Cell Polarity in the Preimplantation Mouse Embryo

  • Carol A. Ziomek


The union of two highly polarized cells, the sperm and the egg, initiates a series of dramatic cellular transformations that culminate, during the first 4 days of mouse preimplantation development, in the production of a multicellular blastocyst (reviewed by Wiley, Chapter 4) having two distinct and committed tissues. The outer layer of transporting epithelial cells, which surround and generate the blastocoelic cavity, are the trophectodermal cells that will give rise to extraembryonic structures. Attached to the interior of the trophectodermal layer at one end of the blastocoelic cavity is a cluster of relatively undifferentiated cells, the inner cell mass, that will subsequently give rise to the embryo proper. Attempts to elucidate the mechanisms by which these two distinct cell types diverge from a common pathway during the first 3 days of preimplantation development have yielded not only clues as to possible differentiative signals operating in development, but also detailed structural information on the morphology and properties of cells from the early embryo. One such piece of structural information gained from these studies is that many embryonic cells are architecturally polarized both at their cell surface and in their cytoplasmic domain; these cell asymmetries may play important roles in embryonic development.


Fluorescent Intensity Cortical Granule Mobility Parameter Lipid Probe Nipple Region 
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  1. Abramczuk, J., Solter, D., and Koprowski, H., 1977, The beneficial effect of EDTA on development of mouse one-cell embryos in chemically defined medium, Dev. Biol. 61: 378–383.PubMedCrossRefGoogle Scholar
  2. Adler, R.A., and Ziomek, C.A., 1986a, Cell specific loss of polarity-inducing ability by later stage mouse preimplantation embryos, Dev. Biol. 114, in press.Google Scholar
  3. Adler, R., and Ziomek, C.A., 1986b, Blastomere polarization by embryonal carcinoma cells, Biol. Bull., in press.Google Scholar
  4. Adler, R., Lepire, M., and Ziomek, C.A., 1985, 8-cell blastomere polarity-inducing ability of a variety of embryonic cells and non-cellular materials, J. Cell Biol. 101: 343a.Google Scholar
  5. Boldt, J., and Wolf, D.P., 1982, A rapid high yield method for preparing zonafree mouse eggs, J. Cell Biol. 97: 184a.Google Scholar
  6. Cholewa-Stewart, J., and Massaro, E.J., 1972, Thermally induced dissolution of the murine zona pellucida, Biol. Reprod. 7: 166–169.PubMedGoogle Scholar
  7. Ducibella, T., and Anderson, E., 1975, Cell shape and membrane changes in eight cell mouse embryo: prerequisite for morphogenesis of the blastocyst, Dev. Biol. 47: 45–58.PubMedCrossRefGoogle Scholar
  8. Ducibella, T., Ukena, T., Karnovsky, M.J., and Anderson, E., 1977, Changes in cell surface and cortical cytoplasmic organization during early embryogenesis in the preimplantation mouse embryo, J. Cell Biol. 74: 153–167.PubMedCrossRefGoogle Scholar
  9. Eager, D.D., Johnson, M.H., and Thurley, K.W., 1976, Ultrastructural studies on the surface membrane of the mouse egg, J. Cell Sci. 22: 345–353.PubMedGoogle Scholar
  10. Flach, G., Johnson, M.H., Braude, P.R., Taylor, R.A.S., and Bolton, V.N., 1982, The transition from maternal to embryonic control in the 2-cell mouse embryo, The EMBO Journal 1: 681–686.PubMedGoogle Scholar
  11. Goddard, M.J., and Pratt, H.P.M., 1983, Control of events during early cleavage of the mouse embryo: an analysis of the “2-cell block”, J. Embryol. Exp. Morphol. 73: 111–123.PubMedGoogle Scholar
  12. Goodall, H., and Johnson, M.H., 1982, Use of carboxyfluorescein diacetate to study formation of permeable channels between mouse blastomeres, Nature (London) 295: 524–526.CrossRefGoogle Scholar
  13. Goodall, H., and Johnson, M.H., 1984, The nature of intercellular coupling within the preimplantation mouse embryo, J. Embryol. Exp. Morphol. 79: 53–76.PubMedGoogle Scholar
  14. Hahnel, A.C., and Eddy, E.M., 1982, Three monoclonal antibodies against cell surface components on early mouse embryos, J. Cell Biol. 95: 156a.Google Scholar
  15. Handyside, A.H., 1980, Distribution of antibody-and lectin-binding sites on dissociated blastomeres from mouse morulae: evidence for polarization at compaction, J. Embryol. Exp. Morphol. 69: 99–116.Google Scholar
  16. Inoue, M., and Wolf, D.P., 1974, Comparative solubility properties of the zonae pellucidae of unfertilized and fertilized mouse ova, Biol. Reprod. 4: 558–565.CrossRefGoogle Scholar
  17. Izquierdo, L., and Ebensperger, C., 1982, Cell membrane regionalization in early mouse embryos as demonstrated by 5’-nucleotidase activity, J. Embryol. Exp. Morphol. 69: 115–126.PubMedGoogle Scholar
  18. Izquierdo, L., Lopez, T., and Marticorena, P., 1980, Cell membrane regions in preimplantation mouse embryos, J. Embryol. Exp. Morphol. 59: 89–102.PubMedGoogle Scholar
  19. Jackowski, S., Leibo, S.P., and Mazur, P., 1980, Glycerol permeabilities of fertilized and unfertilized mouse ova, J. Exp. Zool. 212: 329–341.PubMedCrossRefGoogle Scholar
  20. Jackson, B.W., Grund, C., Schmid, E., Burki, K., Franke, W.W., and Illmensee, K., 1980, Formation of cytoskeletal elements during mouse embryogenesis, Differentiation 17: 161–179.PubMedCrossRefGoogle Scholar
  21. Johnson, L.V., and Calarco, P.G., 1980, Mammalian preimplantation development: the cell surface, Anat. Rec. 196: 201–219.PubMedCrossRefGoogle Scholar
  22. Johnson, M.H., and Edidin, M., 1978, Lateral diffusion in plasma membrane of mouse egg is restricted after fertilization, Nature (London) 272: 448–450.CrossRefGoogle Scholar
  23. Johnson, M.H., and Maro, B., 1984, The distribution of cytoplasmic actin in mouse 8-cell blastomeres, J. Embryol. Exp. Morphol. 82: 97–117.PubMedGoogle Scholar
  24. Johnson, M.H., and Ziomek, C.A., 1981a, Induction of polarity in mouse 8-cell blastomeres: specificity, geometry and stability, J. Cell Biol., 91: 303–308.PubMedCrossRefGoogle Scholar
  25. Johnson, M.H., and Ziomek, CA., 1981b, The foundation of two distinct cell lineages within the mouse morula, Cell 24: 71–80.PubMedCrossRefGoogle Scholar
  26. Johnson, M.H., and Ziomek, C.A., 1982, Cell subpopulations in the late morula and early blastocyst of the mouse, Dev. Biol. 91: 431–439.PubMedCrossRefGoogle Scholar
  27. Johnson, M.H., and Ziomek, C.A., 1983, Cell interactions influence the fate of mouse blastomeres undergoing the transition from the 16-to 32-cell stage, Dev. Biol. 211-218.Google Scholar
  28. Johnson, M.H., Eager, D.D., Muggleton-Harris, A.L., and Grave, M.H., 1975, Mosaicism in the organization of concanavalin A receptors on surface membrane of mouse egg, Nature (London) 257: 321–322.CrossRefGoogle Scholar
  29. Johnson, M.H., McConnell, J., and Van Blerkom, J., 1984, Programmed development in the mouse embryo, J. Embryol. Exp. Morphol. 83 Suppl.: 197–231.PubMedGoogle Scholar
  30. Lehtonen, E., Lehto, V.P., Vartio, T., Badley, R.A., and Virtanen, I., 1983, Expression of cytokeratin polypeptides in mouse oocytes and preimplantation embryos, Dev. Biol. 100: 158–165.PubMedCrossRefGoogle Scholar
  31. Lewis, W.H., and Wright, E.S., 1935, On the early development of the mouse egg, Contrib. Embryol. Carnegie Instn. 148: 115–143.Google Scholar
  32. Longo, F.J., and Chen, D-Y, 1985, Development of cortical polarity in mouse eggs: Involvement of the meiotic apparatus, Dev. Biol 107: 382–394.PubMedCrossRefGoogle Scholar
  33. Malick, I.E., and Wilson, R.B., 1975, Evaluation of a modified technique for SEM examination of vertebrate specimens without evaporated metal layers, in: Scanning Electron Microscopy (O. Johari, ed.), IITRI, Chicago, IL, pp. 259–266.Google Scholar
  34. Maro, B., Johnson, M.H., Pickering, S.J., and Flach, G., 1984, Changes in actin distribution during fertilization of the mouse egg, J. Embryol. Exp. Morphol. 81: 211–237.PubMedGoogle Scholar
  35. Maro, B., and Pickering, S.J., 1984, Microtubules influence compaction in preimplantation mouse embryos, J. Embryol. Exp. Morphol. 84: 217–232.PubMedGoogle Scholar
  36. Mintz, B., 1962, Experimental study of the developing mammalian egg; removal of the zona pellucida, Science 138: 594–595.PubMedCrossRefGoogle Scholar
  37. Muggleton-Harris, A., Whittingham, D.G., and Wilson, L., 1982, Cytoplasmic control of preimplantation development in vitro in the mouse, Nature (London) 299: 460–462.CrossRefGoogle Scholar
  38. Mulnard, J., and Huygens, R., 1978, Ultrastructural localization of nonspecific alkaline phosphatase during cleavage and blastocyst formation in the mouse, J. Embryol. Exp. Morphol. 44: 121–131.PubMedGoogle Scholar
  39. Nicolson, G.L., Yanagimachi, R., and Yanagimachi, H., 1975, Ultrastructural localization of actin-binding sites on the zonae pellucidae and plasma membranes of mammalian eggs, J. Cell Biol. 66: 263–274.PubMedCrossRefGoogle Scholar
  40. Nicosia, S.V., Wolf, D.P., and Inoue, M., 1977, Cortical granule distribution and cell surface characteristics in mouse eggs, Dev. Biol. 57: 56–74.PubMedCrossRefGoogle Scholar
  41. Nizeyimana-Rugina, E., and Mulnard, J., 1979, Ultrastructural localization of 5’-nucleotidase in preimplantation mouse embryos, Arch. Biol. 90: 131–140.Google Scholar
  42. Nuccitelli, R., 1983, Transcellular ion currents: Signals and effectors of cell polarity, in: Modern Cell Biology, Vol. 2 (J.R. McIntosh, ed.), Alan R. Liss, New York, pp. 451–481.Google Scholar
  43. Nuccitelli, R., and Wiley, L.M., 1985, Polarity of isolated blastomeres from mouse morulae: Detection of transcellular ion currents, Dev. Biol., 109: 452–463.PubMedCrossRefGoogle Scholar
  44. Oshima, R.G., Howe, W.E., Klier F.G., Adamson, E.D., and Shevinsky, L.H., 1983, Intermediate filament protein synthesis in preimplantation murine embryos, Dev. Biol. 99: 447–455.PubMedCrossRefGoogle Scholar
  45. Pratt, H.P.M., Ziomek, C.A., Reeve, W.J.D., and Johnson, M.H., 1982, Compaction of the mouse embryo: an analysis of its components, J. Embryol. Exp. Morphol. 70: 113–132.PubMedGoogle Scholar
  46. Reeve, W.J.D., 1981, Cytoplasmic polarity develops at compaction in rat and mouse embryos, J. Embryol. Exp. Morphol. 62: 351–367.PubMedGoogle Scholar
  47. Reeve, W.J.D., and Kelly, F.P., 1983, Nuclear position in the cells of the mouse early embryo, J. Embryol. Exp. Morphol. 75: 117–139.PubMedGoogle Scholar
  48. Reeve, W.J.D., and Ziomek, CA., 1981, Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction, J. Embryol. Exp. Morphol. 62: 339–350.PubMedGoogle Scholar
  49. Shirayoshi, Y., Okada, P.S., and 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: 631–638.PubMedCrossRefGoogle Scholar
  50. Siracusa, G., DeFelici, M., Coletta, M., and Vivarelli, E., 1978, Inhibitors of protein synthesis increase the agglutinability mediated by concanavalin A of the unfertilized mouse oocyte, Dev. Biol. 62: 530–533.PubMedCrossRefGoogle Scholar
  51. Smithberg, M., 1953, The effect of different proteolytic enzymes on the zona pellucida of mouse ova, Anat. Rec. 117: 554.Google Scholar
  52. Sobel, J.S., 1983a, Localization of myosin in the preimplantation mouse embryo, Dev. Biol. 95: 227–231.PubMedCrossRefGoogle Scholar
  53. Sobel, J.S., 1983b, Cell-cell contact modulation of myosin organization in the early mouse embryo, Dev. Biol. 100: 207–213.PubMedCrossRefGoogle Scholar
  54. Sobel, J.S., 1984, Myosin rings and spreading in mouse blastomeres, J. Cell Biol. 99: 1145–1150.PubMedCrossRefGoogle Scholar
  55. Sobel, J.S., and Alliegro, M.A., 1985, Changes in the distribution of a spectrinlike protein during development of the preimplantation mouse embryo, J. Cell Biol. 100: 333–336.PubMedCrossRefGoogle Scholar
  56. Solter, D., and Knowles, B.B., 1975, Immunosurgery of mouse blastocyst, Proc. Natl. Acad. Sci. USA 72: 5009–5102.CrossRefGoogle Scholar
  57. Sutherland, A.E., and Calarco-Gillam, P.G., 1983, Analysis of compaction in the preimplantation mouse embryo, Dev. Biol. 100: 328–338.PubMedCrossRefGoogle Scholar
  58. Tank, D.W., Wu, E-S, and Webb, W.W., 1982, Enhanced molecular diffusibility in muscle membrane blebs: release of lateral constraints, J. Cell Biol. 92: 207–212.PubMedCrossRefGoogle Scholar
  59. Thompson, R.S., and Zamboni, L., 1974, Phagocytosis of supernumerary spermatozoa of the mouse by two-cell mouse embryos, Anat. Rec. 178: 3.PubMedCrossRefGoogle Scholar
  60. Thompson, R,S., Smith, D.M., and Zamboni, L., 1974, Fertilization of mouse ova in vitro: an electron microscopic study, Fertil. Steril. 25: 222–249.PubMedGoogle Scholar
  61. Vorbrodt, A., Konwinski, M., Solter, D., and Koprowski, H., 1977, Ultrastructural cytochemistry of membrane-bound phosphatases in preimplantation mouse embryos, Dev. Biol. 55: 117–134.PubMedCrossRefGoogle Scholar
  62. Wabik-Sliz, B., and Kujat, R., 1979, The surface of mouse oocytes from two inbred strains differing in efficiency of fertilization, as revealed by scanning electron microscopy, Biol. Reprod. 20: 405–408.PubMedCrossRefGoogle Scholar
  63. Whitten, W.K., and Biggers, J.D., 1968, Complete development in vitro of the preimplantation stages of the mouse in a simple chemically defined medium, J. Reprod. Fertil. 17: 399–401.PubMedCrossRefGoogle Scholar
  64. Whittingham, D.G., and Biggers, J.D., 1967, Fallopian tube and early cleavage in the mouse, Nature (London) 213: 942.CrossRefGoogle Scholar
  65. Wolf, D.E., 1983, The plasma membrane in early embryogenesis, in: Development in Mammals, Vol. 5 (M.H. Johnson, ed), Elsevier Science Publishers, pp. 187-208.Google Scholar
  66. Wolf, D.E., and Edidin, M., 1981, Diffusion and mobility of molecules in surface membranes, in: Techniques in Cellular Physiology, P105, Part 1 (P.F. Baker, ed.), Elsevier Biomedicai Press, Amsterdam, pp. 1–14.Google Scholar
  67. Wolf, D.E., and Ziomek, C.A., 1983, Regionalization and lateral diffusion of membrane proteins in unfertilized and fertilized mouse eggs, J. Cell Biol. 96: 1786–1790.PubMedCrossRefGoogle Scholar
  68. Wolf, D.E., Edidin, M., and Handyside, A.H., 1981, Changes in the organization of the mouse egg plasma membrane upon fertilization and first cleavage: indications from the lateral diffusion rates of fluorescent lipid analogs, Dev. Biol. 85: 195–198.PubMedCrossRefGoogle Scholar
  69. Wolf, D.E., Handyside, A.H., and Edidin, M., 1982, Effect of microvilli on lateral diffusion measurements made by the fluorescence photobleaching recovery technique, Biophys. J. 38: 295–297.PubMedCrossRefGoogle Scholar
  70. Wolf, D.P., 1978, The block to polyspermy in zona-free mouse eggs, Dev. Biol. 64: 1–10.PubMedCrossRefGoogle Scholar
  71. Wolf, D.P., Nicosia, S.V., and Mastroianni, L., Jr., 1976, Surface topography of mouse eggs before and after insemination, Biol. Bull. 151: 435a.Google Scholar
  72. Wolf, D.P., Nicosia, S.F., and Hamada, M., 1979, Premature cortical granule loss does not prevent sperm penetration of mouse eggs, Dev. Biol. 71: 22–32.PubMedCrossRefGoogle Scholar
  73. Wu, E-S, Tank, D.W., and Webb, W.W., 1982, Unconstrained lateral diffusion of concanavalin A receptors of bulbous lymphocytes, Proc. Natl. Acad. Sci. USA 79: 4962–4966.PubMedCrossRefGoogle Scholar
  74. Ziomek, C.A., and Johnson, M.H., 1980, Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction, Cell 21: 935–942.PubMedCrossRefGoogle Scholar
  75. Ziomek, C.A., and Johnson, M.H., 1981, Properties of polar and apolar cells from the 16-cell mouse morula, Wilhelm Roux’s Archiv. 190: 287–296.CrossRefGoogle Scholar
  76. Ziomek, C.A., and Johnson, M.H., 1982, The roles of phenotype and position in guiding the fate of 16-cell mouse blastomeres, Dev. Biol. 91: 440–447.PubMedCrossRefGoogle Scholar
  77. Ziomek, C.A., and Lepire, M., 1984, The fluorescent histochemical demonstration of alkaline phosphatase in the preimplantation mouse embryo, J. Cell Biol. 99: 267a.Google Scholar
  78. Ziomek, C.A, and Lepire, M.L., 1986, Fluorescent histochemical and immunofluorescent localization of cell surface alkaline phosphatase on mouse preimplantation embryos, J. Embryol. Exp. Morphol. (submitted).Google Scholar
  79. Ziomek, C.A., Lepire, M., Moynihan, M., and Wolf, D.E., 1984, Membrane protein and lipid diffusion and regionalization in 8-cell mouse embryos, J. Cell Biol. 99: 279a.Google Scholar

Copyright information

© Plenum Press, New York 1987

Authors and Affiliations

  • Carol A. Ziomek
    • 1
  1. 1.Worcester Foundation for Experimental BiologyShrewsburyUSA

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