Relationship between the Programs for Implantation and Trophoblast Differentiation

  • Michael I. Sherman
  • Martin H. Sellens
  • Sui Bi Atienza-Samols
  • Anna C. Pai
  • Joel Schindler

Abstract

Trophoblast cells are specialized cells that appear to be involved at one time or another during pregnancy in several functions essential to the well-being of the fetus. These functions include the attachment of the conceptus to the uterine wall, the acquisition of nutrients from the mother, and the protection of the fetus from immunologic rejection. As trophoblast cells are capable of metabolizing steroids (albeit to varying degrees and beginning at different times, depending upon the species), they might also play a role in fetal endocrinology. In studies on murine trophoblast, a number of biochemical properties have been observed that are exhibited neither by the early embryo per se nor by most other extraembryonic cell types (Table 1). We therefore consider these properties to be indicators of trophoblast differentiation, and we assume that some or all of these biochemical markers are involved in the specialized functions of these cells.

Keywords

Polypeptide Compaction Progesterone Cavitation Oligosaccharide 

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References

  1. Atienza-Samols, S. B., Pine, P., and Sherman, M. I., 1980, Effects of tunicamycin upon glycoprotein synthesis and development of early mouse embryos. Dev. Biol. 79: 19.CrossRefGoogle Scholar
  2. Auerbach, S., and Brinster, R. L., 1967, Lactate dehydrogenase isozymes in the early mouse embryo, Exp. Cell Res. 46: 89.CrossRefGoogle Scholar
  3. Auerbach, S., and Brinster, R. L., 1968, Lactate dehydrogenase isozymes in mouse blastocyst cultures, Exp. Cell Res. 53: 313.CrossRefGoogle Scholar
  4. Barlow, P. W., and Sherman, M. I., 1972, The biochemistry of differentiation of mouse trophoblast cells: Studies on polyploidy, J. Embryol. Exp. Morphol. 27: 447.Google Scholar
  5. Barlow, P. W., Owen, D. A. J., and Graham, C., 1972, DNA synthesis in the preimplantation mouse embryo, J. Embryol. Exp. Morphol. 27: 431.Google Scholar
  6. Bode, V. C., and Dziadek, M. A., 1979, Plasminogen activator secretion during mammalian embryogenesis. Dev. Biol. 73: 272.CrossRefGoogle Scholar
  7. Cantor, J., Shapiro, S. S., and Sherman, M. I., 1976, Chondroitin sulfate synthesis by mouse embryonic, extraembryonic and teratoma cells in vitro. Dev. Biol. 50: 367.CrossRefGoogle Scholar
  8. Chew, N. J., and Sherman, M. I., 1975, Biochemistry of differentiation of mouse trophoblast: A5,3 β-hydroxysteroid dehydrogenase, Biol. Reprod. 12: 351.CrossRefGoogle Scholar
  9. Cole, R. J., and Paul, J., 1%5, Properties of cultured preimplantation mouse and rabbit embryos, and cell strains derived from them, in: Preimplantation Stages in Pregnancy (G. E. W. Wolstenholme and M. O’Connor, eds.), pp. 82–112, Academic Press, New York.Google Scholar
  10. Damsky, C. H., Levy-Benshimol, A., Buck, C. A., and Warren, L., 1979, Effect of tunicamycin on the synthesis, intracellular transport and shedding of membrane glycoproteins in BHK cells, Exp. Cell Res. 119: 1.CrossRefGoogle Scholar
  11. Deane, H. W., Rubin, B. L., Driks, E. C., Lobel, B. L., and Leipsner, G., 1962, Trophoblastic giant cells in placentas of rats and mice and their probable role in steroid-hormone production. Endocrinology 70: 407.CrossRefGoogle Scholar
  12. Duksin, D., and Bomstein, P., 1977, Changes in surface properties of normal and transformed cells caused by tunicamycin, an inhibitor of protein glycosylation, Proc. Natl. Acad. Sci. USA 74: 3433.CrossRefADSGoogle Scholar
  13. Erickson, R. P., and Pedersen, R. A., 1975, In vitro development of embryos, J. Exp. Zool. 193: 377.CrossRefGoogle Scholar
  14. Glass, R. H., Spindle, A. I., and Pedersen, R. A., 1979, Mouse embryo attachment to substratum and interaction of trophoblast with cultured cells, J. Exp. Zool. 208: 327.CrossRefGoogle Scholar
  15. Goldstein, L. S., Spindle, A. I., and Pedersen, R. A., 1975, X-Ray sensitivity of the preimplantation mouse embryo in vitro, Radiat. Res. 62: 276.Google Scholar
  16. Greene, R. M., and Pratt, R. M., 1977, Inhibition by diazo-oxo-norleucine (don) of rat palatal glycoprotein synthesis and epithelial cell adhesion in vitro, Exp. Cell Res. 105: 27.CrossRefGoogle Scholar
  17. Gwatkin, R. B. L., 1966a, Defined media and development of mammalian eggs in vitro, Ann. N.Y. Acad. Sci. 139: 79.CrossRefADSGoogle Scholar
  18. Gwatkin, R. B. L., 1966b, Amino acid requirements for attachment and outgrowth of the mouse blastocyst in vitro, J. Cell. Physiol. 68: 335.CrossRefGoogle Scholar
  19. Handyside, A. H., and Johnson, M. H., 1978, Temporal and spatial patterns of the synthesis of tissue specific polypeptides in the preimplantation mouse embryo, J. Embryol. Exp. Morphol. 44: 191.Google Scholar
  20. Jacob, S., Sadjel, E., Muecke, W., and Munro, H., 1970, Soluble RNA polymerases of rat liver nuclei: Properties, template specificity and amanitin responses in vitro and in vivo. Cold Spring Harbor Symp. Quant. Biol. 35: 681.Google Scholar
  21. Jenkinson, E. J., and Wilson, I. B., 1973, in vitro studies on the control of trophoblast outgrowth in the mouse, J. Embryol. Exp. Morphol. 30: 21.Google Scholar
  22. Jetten, A. M., Jetten, M. E. R., and Sherman, M. I., 1979, Analyses of cell surface and secreted proteins of primary cultures of mouse extraembryonic tissues. Dev. Biol. 70: 89.CrossRefGoogle Scholar
  23. Johnson, M. H., Handyside, A. H., and Braude, P. R., 1977, Control mechanisms in early mammalian development, in: Development in Mammals, Vol. 2 ( M. H. Johnson, ed.), pp. 67–97, Elsevier/North-Holland, Amsterdam.Google Scholar
  24. Levey, I., and Brinster, R. L., 1978, Effects of α-amanitin on RNA synthesis by mouse embryos in culture, J. Exp. Zool. 203: 351.CrossRefGoogle Scholar
  25. Lindell, T. F., Weinberg, F., Morris, P., Roeder, R., and Rutter, W., 1970, Specific inhibition of nuclear RNA polymerase II by α-amanitin. Science 170: 447.CrossRefADSGoogle Scholar
  26. Mintz, B., 1962, Experimental study of the developing mammalian egg: Removal of the zona pellucida. Science 138: 594.CrossRefADSGoogle Scholar
  27. Monk, M., and Petzholdt, U., 1977, Control of inner cell mass development in cultured mouse blastocysts. Nature (London) 265: 338.CrossRefADSGoogle Scholar
  28. Olden, K., Pratt, R. M., and Yamada, K. M., 1979, Selective cytotoxicity of tunicamycin for transformed cells. Int. J. Cancer 24: 60.CrossRefGoogle Scholar
  29. Pratt, R. M., Yamada, K. M., Olden, K., Ohanian, S. H., and Hascall, V. C., 1979, Tunicamycin-induced alterations in the synthesis of sulfated proteoglycans and cell surface morphology in the chick embryo fibroblast, Exp. Cell Res. 118: 245.CrossRefGoogle Scholar
  30. Prives, J., and Shinitzky, M., 1977, Increased membrane fluidity precedes fusion of muscle cells. Nature (London) 26S: 16l.Google Scholar
  31. Rizzino, A., and Sherman, M. I., 1979, Development and differentiation of mouse blastocysts in serum-free medium, Exp. Cell Res. 121: 221.CrossRefGoogle Scholar
  32. Rossant, J., and Papaioannou, V. E., 1977, The biology of embryogenesis, in: Concepts in Mammalian Embryogenesis ( M. I. Sherman, ed.), pp. 1–36, MIT Press, Cambridge, Mass.Google Scholar
  33. Sellens, M. H., and Sherman, M. I., 1980, Effects of culture conditions on the developmental programme of mouse blastocysts, J. Embryol. Exp. Morphol. 56: 1.Google Scholar
  34. Shalgi, R., and Sherman, M. I., 1979, Scanning electron microscopy of the surface of normal and implantation delayed mouse blastocysts during development in vitro, J. Exp. Zool. 210: 69.CrossRefGoogle Scholar
  35. Sherman, M. I., 1972a, The biochemistry of differentiation of mouse trophoblast cells: Esterase, Exp. Cell Res. 75: 449.CrossRefGoogle Scholar
  36. Sherman, M. I., 1972b, The biochemistry of differentiation of mouse trophoblast cells: Alkaline phosphatase. Dev. Biol. 27: 337.CrossRefGoogle Scholar
  37. Sherman, M.I., 1975, Esterase isozymes during mouse embryonic development in vivo and in vitro in: Isozymes (C. L. Market, ed.), Vol. III, pp. 83–98, Academic Press, New York.Google Scholar
  38. Sherman, M.I., 1978, Implantation of mouse blastocysts in vitro, in: Methods in Mammalian Reproduction ( J. C. Daniel, ed.), pp. 247–257, Academic Press, New York.Google Scholar
  39. Sherman, M. I., 1979, Developmental biochemistry of preimplantation mammalian embryos, Armu. Rev. Biochem. 48: 443.CrossRefGoogle Scholar
  40. Sherman, M. I., 1979, Developmental biochemistry of preimplantation mammalian embryos, Armu. Rev. Biochem. 48: 443.CrossRefGoogle Scholar
  41. Sherman, M. I., and Atienza, S. B., 1977, Production and metabolism of progesterone and androstenedione by cultured mouse blastocysts, Biol. Reprod. 16: 190.CrossRefGoogle Scholar
  42. Sherman, M. I., and Atienza-Samols, S. B., 1978, In vitro studies on the surface adhesiveness of mouse blastocysts, in Human Fertilization ( H. Ludwig and P. F. Trauber, eds.), pp. 179–183, Thieme, Stuttgart.Google Scholar
  43. Sherman, M. I., and Atienza-Samols, S. B., 1979, Enzyme analyses of mouse extraembryonic tissues, J. Embryol. Exp. Morphol. 52: 127.Google Scholar
  44. Sherman, M. I., and Chew, N. J., 1972, Detection of maternal esterase in mouse embryonic tissues, Proc. Natl. Acad. Sci. USA 69: 2551.CrossRefADSGoogle Scholar
  45. Sherman, M. I., and Salomon, D. S., 1975, The relationships between the early mouse embryo and its environment, in The Developmental Biology of Reproduction (C. L. Markert and J. Papaconstantinou, eds.), pp. 211 in. Academic Press, New York.Google Scholar
  46. Sherman, M. I., and Wudl, L. W., 1976, The implanting mouse blastocyst, in: The Cell Surface in Animal Embryogenesis and Development ( G. Poste and G. L. Nicolson, eds.), pp. 81–125, Elsevier/North-Holland, Amsterdam.Google Scholar
  47. Sherman, M. I., and Wudl, L. R., 1977, T-Complex mutations and their effects, in: Concepts in Mammalian Embryogenesis ( M.I. Sherman, ed.), pp. 136–234, MIT Press, Cambridge, Mass.Google Scholar
  48. Sherman, M. I., Shalgi, R., Rizzino, A., Sellens, M. H., Gay S., and Gay, R., 1979, Changes in the surface of the mouse blastocyst at implantation, Ciba Found. Symp. 64: 33.Google Scholar
  49. Sherman, M. I., Gay, R., Gay, S., and Miller, E. J., 1980, Association of collagen with preimplantation and peri-implantation mouse embryos. Dev. Biol. 74: 470.CrossRefGoogle Scholar
  50. Spielmann, H., Eibs, H.-G., Jacob-Müller, U., and Bischoff, R., 1978, Expression of lactate dehydrogenase isozyme 5 (LDH-5) in cultured mouse blastocysts in the absence of implantation and outgrowth, Biochem. Genet. 16: 191.CrossRefGoogle Scholar
  51. Spindle, A. I., and Pedersen, R. A., 1973, Hatching, attachment and outgrowth of mouse blastocysts in vitro: Fixed nitrogen requirements, J. Exp. Zool. 186: 305.CrossRefGoogle Scholar
  52. Stirpe, F., and Fiume, L., 1967, Studies on the pathogenesis of liver necrosis by α-amanitin, Biochem. J. 105: 779.Google Scholar
  53. Strickland, S., Reich, E., and Sherman, M. I., 1976, Plasminogen activator in early embryogenesis: Enzyme production by trophoblast and parietal endoderm. Cell 9: 231.CrossRefGoogle Scholar
  54. Struck, D. K., and Lennarz, W. J., 1977, Evidence for the participation of saccharide-lipids in the synthesis of the oligosaccharide chain of ovalbumin, J. Biol. Chem. 252–1007.Google Scholar
  55. Takatsuki, A., and Tamura, G., 1971, Tunicamycin, a new antibiotic. III. Reversal of the antiviral activity of tunicamycin by aminosugars and other derivatives, J. Antibiot. 24: 232.Google Scholar
  56. Takatsuki, A., Kohno, K., and Tamura, G., 1975, Inhibition of biosynthesis of polyisoprenol sugars in chick embryo microsomes by tunicamycin, Agr. Biol. Chem. 39: 2089.CrossRefGoogle Scholar
  57. Tkacz, J. S., and Lampen, J. O., 1975, Tunicamycin inhibition of polyisoprenol N-acetyglucosaminyl pyrophosphate formation of calf liver microsomes, Biochem. Biophys. Res. Commun. 65: 248.CrossRefGoogle Scholar
  58. Van Blerkom, J., Barton, S. C., and Johnson, M. H., 1976, Molecular differentiation in the preimplantation mouse embryo, Nature (London) 259: 319.CrossRefGoogle Scholar
  59. Whitten, W. K., 1971, Nutrient requirements for the culture of preimplantation embryos in vitro, Adv. Biosci. 6: 129.Google Scholar
  60. Wudl, L. R., and Sherman, M. I., 1978, In vitro studies of mouse embryos bearing mutations in the T complex: t6, J. Embryol. Exp. Morphol. 48: 127.Google Scholar
  61. Wudl, L. R., Sherman, M. I., and Hillman, N., 1977, Nature of lethality of t mutations in embryos, Nature (London) 270: 137.CrossRefADSGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Michael I. Sherman
    • 1
  • Martin H. Sellens
    • 1
  • Sui Bi Atienza-Samols
    • 1
  • Anna C. Pai
    • 1
  • Joel Schindler
    • 1
  1. 1.Roche Institute of Molecular BiologyNutleyUSA

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