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Cell surface localisation and stability of uvomorulin during early mouse development

Published online by Cambridge University Press:  26 September 2008

Lesley Clayton*
Affiliation:
Department of Anatomy, University of Cambridge, Cambridge, UK.
Siân V. Stinchcombe
Affiliation:
Department of Anatomy, University of Cambridge, Cambridge, UK.
Martin H. Johnson
Affiliation:
Department of Anatomy, University of Cambridge, Cambridge, UK.
*
Dr L. Clayton, Department of Anatomy, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK. Tel: 0223 333755. Fax: 0223 333786.

Extract

We have examined immunocytochemically the subcellular distribution of the cell adhesion molecule uvomorulin in cleavage stage mouse embryos using conventional and confocal microscopy, under a range of detergent extraction and fixation regimes. Only traces of uvomorulin were detectable on the surface of unfertilised oocytes, whereas between 6 and 11 h after activation detergent-resistant surface expression was evident. This shift correlates with previously demonstrated changes in the pattern of synthesis and accumulation of uvomorulin from precursor state in unfertilised oocytes to mature protein after fertilisation. Embryos at subsequent stages up to the 8-cell stage exhibited a uniform distribution of uvomorulin on free surfaces and its concentration in regions of contact between blastomeres. At the 8-cell stage, during compaction, there was increased intercellular adhesion with concomitant accumulation of uvomorulin at intercellular contacts, whilst free surface uvomorulin was reduced and became relatively more susceptible to detergent extraction. When compact 8-cell embryos were decompacted in calcium-free medium, uvomorulin at contacts decreased while free surface and cytoplasmic staining increased. Blastomeres disaggregated from 4- and 8-cell embryos showed traces or ‘footprints’ of anti-uvomorulin staining in regions previously in apposition. These footprints disappeared over 45–60 min, during which time uvomorulin distribution became uniform. Possible mechanisms underlying the rearrangements which take place both at fertilisation and during compaction and experimental decompaction are discussed.

Type
Article
Copyright
Copyright © Cambridge University Press 1993

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References

Damsky, C.H., Richa, J., Solter, D., Knudsen, K. & Buck, C.A. (1983). Identification and purification of a cell surface glycoprotein involved in cell-cell interactions. Cell 34, 455–66.CrossRefGoogle Scholar
Day, M.L., Pickering, S.J., Johnson, M.H. & Cook, D.I. (1993). Cell cycle control of a large conductance K+ channel in mouse early embryos. Nature 365, 560–2.CrossRefGoogle ScholarPubMed
Edelman, G.M. (1988) Morphoregulatory molecules. Biochemistry 27, 3533–43.CrossRefGoogle ScholarPubMed
Fleming, T.P. & Johnson, M.H. (1988). From egg to epithelium. Annu. Rev. Cell. Biol. 4, 459–85.CrossRefGoogle ScholarPubMed
Fleming, T.P., Pickering, S.J., Qasim, F. & Maro, B. (1986). The generation of cell surface polarity in mouse 8-cell blastomeres: the role of cortical microfilaments analysed using cytochalasin D. J. Embryol. Exp. Morphol. 95, 169–91.Google ScholarPubMed
Gallin, W.J., Edelman, G.M. & Cunningham, B.A. (1983). Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. Proc. Natl. Acad. Sci. USA 80, 1038–42.CrossRefGoogle Scholar
Goodall, H. & Maro, B. (1986). Major loss of junctional coupling during mitosis in early mouse embryos. J. Cell Biol. 102, 568–75.CrossRefGoogle ScholarPubMed
Hirano, S., Nose, A., Hatta, K., Kawakami, A. & Takeichi, M. (1987). Calcium-dependent cell-cell adhesion molecules (cadherins): subclass specificities and possible involvement of actin bundles. J. Cell Biol. 105, 2501–10.CrossRefGoogle ScholarPubMed
Houliston, E., Pickering, S.J. & Maro, B. (1987). Redistribution of microtubules and pericentriolar material during the development of polarity in mouse blastomeres. J. Cell Biol. 104, 1299–308.CrossRefGoogle ScholarPubMed
Howlett, S.K. (1986). A set of proteins showing cell cycle dependent modification in the early mouse embryo. Cell 45, 387–96.CrossRefGoogle ScholarPubMed
Johnson, M.H. & Maro, B. (1984). The distribution of cytoplasmic actin in mouse 8-cell blastomeres. J. Embryol. Exp. Morphol. 82, 97117.Google ScholarPubMed
Johnson, M.H. & Maro, B. (1985). A dissection of the mechanisms generating and stabilising polarity in mouse 8- and 16-cell blastomeres: the role of cytoskeletal elements. J. Embryol. Exp. Morphol. 90, 311–34.Google ScholarPubMed
Johnson, M.H. & Maro, B. (1986). Time and space in the early mouse embryo: a cell biological approach to cell diversification. In: Experimental Approaches to Mammalian Embryonic Development, ed. Rossant, J.Pedersen, R.. pp3565. Cambridge: Cambridge University Press.Google Scholar
Johnson, M.H., Maro, B. & Takeichi, M. (1986). The role of cell adhesion in the synchronisation and orientation of polarisation in 8-cell mouse blastomeres. J. Embryol. Exp. Morphol. 93, 239–55.Google ScholarPubMed
Lehtonen, E. (1980). Changes in cell dimensions and intercellular contacts during cleavagerstage cell cycles in mouse embryonic cells. J. Embryol. Exp. Morphol. 58, 231–49.Google ScholarPubMed
Levy, J., Johnson, M.H., Goodall, H. & Maro, B. (1986). The timing of compaction: control of a major developmental transition in mouse early embryogenesis. J. Embryol. Exp. Morphol. 95, 213–37.Google Scholar
Maro, B., Johnson, M.H., Pickering, S.J. & Flach, G. (1984). Changes in actin distribution during fertilization of the mouse egg. J. Embryol. Exp. Morphol. 81, 211–37.Google ScholarPubMed
McNeil, H., Ryan, T., Smith, S.J. & Nelson, W.J. (1993). Spatial and temporal dissection of immediate and early events following cadherin-mediated epithelial cell adhesion. J. Cell Biol. 120, 1217–26.CrossRefGoogle Scholar
Nagafuchi, A. & Takeichi, M. (1989). Transmembrane control of cadherin-mediated cell adhesion: a 94kDa protein functionally associated with a specific region of the cyto-plasmic domain of E-cadherin. Cell Regulation 1, 3744.CrossRefGoogle Scholar
Nasr-Esfahani, M., Johnson, M.H. & Aitken, R.J. (1991). The effect of iron and iron chelators on the in vitro block to development of the mouse preimplantation embryo: BAT6 a new medium for improved culture of mouse embryos in vitro. Hum. Reprod. 5, 9971003.CrossRefGoogle Scholar
Nelson, W.J. & Veshnock, P.J. (1987). Modulation of fodrin (membrane skeleton) stability by cell-cell contact in Madin-Darby canine kidney epithelial cells. J. Cell Biol. 104, 1527–37.CrossRefGoogle ScholarPubMed
Nelson, W.J., Shore, E.M., Wang, A.Z. & Hammerton, R.W. (1990). Identification of a membrane-cytoskeletal complex containing the cell adhesion molecule uvomorulin (E-cadherin), ankyrin, and fodrin in Madin-Darby canine kidney cells. J. Cell Biol. 110, 349–57.CrossRefGoogle Scholar
Nicolson, G.L., Yanagimachi, R. & Yanagimachi, H. (1975). Ultrastructural localization of lectin-binding sites on the zonae pellucidae and plasma membranes of mammalian eggs. J. Cell Biol. 66, 263–74.CrossRefGoogle ScholarPubMed
Ozawa, M. & Kemler, R. (1990). Correct proteolytic cleavage is required for the cell adhesive function of uvomorulin. J. Cell Biol. 111, 1645–50.CrossRefGoogle ScholarPubMed
Ozawa, M., Baribault, H. & Kemler, R. (1989). The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J. 8, 1711–17.CrossRefGoogle ScholarPubMed
Peyrieras, N., Hyafil, F., Louvard, D., Ploegh, H.L. & Jacob, F. (1983). Uvomorulin: a nonintegral membrane protein of early mouse embryos. Proc. Natl. Acad. Sci. USA. 80, 6275–7.CrossRefGoogle Scholar
Pratt, H.P.M. (1989). Marking time and making space: chronology and topography in the early mouse embryo. Int. Rev. Cytol. 117, 99130.CrossRefGoogle ScholarPubMed
Pratt, H.P.M. & George, M.A. (1989). Organisation and assembly of the surface membrane during early cleavage of the mouse embryo. Rouxs Arch. Dev. Biol. 198, 170–8.CrossRefGoogle ScholarPubMed
Rodriguez-Boulan, E. & Nelson, W.J. (1989). Morphogenesis of the epithelial cell phenotype. Science 245, 718–25.CrossRefGoogle ScholarPubMed
Schatten, H., Cheney, R., Balczon, R., Willard, M., Cline, C., Simerly, C., & Schatten, G. (1986). Localization of fodrin during fertilization and early development of sea urchins and mice. Dev. Biol. 118, 457–66.CrossRefGoogle ScholarPubMed
Sefton, M., Johnson, M.H. & Clayton, L. (1992). Synthesis and phosphorylation of uvomorulin during mouse early development. Development 115, 313–18.CrossRefGoogle ScholarPubMed
Shirayoshi, Y., Okada, T.S. & Takeichi, M. (1983). The calcium-dependent cell-cell adhesion system regulates inner cell mass formation and cell surface polarization in early mouse development. Cell 35, 631–8.CrossRefGoogle ScholarPubMed
Shirayoshi, Y., Nose, A., Iwasaki, K. & Takeichi, M. (1986). N-linked oligosaccharides are not involved in the function of a cell-cell binding glycoprotein. Cell struct. Funct. 11, 245–52.CrossRefGoogle Scholar
Shore, E.M. & Nelson, W.J. (1991). Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby canine kidney epithelial cells. J. Biol. Chem. 266, 19672–80.CrossRefGoogle ScholarPubMed
Sobel, J.S. & Alliegro, M.A. (1985). Changes in the distribution of a spectrin-like protein during development of the preimplantation mouse embryo. J. Cell Biol. 100, 333–6.CrossRefGoogle ScholarPubMed
Sobel, J.S. & Goldstein, E.G. (1988). Spectrin synthesis in the preimplantation mouse embryo. Dev. Biol. 128, 284–9.CrossRefGoogle ScholarPubMed
Takeichi, M. (1991). Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451–5.CrossRefGoogle ScholarPubMed
Vestweber, D., Gossler, A., Boller, K. & Kemler, R. (1987). Expression and distribution of the cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev. Biol. 124, 451–6.CrossRefGoogle ScholarPubMed
Vincent, C., Cheek, T.R. & Johnson, M.H. (1992). Cell cycle progression of parthenogenetically activated mouse oocytes to interphase is dependent on the level of internal calcium. J. Cell Sci. 103, 389–96.CrossRefGoogle ScholarPubMed
Waksmundzka, M., Krysiak, E., Karasiewicz, J., Czlowska, R. & Tarkowski, A.J. (1984). Autonomous cortical activity in mouse eggs controlled by a cytoplasmic clock. J. Embryol. Exp. Morphol. 79, 6777.Google ScholarPubMed
Webster, S.D. & McGaughey, R.W. (1990). The cortical cytoskeleton and its role in sperm penetration of the mammalian eggs. Dev. Biol. 142, 6774.CrossRefGoogle Scholar
Wheelock, M.J. (1990). Catenin association with E-cadherin changes with the state of polarity of HT-29 cells. Exp. Cell Res.. 191, 186–93.CrossRefGoogle ScholarPubMed
Wollner, D.A., Krzeminski, K.A. & Nelson, W.J. (1992). Remodeling of the cell surface distribution of membrane proteins during the development of epithelial polarity. J. Cell Biol. 116, 889–99.CrossRefGoogle Scholar