The cell surface of the mammalian embryo during early development

  • Lynn M. Wiley
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 2)


In experiments wherein he rearranged the blastomeres of cleavage-stage mouse embryos, Tarkowski (1) made the very simple yet profound observation that those blastomeres residing within the embryo tend to become inner cell mass (ICM) while those on the outside of the embryo tend to become trophectoderm (Fig. 1). He concluded that individual blastomeres possessed the ability to become either ICM or trophectoderm, based on relative cell position within the embryo, at least up to the 8-cell stage. Subsequent experiments have shown that this ability is not lost until the morula stage, when the embryo consists of 16–32 closely apposed cells (2). These observations have led to the ‘inside/outside’ hypothesis, which states that the relative position of a cell within the morula determines the subsequent developmental fate of that cell (1–3). If this is so, how is such positional information translated into the appropriate genetic activity which will lead to the differentiation of the cell to ICM or trophectoderm? In addition, how is this developmental restriction related to the formation of the blastocyst (i.e., cavitation)?


Inner Cell Mass Cell Surface Glycoprotein Mammalian Embryo Morula Stage Cell Surface Property 
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  1. 1.
    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, 1967.PubMedGoogle Scholar
  2. 2.
    Hillman N, Sherman MI, Graham C: The effect of spatial arrangement on cell determination during mouse development. J Emb Exp Morph 28: 263–278, 1972.Google Scholar
  3. 3.
    Gardner RL: Analysis of determination and differentiation in the early mammalian embryo using intra-and interspecific chimaeras. In: The Developmental Biology of Reproduction Markert CL, Papaconstantinou J (eds) Academic Press, New York, 1975, pp 207–236.Google Scholar
  4. 4.
    Vogt W: Gestaltungsanalyse am Amphilbienkeim mit ortlicher Vitalfar-bung. II. Gastrulation und mesodermbildung bei urodelen und anuren. Roux Arch 120: 385–706, 1929.CrossRefGoogle Scholar
  5. 5.
    Johnson MH, Eager D, Muggleton-Harris A: Mosaicism in organisation of concanavalin A receptors on surface membrane of mouse egg. Nature 257: 321–322, 1975.PubMedCrossRefGoogle Scholar
  6. 6.
    Eager DD, Johnson MH, Thurley KW: Ultrastructural studies on the surface membrane of the mouse egg, J Cell Sei 22: 345–353, 1976.Google Scholar
  7. 7.
    Nicosia SV, Wolf DP, Inoue M: Cortical granule distribution and cell surface characteristics in mouse eggs. Develop Biol 57: 56–74, 1977.PubMedCrossRefGoogle Scholar
  8. 8.
    Nicosia SV, Wolf DP, Mastroianni L Jr: Surface topography of mouse eggs before and after insemination. Gamete Res 1: 145–155, 1978.CrossRefGoogle Scholar
  9. 9.
    Moon HV, Isaacson RE, Pohlenz J: Mechanisms of association of enteropathogenic Escherichia coli with intestinal epithelium. Am J Clin Nutr 32: 119–127, 1979.PubMedGoogle Scholar
  10. 10.
    Maul GG, Steplewski Z, Weibel J, Koprowski H: Time sequence and morphological evaluations of cells fused by polyethylene glycol. 6000. In vitro 12: 787–796, 1976Google Scholar
  11. 11.
    Wiley LM Calarco PG: The effects of anti-embryo sera and their localization on the cell surface during mouse preimplantation development. Develop Biol 47: 407–418, 1975.PubMedCrossRefGoogle Scholar
  12. 12.
    Johnson MH, Edidin M: Lateral diffusion in plasma membrane of mouse egg is restricted after fertilization. Nature 272: 448–450, 1978.PubMedCrossRefGoogle Scholar
  13. 13.
    Gabel CA, Eddy EM, Shapiro BM: After fertilization, sperm surface components remain as a patch in sea urchin and mouse embryos. Cell 18: 207–215, 1979.PubMedCrossRefGoogle Scholar
  14. 14.
    Brachet J: An old enigma: The grey crescent of amphibian eggs. Curr Topics Dev Biol 11: 133–186, 1977.CrossRefGoogle Scholar
  15. 15.
    Gerhard J, Ubbels G, Black S, Hara K, Kirschner M: A reinvestigation of the role of the grey crescent in axis formation in xenopus laevis. Nature 292: 511–516. 1981.CrossRefGoogle Scholar
  16. 16.
    De Felici M, Siracusa G: Fertilization-induced changes in concanavalin A binding to mouse eggs. Exp Cell Res 132: 41–45, 1981.PubMedCrossRefGoogle Scholar
  17. 17.
    Inbar M, Huet C, Oseroff AR, Benbassat H, Sachs L: Inhibition of lectin agglutinability by fixation of the cell surface membrane. Biochim Biophys Acta 311: 594–599, 1973.PubMedCrossRefGoogle Scholar
  18. 18.
    Rutishauser V, Sachs L: Cell-to-cell binding induced by different lectins. J Cell Biol 65: 247–257, 1975.PubMedCrossRefGoogle Scholar
  19. 19.
    Marshall JD, Heiniger H-J: High affinity concanavalin A binding to sterol-depleted L cells. J Cell Physiol, 100: 539–550, 1979.PubMedCrossRefGoogle Scholar
  20. 20.
    Heyner S, Hunziker RD: Differential expression of alloantigens of the major histocompatability complex on unfertilized and fertilized mouse eggs. Develop Genet 1: 69–76, 1979.CrossRefGoogle Scholar
  21. 21.
    Wiley LM: Early embryonic cell surface antigens as developmental probes. In: Current Topics in Developmental Biology Moscona AA, Friedlander M (eds) Academic Press, New York, Vol 13, 1979, pp 167–197.Google Scholar
  22. 22.
    Heyner S: Antigens of trophoblast and early embryo. In: Immunol Aspects of Infertility & Fertility Regulation. Dhindsa, Schumager (eds) Amsterdam, Elsevier North Holland, Inc, 1980, pp 183–203.Google Scholar
  23. 23.
    Pinsker MC, Mintz B: Changes in cell-surface glycoproteins of mouse embryos before implantation. Proc Nat Acad Sei USA 70: 1645–1648, 1973.CrossRefGoogle Scholar
  24. 24.
    Magnuson T, Epstein CJ: Characterization of concanavalin A pre-cipitated proteins from early mouse embryos: A 2-dimensional gel electrophoresis study. Develop Bio 81: 193–199, 1981.CrossRefGoogle Scholar
  25. 25.
    Lewis WA, Wright ES: On the early development of the mouse egg. Contrib Embryol Carnegie Inst, No. 148: 115–143, 1935.Google Scholar
  26. 26.
    Calarco PG, Brown EH: An ultrastructural and cytological study of preimplantation development of the mouse. J Exp Zool 171: 253–284, 1969.PubMedCrossRefGoogle Scholar
  27. 27.
    Calarco PG, Epstein CJ: Cell surface changes during preimplantation development in the mouse. Develop Biol 32: 208–213, 1973.PubMedCrossRefGoogle Scholar
  28. 28.
    Ducibella T, Ukena T, Karnovsky M, Anderson E: Changes in cell surface and cortical cytoplasmic organization during early embryo-genesis in the preimplantation mouse embryo. J Cell Biol 74: 153–167, 1977.PubMedCrossRefGoogle Scholar
  29. 29.
    Ziomek CA, Johnson MH: Cell surface interaction induces polarization of mouse 8-cell blastomeres at compaction. Cell 21: 935–942, 1980.PubMedCrossRefGoogle Scholar
  30. 30.
    Reeve WJD, Ziomek CA: Distribution on dissociated blastomeres from mouse embryos: evidence for surface polarization at compaction. J Emb Exp Morph 62: 339–350, 1981.Google Scholar
  31. 31.
    Surani MAH, Kimber SJ, Handyside AH: Synthesis and role of cell surface glycoproteins in preimplantation mouse development. Exp Cell Res, 133: 311–340, 1981.CrossRefGoogle Scholar
  32. 32.
    Ducibella T, Anderson E: Cell shape and membrane changes in the eight-cell mouse embryo: prerequisites for morphogenesis of the blastocyst. Develop Biol 47: 45–58, 1975.PubMedCrossRefGoogle Scholar
  33. 33.
    Steinberg MS: Calcium complexing by embryonic cell surfaces: relation to intercellular adhesiveness. In: Biological Interactions in Normal and Neoplastic Growth Brennan MJ, Simpson WL (eds) Little, Brown, Boston, USA 1962, pp 127–140.Google Scholar
  34. 34.
    Atienza-Samols, SB, Pine PR, Sherman MI: Effects of tunicamycin upon glycoprotein synthesis and developmental of early mouse embryos. Develop Biol 79: 19–32, 1980.PubMedCrossRefGoogle Scholar
  35. 35.
    Rees DA, Lloyd CW, Thom D: Control of grip and stick in cell adhesion through lateral relationships of membrane glycoproteins. Nature, 267: 124–128, 1977.PubMedCrossRefGoogle Scholar
  36. 36.
    Pratt HPM: Lipids and transitions in embryos. In: Development in Mammals Johnson MH (ed) North-Holland Publishing Co, Amsterdam, Vol 3, 1978, pp 83–129.Google Scholar
  37. 37.
    Helentjaris TG, Lombardi PS, Glasgow LA: Effect of cytochalasin B on the adhesion of mouse peritoneal macrophages. J Cell Biol 64: 407–414, 1976.CrossRefGoogle Scholar
  38. 38.
    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
  39. 39.
    Kemler R, Babinet C, Eisen H, Jacob F: Surface antigen in early differentiation. Proc Nat Acad Sci, USA 74: 4449–445, 1977.CrossRefGoogle Scholar
  40. 40.
    Sherman MI, Atienza-Samols SB: Differentiation of mouse trophoblast does not require cell-cell interaction. Exp Cell Res 123: 73–78, 1979.PubMedCrossRefGoogle Scholar
  41. 41.
    Mintz B: Experimental genetic mosaicism in the mouse. In: Preimplantation Stages of Pregnancy Wolstenholme GEW, O’Connor M (eds) Churchill, Ltd, London, 1965, pp 194–207.Google Scholar
  42. 42.
    Eglitis MA, Wiley LM: Tetraploidy and early development: effects on developmental timing and embryonic metabolism J Embryol Exp Morph 66: 91–108, 1981.PubMedGoogle Scholar
  43. 43.
    Dalcq AM: Introduction to general embryology. Oxford Univ Press, Sondon/New York, 1957.Google Scholar
  44. 44.
    Wiley LM, Eglitis MA: Effects of colcemid on cavitation during mouse blastocoele formation. Exp. Cell Res. 127: 89–101, 1980.PubMedCrossRefGoogle Scholar
  45. 45.
    Wiley LM, Eglitis MA: Cell Surface and cytoskeletal elements: cavitation in the mouse preimplantation embryo. Develop Biol 86: 493–501, 1981.PubMedCrossRefGoogle Scholar
  46. 46.
    Melissinos K: Die entwicklung des eles der mause. Arch Mikr Anat 70: 577–628, 1907.CrossRefGoogle Scholar
  47. 47.
    Granholm NH, Brenner GM: Effects of cytochalasin B (CB) on the morula-to-blastocyst transformation trophoblast outgrowth in the early mouse embryo. Exp Cell Res 101: 143–153, 1976.PubMedCrossRefGoogle Scholar
  48. 48.
    Malaisse WJ, Malaisse-Lange F, Van Obberghen E, Somers G, Devis G, Ravazzola M, Orci L: Role of microtubules in the phasic pattern of insulin release. Ann N Y Acad Sci 253: 630–652, 1975.PubMedCrossRefGoogle Scholar
  49. 49.
    Izquierdo L, Lopez T, Marticorena P: Cell membrane regions in preimplantation mouse embryos. J Embryol Exp Morph 59: 89–102, 1980.PubMedGoogle Scholar
  50. 50.
    Vorbrodt A, Konwinski M, Solter D, Koprowski H: Ultrastructural cytochemistry of membrane-bound phosphatases in preimplantation mouse embryos. Develop Biol 55: 117–134, 1977.PubMedCrossRefGoogle Scholar
  51. 51.
    Nuccitelli R, Jaffe LF: The pulse current pattern generated by developing fucoid eggs. J Cell Biol 64: 636–643, 1975.PubMedCrossRefGoogle Scholar
  52. 52.
    Ducibella T, Albertini DF, Anderson E, Biggers JD: The preimplantation mammalian embryo: characterization of intercellular junctions and their appearance during development. Develop Biol 45: 231–250, 1975.PubMedCrossRefGoogle Scholar
  53. 53.
    Machen TE, Erlij D, Wooding FBP: Permeable junctional complexes. The movement of lanthanum across rabbit gallbladder and intestine. J Cell Biol 54: 302–312, 1972.PubMedCrossRefGoogle Scholar
  54. 54.
    McLaren A, Smith R: Functional test of tight junctions in the mouse blastocyst. Nature 267: 351–353, 1977.PubMedCrossRefGoogle Scholar
  55. 55.
    Benos DJ: Developmental changes in epithelial transport characteristics of preimplantation rabbit blastocysts. J Physiol 316: 191–202, 1981.PubMedGoogle Scholar
  56. 56.
    Steinberg MS: Does differential adhesion govern self-assembly process in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J Exp Zool 173: 395–434, 1970.PubMedCrossRefGoogle Scholar
  57. 57.
    Wiley LM, Spindle AI, Pedersen RA: Morphology of isolated mouse inner cell masses developing in vitro. Develop Biol 63: 1–10, 1978.PubMedCrossRefGoogle Scholar
  58. 58.
    Rowinski J, Solter D, Koprowski H: Change of concanavalin A induced agglutinability during preimplantation mouse development. Exp Cell Res 100: 404–408, 1976.PubMedCrossRefGoogle Scholar
  59. 59.
    Sobel JS, Nebel L: Changes in concanavalin A agglutinability during development of the inner cell mass and trophoblast of mouse blastocysts in vitro. J Reprod Fert 52: 239–248, 1978.CrossRefGoogle Scholar
  60. 60.
    Willison KR, Stern PL: Expression of a forssman antigenic specificity in the preimplantation mouse embryo. Cell 14: 785–793, 1978.PubMedCrossRefGoogle Scholar
  61. 61.
    Wiley LM: Early mouse embryonic cell surface antigens that are detectable by antisera to human chorionic gonadotropin (hCG). Exp Cell Res., 129: 47–54, 1980.PubMedCrossRefGoogle Scholar
  62. 62.
    Searle SF, Jenkinson EJ: Localization of trophoblast-defined surface antigens during early mouse embryogenesis. J Emb Exp Morph 43: 147–156, 1978.Google Scholar
  63. 63.
    Martin GR: Teratocarcinomas and mammalian embryogenesis. Science, 209: 768–776, 1980.PubMedCrossRefGoogle Scholar
  64. 64.
    Borland RM, Tasca RJ: Na+-dependent amino acid transport in preimplantation mouse embryos. II. Metabolic inhibitors and nature of the cation requirement. Develop Biol 46: 192–201, 1975.PubMedCrossRefGoogle Scholar
  65. 65.
    Dizio SM, Tasca RJ: Sodium-dependent amino acid transport in preimplantation mouse embryos. III. Na+-K+-ATPase-linked mechanism in blastocysts. Develop Biol 59: 198–205, 1977.PubMedCrossRefGoogle Scholar
  66. 66.
    Borland RM, Biggers JD, Lechene CP: Studies on the composition and formation of mouse blastocoele fluid using electron probe microanalysis. Develop Biol 55: 1–8, 1977.PubMedCrossRefGoogle Scholar
  67. 67.
    Cross MH, Brinster RL: Transmembrane potential of rabbit blastocyst trophoblast. Exp Cell Res 58: 125–127, 1969.PubMedCrossRefGoogle Scholar
  68. 68.
    Daniel JC: Early growth of rabbit trophoblast. Amer Naturalist 98: 85–98, 1964.CrossRefGoogle Scholar
  69. 69.
    Biggers JD: Mammalian blastocyst and amnion formation. In: The Water Metabolism of the Fetus Barnes AC, Seeds AE (eds) Charles C Thomas, New York, 1972, pp 3–31.Google Scholar
  70. 70.
    Powers RD, Tupper JT: Some electrophysiological and permeability properties of the mouse egg. Develop Biol 38: 320–331, 1974.PubMedCrossRefGoogle Scholar
  71. 71.
    Powers RD, Biggers JD: Inhibition of mouse oocyte maturation by cell membrane potential hyperpolarization. J Cell Biol 70: 352a 1976.Google Scholar
  72. 72.
    Powers RD, Tupper JT: Developmental changes in membrane transport and permeability in the early mouse embryo. Develop Biol 56: 306–315, 1977.PubMedCrossRefGoogle Scholar
  73. 73.
    Pederson RA, Spindle AI. Role of the blastocoele microenvironment in early mouse embryo differentiation. Nature, 284: 550–552, 1980.CrossRefGoogle Scholar
  74. 74.
    Kirby DRS, Potts DM, Wilson IB: On the orientation of the implanting blastocyst. J Embryol Exp Morphol 17: 527–532, 1967.PubMedGoogle Scholar
  75. 75.
    Potts M, Wilson IB: The preimplantation conceptus of the mouse at 90 hours post coitum. J Anat 102: 1–11, 1967.PubMedGoogle Scholar
  76. 76.
    Potts M: The ultrastructure of implantation in the mouse. J Anat 103: 77–90, 1968.PubMedGoogle Scholar
  77. 77.
    Sherman MI, Atienza-Samols SB: in vitro studies on the surface adhesiveness of mouse blastocysts. In: Human Fertilization Ludwig H, Tauber PF (eds) Georg Thieme Pub, Stuttgart, 1978, pp 179–183.Google Scholar
  78. 78.
    Sherman MI, Shalgi R, Rizzino A, Sellens MH, Gay S, Gay R: Changes in the surface of the mouse blastocyst at implantation. In: Maternal Recognition of Pregnancy. Ciba Fdn Series 64, 1979, pp 33–52.Google Scholar
  79. 79.
    Sobel JS, Nebel L: Concanavalin A agglutinability of developing mouse trophoblast. J Reprod Fertil 49: 399–402, 1976.Google Scholar
  80. 80.
    Brady RO, Fishman PH: Membranes of transformed mammalian cells. In: Biochemistry of Cell Walls and Membranes. Fox CF (ed) Butterworths, London, 1975.Google Scholar
  81. 81.
    Sherman MI, Gay R, Gay S, Miller EJ: Association of collagen with preimplantation and peri-implantation mouse embryos. Develop Biol 74: 470–478, 1980.PubMedCrossRefGoogle Scholar
  82. 82.
    Sherman MI, Matthaei KI: Factors involved in implantation-related events. In: Prog Reprod Biol 7: 43–53, 1980.Google Scholar
  83. 83.
    Sherman MI, Wudl LR: The implanting mouse blastocyst. In: The cell Surface in Animal Embryogenesis and Development Poste G, Nicolson G (eds) North Holland, Amsterdam, 1976, pp 81–125.Google Scholar
  84. 84.
    Huang TTF Jr, Calarco PG: Evidence for the cell surface expression of intracisternal A particle-associated antigens during early mouse development. Develop Biol 82: 388–392, 1981.PubMedCrossRefGoogle Scholar
  85. 85.
    Heyner S, Hunziker RD, Zink GL: Differential expression of minor histo-compatibility antigens on the surface of the mouse oocyte and preimplantation developmental stages. J Reprod Immunol 2: 269–280, 1980.PubMedCrossRefGoogle Scholar
  86. 86.
    Johnson LV, Calarco PG: Immunological characterization of embryonic cell surface antigens recognized by antiblastocyst serum. Develop Biol 79: 208–223, 1980.PubMedCrossRefGoogle Scholar
  87. 87.
    Artzt K, Dubois P, Benett D, Condamine H, Babinet C, Jacob F: Surface antigens common to mouse cleavage embryos and primitive teratocarcinoma cells in cultures. Proc Nat Acad Sci USA 70: 2988–2992, 1973.PubMedCrossRefGoogle Scholar
  88. 88.
    Jacob F: Immunology and differentiation; mouse teratocarcinoma and embryonic antigens. Immunol Rev 33: 3–32, 1977.PubMedCrossRefGoogle Scholar
  89. 89.
    Goldberg EH, Boyse EA, Bennett D, Scheid M, Carswell EA: Serological demonstration of H-Y (male) antigen on mouse sperm. Nature (London) 232: 478–480, 1971.CrossRefGoogle Scholar
  90. 90.
    Krco CJ, Goldberg EH: H-Y (male) antigen: detection on eight-cell mouse embryos. Science, 193: 1134–1135, 1976.PubMedCrossRefGoogle Scholar
  91. 91.
    Solter D, Knowles BB: Monoclonal antibody defining a stagespecific mouse embryonic antigen (SSEA-1). Proc Nat Acad Sci USA 75: 5565–5569, 1978.PubMedCrossRefGoogle Scholar
  92. 92.
    Gooi HC, Feizi T, Kapadia A, Knowles BB, Solter D, Evans MJ. Stage-specific embryonic antigen involves 1–3 fucosylated type 2 blood group chains. Nature, 292: 156–158, 1981.PubMedCrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Lynn M. Wiley
    • 1
  1. 1.Department of Human AnatomyUniversity of CaliforniaDavisUSA

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