The mosaic organisation of the preimplantation mouse embryo

  • M. H. Johnson
  • C. A. Ziomek
  • W. J. D. Reeve
  • H. P. M. Pratt
  • H. Goodall
  • A. H. Handyside
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 2)


The formation of the inner cell mass (ICM) and trophectoderm of the blastocyst constitutes the first definitive spatial differentiation of cells during embryogenesis. The two tissues show differences in structure, function, biochemistry, prospective fate and developmental potency. An understanding of the origins of these cell subpopulations, and the mechanism by which they are generated during cleavage, has proved to be elusive. It has been agreed generally that whatever mechanism operates, it must accommodate the prodigious regulatory capacity of the cells of the cleaving embryo, the morula and even the early blastocyst itself. Whilst this prolonged period of developmental lability apparently places the mammalian embryo in a unique position, it has also led frequently to the erroneous conclusion that the underlying mechanisms operating within the embryo must be correspondingly unique. Thus, embryos of many lower vertebrates and invertebrates appear to be mosaics, in which spatial differences in the cytoplasmic organisation within the individual egg, zygote or early blastomere are translated by cell divisions into regional differences among the cells of the embryo.


Mouse Embryo Polar Cell Inner Cell Mass Mammalian Embryo Preimplantation Mouse Embryo 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Wilson EB: The Cell in Development and Heredity. 3rd edition Macmillan, New York, 1925.Google Scholar
  2. 2.
    Davidson EH: Gene Activity in Early Development. 2nd edition Academic Press, New York, 1976.Google Scholar
  3. 3.
    Graham CF, Wareing PF: The Developmental Biology of Plants and Animals. Blackwell Scientific Publications. Oxford, 1976.Google Scholar
  4. 4.
    Johnson MH: Membrane events associated with the generation of a blastocyst. Int Rev Cytol Suppl 12: 1–37, 1981.PubMedGoogle Scholar
  5. 4.
    Johnson MH: Membrane events associated with the generation of a blastocyst. Int Rev Cytol Suppl 12: 1–37, 1981.PubMedGoogle Scholar
  6. 6.
    Jones-Seaton A: A study of cytoplasmic basophily in the egg of the rat and some other mammals. Ann Soc Roy Zool (Belgium) 80: 76–86, 1950.Google Scholar
  7. 7.
    Dalcq AM: Introduction to General Embryology. Oxford University Press, London, 1957.Google Scholar
  8. 8.
    Mulnard JG: Studies of regulation of mouse ova in vitro. In: Pre-implantation Stages of Pregnancy. Ciba Foundation Symposium. Wolstenholme, GEW, O’Connor M (eds) Churchill, London, 1965, pp 123–138.Google Scholar
  9. 9.
    Johnson MH, Pratt HPM, Handyside AH: The generation and recognition of positional information in the preimplantation mouse embryo. In: Cellular and Molecular Aspects of Implantation. Glasser SR, Bullock DW (eds) Plenum Press, New York, 1981, pp 55–74.Google Scholar
  10. 10.
    Lewis WH, Wright ES: On the early development of the mouse egg. Contrib to Embryol Carnegie Inst 148: 115–143, 1935.Google Scholar
  11. 11.
    Lehtonen E: Changes in cell dimensions and intercellular contacts during cleavage-stage cell cycles in mouse embryonic cells. J Embryol exp Morph 58: 231–249, 1980.PubMedGoogle Scholar
  12. 12.
    Ducibella T, Anderson E: Cell shape and membrane changes in the eight-cell mouse embryo: prerequisites for morphogenesis of the blastocyst. Dev Biol 47: 45–58, 1975.PubMedCrossRefGoogle Scholar
  13. 13.
    Ducibella T, Albertini DF, Anderson E & Biggers SD: The pre-implantation mammalian embryo: characterization of intercellular junctions and their appearance during development. Dev Biol 45: 231–250, 1975.PubMedCrossRefGoogle Scholar
  14. 14.
    Ducibella T, Anderson E: The effects of calcium deficiency on the formation of the zonula occludens and blastocoel in the mouse embryo. Dev Biol 73: 46–58, 1979.PubMedCrossRefGoogle Scholar
  15. 15.
    Magnuson T, Jacobson JB, Stackpole CW: Relationship between intercellular tation mouse embryo. Dev Biol 67: 214–224, 1978.PubMedCrossRefGoogle Scholar
  16. 16.
    Lo CW, Gilula NB: Gap junctional communication in the pre-implantation mouse embryo. Cell 18: 399–409, 1979.PubMedCrossRefGoogle Scholar
  17. 17.
    Lo CW: Gap junctions and development. In: Development in Mammals, vol. 4. Johnson MH (ed) Elsevier/North-Holland Biomedical Press, Amsterdam, 1980, pp 39–80.Google Scholar
  18. 18.
    Goodall H, Johnson MH: The use of carboxy-fluorescein diacetate to study the formation of permeable channels between mouse blastomeres. Nature, 295, 524–526, 1982.PubMedCrossRefGoogle Scholar
  19. 19.
    Calarco PG, Epstein CJ: Cell surface changes during preimplantation development in the mouse. Dev Biol 32: 208–213, 1973.PubMedCrossRefGoogle Scholar
  20. 20.
    Reeve WJD, Ziomek CA: Distribution of microvilli on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J Embryol exp Morph 62: 339–350, 1981.PubMedGoogle Scholar
  21. 21.
    Ducibella T, Ukena T, Karnovsky M, Anderson E: Changes in cell surface and cortical cytoplasmic organization during embryogenesis in the preimplantation mouse embryo. J Cell Biol 74: 153–167, 1977.PubMedCrossRefGoogle Scholar
  22. 22.
    Handyside AH: Distribution of antibody- and lectin-binding sites on dissociated blastomeres from mouse morulae: evidence for polarization at compaction. J Embryol exp Morph 60: 99–116, 1980.PubMedGoogle Scholar
  23. 23.
    Ziomek CA, Johnson MH: Cell surface interation induces polarization of mouse 8-cell blastomeres at compaction. Cell 21: 935–942, 1980.PubMedCrossRefGoogle Scholar
  24. 24.
    Johnson LV, Calarco PG: Immunological characterization of em¬bryonic cell surface antigens recognized by antiblastocyst serum. Dev Biol 79: 208–223, 1981.CrossRefGoogle Scholar
  25. 24.
    Johnson LV, Calarco PG: Immunological characterization of em¬bryonic cell surface antigens recognized by antiblastocyst serum. Dev Biol 79: 208–223, 1981.CrossRefGoogle Scholar
  26. 26.
    Reeve WJD: Cytoplasmic polarity develops at compaction in rat and mouse embryos. J Embryol exp Morph 62: 351–367, 1981.PubMedGoogle Scholar
  27. 27.
    Johnson MH, Ziomek CA: Induction of polarity in mouse 8-cell blastomeres: specificity, geometry and stability. J Cell Biol 91: 303–308, 1981.PubMedCrossRefGoogle Scholar
  28. 28.
    Johnson, MH: The molecular and cellular basis of preimplantation mouse development. Biol Rev 56: 463–498.Google Scholar
  29. 29.
    Flach G, Johnson MH, Braude PR, Taylor RAS, Bolton V: The transition from maternal to embryonic control of preimplantation mouse development. The EMBO Journal 1: 681–686, 1982.PubMedGoogle Scholar
  30. 30.
    Pratt HPM, Ziomek CA, Reeve WJD, Johnson MH: Compaction of the mouse embryo: an analysis of its components. J Embryol exp Morph 70: 113–132, 1982.PubMedGoogle Scholar
  31. 31.
    Surani MAH, Barton Sc, Burling A: Differentiation of 2-cell and 8-cell mouse embryos arrested by cytoskeletal inhibitors. Exp Cell Res 125: 275–286, 1980.PubMedCrossRefGoogle Scholar
  32. 32.
    Pratt HPM, Chakraborty J, Surani MAH: Molecular and morphological differentiation of the mouse blastocyst after manipulations of compaction with cytochalasin D. Cell 26: 279–292, 1981.PubMedCrossRefGoogle Scholar
  33. 33.
    Surani MAH: Glycoprotein synthesis and inhibition of glycosylation by tunicamycin in preimplantation mouse embryos: compaction and trophoblast adhesion. Cell 18: 217–227, 1979.PubMedCrossRefGoogle Scholar
  34. 34.
    Surani MAH, Kimber SJ, Handyside AH: Synthesis and role of cell surface glycoproteins in preimplantation mouse development. Exp Cell Res 133: 331–339, 1981.PubMedCrossRefGoogle Scholar
  35. 35.
    Webb CG, Duksin D: Involvement of glycoproteins in the develop ment of early mouse embryos: effect of tunicamycin and α, α dipyridyl in vitro. Differentiation 20: 81–86, 1982.CrossRefGoogle Scholar
  36. 36.
    Kemler R, Babinet C, Eisen H, Jacob F: Surface antigen in early differentiation. Proc Natn Acad Sci USA 74: 4449–4452, 1977.CrossRefGoogle Scholar
  37. 37.
    Johnson MH, Chakraborty J, Handyside AH, Willison K, Stern P: The effect of prolonged decompaction on the development of the pre-implantation mouse embryo. J Embryol exp Morph 54: 241–261, 1979.PubMedGoogle Scholar
  38. 38.
    Ducibella T: Divalent antibodies to mouse embryonal cacinoma cells inhibit compaction in the mouse embryo. Devel Biol 79: 356–366, 1980.CrossRefGoogle Scholar
  39. 39.
    Reeve WJD: Effect of concanavalin A on the formation of the mouse blastocyst. J Reprod Immunol 4: 53–64, 1982.PubMedCrossRefGoogle Scholar
  40. 40.
    Siracusa G, Whittingham DG, De Felici M: The effect of microtubule-and microfilament-disrupting drugs on preimplantation mouse embryos. J Embryol exp Morph 60: 71–82, 1980.PubMedGoogle Scholar
  41. 41.
    Johnson MH, Ziomek CA. The foundation of two distinct cell lineages within the mouse morula. Cell 24: 71–80, 1981.PubMedCrossRefGoogle Scholar
  42. 42.
    Reeve WJD: The distribution of ingested horseradish peroxidase in the 16-cell mouse embryo. J Embryol exp Morph 66: 191–207, 1981.PubMedGoogle Scholar
  43. 43.
    Handyside AH: Immunofluorescence techniques for determining the numbers of inner and outer blastomeres in mouse morulae. J Reprod Immunol 2: 339–350, 1981.PubMedCrossRefGoogle Scholar
  44. 44.
    Ziomek CA, Pratt HPM, Johnson MH: The origins of cell diversity in the early mouse embryo. In: Brit Soc Cell Biol Symp No 5. Functional integration of cells in animal tissues. Finbow ME, Pitts JD (eds) Cambridge Univ. Press, 1982, pp 149–165.Google Scholar
  45. 45.
    Ziomek CA, Johnson MH: Properties of polar and apolar cells from the 16-cell mouse morula. W Roux’s Arch Dev Biol 190: 287–296, 1981.CrossRefGoogle Scholar
  46. 46.
    Ziomek CA, Johnson MH: The roles of phenotype and position in guiding the fate of 16-cell mouse blastomeres. Devel Biol 91: 440–447, 1982.CrossRefGoogle Scholar
  47. 47.
    Gardner RL, Johnson MH: An investigation of inner cell mass and trophoblast tissues following their isolation from the mouse blastocyst. J Embryol exp Morph 28: 279–312, 1972.PubMedGoogle Scholar
  48. 48.
    Nadijcka M, Hillman N: Ultrastructural studies of the mouse blastocyst substages. J Embryol exp Morph 32: 675–695, 1974.PubMedGoogle Scholar
  49. 49.
    Borland RM: Transport processes in the mammalian blastocyst. In: Development in Mammals, vol. 1 (MH Johnson, ed.) pp 31–67, North- Holland, 1977.Google Scholar
  50. 50.
    Burgoyne PS, Ducibella T: Changes in the properties of the developing trophoblast of preimplantation mouse embryos as revealed by aggregation studies. J Embryol exp Morph 40, 143–157, 1977.PubMedGoogle Scholar
  51. 51.
    Rossant J: Investigation of inner cell mass determination by aggregation of isolated rat inner cell masses with mouse morulae. J Embryol exp Morph 36: 163–174, 1976.PubMedGoogle Scholar
  52. 52.
    Stewart CL, Kimber SJ: The cell surface and interactions between different cell types of the mouse embryo. J Embryol exp Morph (submitted).Google Scholar
  53. 53.
    Johnson MH, Ziomek CA: Cell subpopulations in the late morula and early blastocyst of the mouse. Devel Biol 91: 431–439, 1982.CrossRefGoogle Scholar
  54. 54.
    Ziomek CA, Johnson MH, Handyside AH: The development potential of mouse 16-cell blastomeres. J Exp Zool 221: 345–355, 1982.PubMedCrossRefGoogle Scholar
  55. 55.
    Kimura S, Kato Y: Cell proliferation and the cell cycle in mouse blastocysts. Proc 51st Annual meeting of the Zoological Society of Japan, 1981.Google Scholar
  56. 56.
    Ziomek CA: The use of fluorescein isothiocyanate (F1TC) as a short-term cell lineage marker in the peri-implantation mouse embryo. W. Roux’s Arch Dev Biol, 191: 37–41, 1982.CrossRefGoogle Scholar
  57. 57.
    Balakier H, Pedersen RA: Allocation of cells to inner cell mass and trophectoderm lineage in preimplantation mouse embryos. Devel Biol 90: 352–362, 1982.CrossRefGoogle Scholar
  58. 58.
    Randle, B: Cosegregation of monoclonal reactivity and cell behaviour in the mouse preimplantation embryo. J Embryol exp Morph, 70: 261–278, 1982.PubMedGoogle Scholar
  59. 59.
    Johnson MH, Handyside AH, Braude PR: Control mechanisms in early mammalian development. In: Development in Mammals, vol 2. Johnson MH (ed) North-Holland, Amsterdam, 1977, pp 67–97.Google Scholar
  60. 60.
    Handyside AH: Time of commitment of inside cells isolated from preimplantation mouse embryos. J Embryol exp Morph 45: 37–53, 1978.PubMedGoogle Scholar
  61. 61.
    Hogan B, Tilly R: In vitro development of inner cell masses isolated immunosurgically from mouse blastocysts. 1. Inner cell masses from 3.5 day p.c. blastocysts incubated for 24 h before immunosurgery. J Embryol exp Morph 45: 93–105, 1978.PubMedGoogle Scholar
  62. 62.
    Spindle AI: Trophoblast regeneration by inner cell masses isolated from cultured mouse embryos. J exp Zool 203: 483–489, 1978.PubMedCrossRefGoogle Scholar
  63. 63.
    Rossant J, Vijh KM: Ability of outside cells from preimplantation mouse embryos to form inner cell mass derivatives. Devel Biol 76: 475–482, 1980.CrossRefGoogle Scholar
  64. 64.
    Rossant J, Lis WJ: Potential of isolated mouse inner cell masses to form trophectoderm derivatives in vivo. Devel Biol 70: 255–261, 1979.CrossRefGoogle Scholar
  65. 65.
    Mintz B: Experimental genetic mosaicism in the mouse. In: Pre-implantation Stages of Pregnancy. Ciba Foundation Symposium. (GEW Wolstenhome, O’Connor M, eds) pp 194–207. Churchill, London, 1965.Google Scholar
  66. 66.
    Tarkowski AK, Wroblewska J: Development of blastomeres of mouse eggs isolated at the 4– and 8-cell stage. J Embryol exp Morph 18, 155–180.Google Scholar
  67. 67.
    Herbert MC, Graham CF, 1974: Cell determination and biochemical differentiation of the early mammalian embryo. Current topics. Dev Biol 8: 151–178, 1974.Google Scholar
  68. 68.
    Ducibella T: Surface changes of the developing trophoblast cell. In: Development in Mammals, vol. 1. Johnson MH (ed) Elsevier/North-Holland Biomedical Press, Amsterdam, 1977, pp 5–30.Google Scholar
  69. 69.
    Johnson MH: Intrinsic and extrinsic factors in preimplantation development. J Reprod Fert 55, 255–265, 1979.CrossRefGoogle Scholar
  70. 70.
    Pedersen RA, Spindle AI: Role of the blastocoele microenvironment in early mouse embryo differentiation. Nature 284: 550–552, 1980.PubMedCrossRefGoogle Scholar
  71. 71.
    Pedersen RA, Spindle AI: Role of the blastocoele microenvironment in early mouse embryo differentiation. Nature 284: 550–552, 1980.PubMedCrossRefGoogle Scholar
  72. 72.
    Geathart J, Shaffed RM, Mussel JM, Oster-Granite ML: Cell lineage analyses of preimplantation mouse embryos after blastomere injections with horse radish peroxidase. Ped Res 16: 111, 1982.Google Scholar
  73. 73.
    Johnson MH, Ziomek CA: Cell interactions influence the fate of mouse blastomeres undergoing the transition from the 16- to the 32-cell stage. Dev Biol 85: 211–218, 1983.CrossRefGoogle Scholar

Copyright information

© Martinus Nijhoff Publishers, Boston, The Hague, Dordrecht, Lancaster 1984

Authors and Affiliations

  • M. H. Johnson
    • 1
  • C. A. Ziomek
    • 1
  • W. J. D. Reeve
    • 1
  • H. P. M. Pratt
    • 1
  • H. Goodall
    • 1
  • A. H. Handyside
    • 1
  1. 1.Department of AnatomyCambridgeUK

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