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Communication compartments in the axial mesoderm of the chick embryo

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Summary

Intracellular microinjection of the fluorescent tracer Lucifer Yellow into mesoderm cells along the rostrocaudal axis of the early chick embryo has revealed compartments where the intercellular diffusion of dye, presumably via gap junctions, is restricted at the borders between groups of cells. Cells in the segmental plate were dye-coupled, as were cells forming the epithelial somites. However, dye-coupling was not observed between different somites, nor was it observed between the outer epithelial cells and the cells in the somitocoele. On dispersal of the somite, dermatome cells were dye-coupled. However, sclerotome cells were found to be divided into rostral and caudal compartments separated by a group of cells bordering the intrasclerotomal fissure (of von Ebner) that also exhibited dye-coupling, restricted primarily to cells along the fissure. Some of these compartment borders can be accounted for by the presence of a morphological barrier which reduces cell-cell contact, but others are more difficult to explain, as there appears to be extensive cell-cell contact across the border. This would be analogous to some compartments found in insects. Some of the compartments also have borders similar to those described by cell lineage studies. The results also indicate that dye-coupling becomes restricted in a spatial and temporal manner as the mesodermal cells mature.

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References

  • Bagnall K, Sanders E (1989) The binding pattern of peanut lectin associated with sclerotome migration and the formation of the vertebral axis in the chick embryo. Anat Embryol 180:505–513

    Google Scholar 

  • Bagnall K, Higgins S, Sanders E (1988) The contribution made by a single somite to the vertebral column: experimental evidence in support of resegmentation using the chick-quail chimaera model. Development 103:69–85

    CAS  PubMed  Google Scholar 

  • Bagnall K, Higgins S, Sanders E (1989) The contribution made by cells from a single somite to tissues within a body segment and assessment of their integration with similar cells from adjacent segments. Development 107:931–943

    CAS  PubMed  Google Scholar 

  • Bellairs R, Breathnach A, Gross M (1975) Freeze-fracture replication of junctional complexes in unincubated and incubated chick embryos. Cell Tissue Res 162:235–252

    Google Scholar 

  • Bennett M, Spray D, Harris A (1981) Electrical coupling in development. Am Zool 21:413–427

    Google Scholar 

  • Bennett M, Barrio L, Bargiello T, Spray D, Hertzberg E, Saez J (1991) Gap junctions: new tools, new answers, new questions. Neuron 6:305–320

    Google Scholar 

  • Berdan R (1987) Intercellular communication in arthropods. Biophysical, ultrastructural, and biochemical approaches. In: De Mello W (ed) Cell-to-cell communication. Plenum Press, New York, pp 299–370

    Google Scholar 

  • Blennerhassett M, Caveney S (1984) Separation of developmental compartments by a cell type with reduced junctional permeability. Nature 309:361–364

    Google Scholar 

  • Caveney S (1985) The role of gap junctions in development. Ann Rev Physiol 47:319–335

    Google Scholar 

  • Crick F, Lawrence P (1975) Compartments and polyclones in insect development. Science 189:340–347

    Google Scholar 

  • Fraser S, Green C, Bode H, Gilula N (1987) Selective disruption of gap junctional communication interferes with a patterning process in hydra. Science 237:49–55

    Google Scholar 

  • Fraser S, Keynes R, Lumsden S (1990) Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344:431–435

    Article  CAS  PubMed  Google Scholar 

  • Furshpan E, Potter D (1968) Low resistance junctions between cells in embryos and tissue culture. Curr Top Dev Biol 3:95–127

    Google Scholar 

  • Garcia-Bellido A, Ripoll P, Morata G (1973) Developmental compartmentalisation of the wing disc of Drosophila. Nature 245:251–253

    Google Scholar 

  • Garcia-Bellido A, Ripoll P, Morata G (1976) Developmental compartmentalization in the dorsal mesothoracic disc of Drosophila. Dev Biol 48:132–147

    Google Scholar 

  • Gaunt S (1987) Homoeobox gene Hox 1.5 expression in mouse embryos: earliest detection by in situ hybridization is during gastrulation. Development 101:51–60

    Google Scholar 

  • Gaunt S (1988) Mouse homeobox gene transcripts occupy different overlapping domains in embryonic germ layers and organs: a comparison of Hox 3.1 and Hox 1.5. Development 103:135–144

    Google Scholar 

  • Gaunt S, Sharpe P, Duboule D (1988) Spatially restricted domains of homeo-gene transcripts in mouse embryos: relation to a segmented body plan. Development 104 (Suppl I): 169–179

    Google Scholar 

  • Guthrie S (1984) Patterns of junctional communication in the early amphibian embryo. Nature 311:149–151

    Google Scholar 

  • Hamburger V, Hamilton H (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    Google Scholar 

  • Kalimi G, Lo C (1988) Communication compartments in the gastrulating mouse embryo. J Cell Biol 107:241–255

    Google Scholar 

  • Kanno Y, Lowenstein W (1966) Cell-to-cell passage of large molecules. Nature 212:629–630

    Google Scholar 

  • Keynes R, Stern C (1984) Segmentation in the vertebrate nervous system. Nature 310:786–789

    CAS  PubMed  Google Scholar 

  • Lawrence P (1973) Maintenance of boundaries between developing organs in insects. Nature 242:31–32

    Google Scholar 

  • Lawrence P (1990) Compartments in vertebrates. Nature 344:382–383

    Google Scholar 

  • Lo C, Gilula N (1979a) Gap junctional communication in the preimplantation mouse embryo. Cell 18:399–409

    Google Scholar 

  • Lo C, Gilula N (1979b) Gap junctional communication in the post-implantation mouse embryo. Cell 18:411–422

    Google Scholar 

  • Lumsden A, Keynes R (1989) Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424–429

    Google Scholar 

  • Mackie E, Tucker R, Halfter W, Chiquet-Ehrismann R, Epperlein H (1988) The distribution of tenascin coincides with pathways of neural crest cell migration. Development 102:237–250

    CAS  PubMed  Google Scholar 

  • Newgreen D, Erickson C (1986) The migration of neural crest cells. Int Rev Cytol 103:89–145

    Google Scholar 

  • O'Brochta D, Bryant P (1985) A zone of non-proliferating cells at a lineage restriction boundary in Drosophila. Nature 313:138–141

    Google Scholar 

  • Patel N, Kornberg T, Goodman C (1989) Expression of Engrailed during segmentation in grasshopper and crayfish. Development 107:201–212

    CAS  PubMed  Google Scholar 

  • Revel J-P, Yip P, Chang L (1973) Cell junctions in the early chick — embryo freeze-etch study. Dev Biol 35:302–317

    Google Scholar 

  • Robertis E de, Oliver G, Wright C (1990) Homeobox genes and the vertebrate body plan. Sci Am 263:46–52

    Google Scholar 

  • Shaner D (1985) In development of the human vertebral column, M Sc Thesis, University of Alberta

  • Sheridan J (1968) Electrophysiological evidence for low-resistance intercellular junctions in the early chick embryo. J Cell Biol 37:650–659

    Google Scholar 

  • Solursh M, Fisher M, Meier S, Singley C (1979) The role of extracellular matrix in the formation of the sclerotome. J Embryol Exp Morphol 54:75–98

    Google Scholar 

  • Stern C, Keynes R (1986) Cell lineage and the formation and maintenance of half somites. In: Bellairs R, Ede D, Lash J (eds) Somites in developing embryos, Nato ISI series, Plenum Press, London, pp 147–160

    Google Scholar 

  • Stern C, Keynes R (1987) Interactions between somite cells: the formation and maintenance of segment boundaries in the chick embryo. Development 99:261–272

    Google Scholar 

  • Stern C, Sisodaya S, Keynes R (1986) Interactions between neurites and somite cells: inhibition and stimulation of nerve growth in the chick embryo. J Embryol Exp Morphol 91:209–226

    Google Scholar 

  • Tan S, Crossin K, Hoffman S, Edelman G (1987) Asymmetric expression in somites of cytotactin and its proteoglycan ligand is correlated with neural crest distribution. Proc Natl Acad Sci USA 84:7977–7981

    Google Scholar 

  • Trelstad R, Hay E, Revel J-P (1967) Cell contact during early morphogenesis in the chick embryo. Dev Biol 16:78–106

    Google Scholar 

  • Warner A (1988) The gap junction. J Cell Sci 89:1–7

    Google Scholar 

  • Warner A, Lawrence P (1973) Electrical coupling across developmental boundaries in insect epidermis. Nature 245:47–48

    Google Scholar 

  • Warner A, Lawrence P (1982) Permeability of gap junctions at the segmental border in insect epidermis. Cell 28:243–252

    Google Scholar 

  • Weir M, Lo C (1982) Gap junctional communication compartments in the Drosophila wing disk. Proc Natl Acad Sci USA 79:3232–3235

    Google Scholar 

  • Weir M, Lo C (1984) Gap junctional communication compartments in the Drosophila wing imaginal disk. Dev Biol 102:130–146

    Google Scholar 

Download references

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Bagnall, K.M., Sanders, E.J. & Berdan, R.C. Communication compartments in the axial mesoderm of the chick embryo. Anat Embryol 186, 195–204 (1992). https://doi.org/10.1007/BF00174957

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