb of Science
    1. Seydoux G.,
    2. Savage C.,
    3. Greenwald I.
    (1993) Isolation and characterization of mutations causing abnormal eversion of the vulva in Caenorhabditis elegans. Dev. Biol 157, 423–436
    OpenUrlCrossRefPubMedWeb of Science
    1. Sitar G.,
    2. Bianchi A. S.,
    3. Rosti V.,
    4. Shaskin P.,
    5. Blago R.,
    6. Santamaria L.,
    7. Ascari E.
    (1994) Giant cell formation in Hodgkin's disease. Res. Immunol 145, 499–515
    OpenUrlCrossRefPubMed
    1. Sommer R. J.
    (1997) Evolutionary changes of developmental mechanisms in the absence of cell lineage alterations during vulva formation in the Diplogastridae (Nematoda). Development 124, 243–251
    OpenUrlAbstract
    1. Sternberg P. W.,
    2. Horvitz H. R.
    (1986) Pattern formation during vulval development in C. elegans. Cell 14, 761–772
    OpenUrlCrossRef
    1. Sternberg P. W.,
    2. Horvitz H. R.
    (1989) The combined action of two intercellular signaling pathways specifies three cell fates during vulval induction in C. elegans. Cell 58, 679–693
    OpenUrlCrossRefPubMedWeb of Science
    1. Sulston J. E.,
    2. Horvitz H. R.
    (1977) Postembryonic cell lineages of the nematode Caenorhabditis elegans. Dev. Biol 56, 110–156
    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. Thesleff I.,
    2. Nieminen P.
    (1996) Tooth morphogenesis and cell differentiation. Curr. Opin. Cell Biol 8, 844–850
    OpenUrlCrossRefPubMedWeb of Science
    1. Wang B. B.,
    2. M.M. M.-I.,
    3. Austin J.,
    4. Robinson N. T.,
    5. Chisholm A.,
    6. Kenyon C.
    (1993) A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74, 29–42
    OpenUrlCrossRefPubMedWeb of Science
    1. White J. G.,
    2. Southgate E.,
    3. Thomson J. N.,
    4. Brenner S.
    (1986) The structure of the nervous system of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci 314, 1–340
    OpenUrlCrossRef
    1. Yap A. S.,
    2. Brieher W. M.,
    3. Gumbiner B. M.
    (1997) Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol 13, 119–146
    OpenUrlCrossRefPubMedWeb of Science
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JOURNAL ARTICLES
Formation of the vulva in Caenorhabditis elegans: a paradigm for organogenesis
R. Sharma-Kishore, J.G. White, E. Southgate, B. Podbilewicz
Development 1999 126: 691-699;
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