Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T20:54:04.190Z Has data issue: false hasContentIssue false

Control of the surface expression of uvomorulin after activation of mouse oocytes

Published online by Cambridge University Press:  26 September 2008

Lesley Clayton*
Affiliation:
Department of Anatomy, University of cambridge, Cambridge, UK.
Josie M.L.
Affiliation:
Department of Anatomy, University of cambridge, Cambridge, UK.
McConnell Martin
Affiliation:
Department of Anatomy, University of cambridge, Cambridge, UK.
H. Johnson
Affiliation:
Department of Anatomy, University of cambridge, Cambridge, UK.
*
Dr L. Clayton, Department of Anatomy, University of Cambridge, Downing Street, Camhbridge CB2 3DY, UK. Telephone: (01223) 333755. Fax: (01223) 333786.

Extract

Uvomorulin (E-cadherin) is the major cell adhesion molecule responsible for intercellular adhesion in early mouse embryos. In contrast to other cell adhesion molecules, it is not detectable on the cell surface until around 6 h after fertilisation or parthenogenetic activation, at the time when pronuclear formation occurs (Clayton, L., Stinchcombe, S.V. and Johnson, M.H., Zygote 1, 333–44, 1993). In order to investigate this developmental control of surface expression of uvomorulin, we examined the effects of inhibitors of various cellular processes on the appearance of uvomorulin at the oocyte surface, as assessed immunocytochemically. Inhibitors of cytoskeletal assembly (cytochalasin D and nocodazole), protein synthesis (puromycin and anisomycin), and DNA synthesis (aphidicolin) had no effect on surface expression. Brefeldin A, which inhibits intracellular transport and secretion, did prevent surface expression, but monensin did not. The effects of brefeldin were reversible; following 8 h of treatment, recovery of surface expression after removal of brefeldin began within 2 h. The time-course of surface expression post-activation suggested a link with pronuclear formation. However, when pronuclear formation was advanced experimentally using 6-dimethylaminopurine(DMAP), concomitant advancement of surface uvomorulin was not observed. Similarly, surface expression of uvomorulin did not accompany puromycin-induced pronuclear formation in maturing meiotic metaphase 1 (MI) oocytes in vitro. Thus, surface uvomorulin expression does not appear to be linked simply to pronuclear formation. Proteolytic processing of both newly synthesised and total uvomorulin to generate mature molecule from precursor increased within 30 min to 1 h after activation, and also occurred in the continued presence of brefeldin, suggesting that uvomorulin processing appears to be controlled independently of its suface expression.

Type
Article
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

references

Clarke, H.J. & Masui, Y. (1983). The induction of reversible and irreversible chromosome decondensation by protein synthesis inhibition during meiotic maturation of mouse oocytes. Devl. Biol. 97, 291301.CrossRefGoogle ScholarPubMed
Clayton, L., Stinchcombe, S.V. & Johnson, M.H. (1993). Cell surface localisation and stability of uvomorulin during early mouse development. Zygote 1, 333–44.CrossRefGoogle ScholarPubMed
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
De, SousaPA, Valdimarsson, G., Nicholson, B.J. & Kidder, G.M. (1993). Connexin trafficking and the control of gap junction assembly in mouse preimplantation embryos. Development 117, 1355–67.Google Scholar
Edelman, G.M. (1988). Morphoregulatory molecules. Biochemistry 27, 3533–43.CrossRefGoogle ScholarPubMed
Fishman, P.H. & Curran, P.K. (1992). Brefeldin A inhibits protein synthesis in cultured cells. FEBS Lett. 314, 371–4.CrossRefGoogle ScholarPubMed
Fleming, T.P. & Johnson, M.H. (1988). From egg to epithelium. Annu. Rev. Cell Biol. 4, 459–85.CrossRefGoogle Scholar
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
Gawantka, V., Ellinger–Ziegelbauer, H. & Hausen, P. (1992). β1-integrin is a maternal protein that is inserted into all newly formed plasma membranes during early Xenopus embryogenesis. Development, 595605.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. (1986a). The effect of inhibiting DNA replication in the one–cell mouse embryo. Wilhelm Rouxás Arch. Dev. Biol. 195, 499505.CrossRefGoogle ScholarPubMed
Howlett, S.K. (1986b). A set of proteins showing cell cycle dependent modification in the early mouse embryo. Cell 45, 387–96.CrossRefGoogle ScholarPubMed
Howlett, S.K., Webb, M., Maro, B. & Johnson, M.H. (1985). Meiosis II, mitosis I and the linking interphase: a study of the cytoskeleton in the fertilized mouse egg. Cytobios 43, 295305.Google Scholar
Hyafil, F., Morello, D., Babinet, C. & Jocob, F. (1981). A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell, 21, 927–34.CrossRefGoogle Scholar
Johnson, M. & 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, pp. 3565. 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
Kellom, T., Vick, A. & Boldt, J. (1992). Recovery of penetration ability in protease–treated zona–free mouse eggs occurs coincident with recovery of a cell surface 94 KD protein. Mol.Reprod. Dev. 33, 4652.CrossRefGoogle ScholarPubMed
Kimber, S.J., Bentley, J., Ciemerych, M., Moller, C.J. & Bock, E.. (1994). Expression of N–CAM in fertilized pre– and periimplantation and parthenogenetically activated mouse embryos. J. Cell Biol. 63, 102–13.Google ScholarPubMed
Klausner, R.D., Donaldson, J.G. & Lippincott–schwartz, J. (1992). Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071–80.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.CrossRefGoogle ScholarPubMed
Larue, L., Ohsugi, M., Hirchenhain, J. & Kemler, R. (1994). E–cadhedrin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl.Acad. Sci. USA 91, 8263–7.CrossRefGoogle Scholar
Leaf, D.S., Roberts, S.J., Gerhart, J.C. & Moore, H.P. (1900). The secretory pathway is blocked between the trans–Golgi and the plasma membrane during meiotic maturation in Xenopus oocytes. Dev. Biol. 141, 112.CrossRefGoogle Scholar
Lippincott–Schwartz, J., Yuan, L.C., Bonifacino, J.S. & Klausner, R.D. (1989). Rapid distribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to er. Cell 56, 801–13.CrossRefGoogle Scholar
Lippincott–Schwartz, J., Donaldson, J.G., Schweizer, A., Berger, E.G., Hauri, H.P., Yuan, L.C. & Klausner, R.D.(1990). Microtubule–dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60, 821–36.CrossRefGoogle Scholar
Maro, B. & Pickering, S. (1984). Microtubules influence compaction in preimplantation mouse embryos. J. Embryol. Exp. Morphol. 84, 217–32.Google ScholarPubMed
Mollenhauer, H.M., Morre, D.J. & Rowe, L.D. (1990). Alteration of intracellular traffic by monensin: mechanism, specificity and relationship to toxicity. Biochim. Biophys. Acta. 114, 225–46.CrossRefGoogle Scholar
Möller, A.H.J., Angres, B. & Hausen, P. (1992). U–cadherin in Xenopus oogenesis and oocyte maturation. Development 114, 533–43.CrossRefGoogle Scholar
Möller, A.H.J.., Gawantka, V., Ding, X. & Hausen, P. (1993). Maturation induced internalisation of β1-integrin by Xenopus oocytes and formation of the maternal integrin pool. Mechanisms of Development 42, 7788.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
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
Odor, L. (1960). Electron microscopic studies on ovarian oocytes and unfertilized ova in the rat. J. Biophys. Biochem. Cytol. 7, 567–74.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
Roberts, J.M. (1993). Turning DNA replication on and off. Curr. Opin. Cell Biol. 5, 201–6.CrossRefGoogle ScholarPubMed
Rodriguez–Boulan, E. & Nelson, W.J. (1989). Morphogenesis of the epithelial cell phenotype. Science 245, 718–25.CrossRefGoogle ScholarPubMed
Sanchez, R.M., Vervoordeldonk, M.J.B.M.., Schalwijk, C.G.van den Bosch, H. (1993). Prevention of the induced synthesis and secretion of group II phospholipase A2 by brefeldin A. FEBS Left. 332, 99104.CrossRefGoogle ScholarPubMed
Sathanan, H. (1994). Ultrastructural changes during meiotic maturation in mammalian oocytes: unique aspects in the human oocyte. Microscopy Research and Technique 27, 145–64.CrossRefGoogle Scholar
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., Nose, A., Iwasaki, K.&Takeich, M. (1986). N–linked oligosaccharides are not involved in the function of a cell–cell binding glycoprotein. Cell Struct. Func. 11, 245–52.CrossRefGoogle Scholar
Shore, E.M. & Nelson, W.J. (1991). Biosynthesis of the cell adhesion molecule uvomorulin (E–cadhedrin) in Madhin–Darby canine kidney epithelial cells J. Biol. Chem. 266, 19672–80.CrossRefGoogle Scholar
Siracusa, G., Whittingham, D.G., Molinaro, M. & Vivarelli, E. (1978). Parthenogenetic activation of mouse oocytes induced by inhibitors of protein synthesis. J. Embryol. Exp. Morphol. 43, 157–66.Google ScholarPubMed
Szoilosi, M.S., Kubiak, J.Z., Debey, P., de Pennart, H., Szollosi, D. & Maro, B.. (1993). Inhibition of protein kinases by 6–dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell Sci. 104, 861–72.CrossRefGoogle Scholar
Takeichi, M. (1991). Cadhedrin cell adhesion receptors as a morphogenetic regulator. Science 251, 251–5.CrossRefGoogle Scholar
Tarone, G., Russo, M.A.Hirsch, E., Odorisio, T., Altruda, F., Silengo, L. & Siracusa, G. (1993). Expression of β1; integrin complexes on the surface of unfertilized mouse oocyte, Development 117, 1369–75.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