Separated Cell Types as Analytical Tools in the Study of Decidualization and Implantation

  • Stanley R. Glasser
  • Shirley A. McCormack


Various strategies used by different species to assure successful blastocyst-endometrial interaction have evolved. The advantages and limitations of the decidual cell reaction (DCR) as a model for studying these events have been recognized (Psychoyos, 1973; Glasser and Clark, 1975; Glasser and McCormack, 1980a,c). Concise descriptions of the sequential relationships of the steroid hormones (Psychoyos, 1973; Glasser and Clark, 1975) and the different hormonal responses of epithelial and stromal cells have been provided (Martin and Finn, 1968; Tachi et al., 1972; Martin et al., 1973a,b). These researches have validated the determinant role of progesterone in the development of uterine sensitivity. Certain species require estrogen to complete the maturation of the sensitive uterus to the final stages of uterine receptivity for ovum implantation. Detailed cytological, ultrastructural (Nilsson, 1970; Enders and Schlafke, 1971; Schlafke and Enders, 1975; Sherman and Wudl, 1976), and physiological correlates (Meyers, 1970; Psychoyos, 1973; Glasser and Clark, 1975; Glasser and McCormack, 1979) of these events are also part of the literature.


Stromal Cell Mouse Uterus Myometrial Cell Individual Cell Type Uterine Cell 
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  1. Alberga, A., and Baulieu, E.-E., 1968, Binding of estradiol in castrated rat endometrium in vivo and in vitro, Mot. Pharmacol. 4: 311.Google Scholar
  2. Anderson, J. M., Clark, J. H., and Peck, E. J., 1972, The relationship between nuclear receptor-oestrogen binding and uterotrophic responses, Biochem. Biophys. Res. Commun. 48:1460. Clark, B. F., 1973, The effect of oestrogen and progesterone on uterine cell division and epithelial morphology in spayed-hypophysectomized rats, J. Endocrinol. 56: 341.Google Scholar
  3. Clark, J. H., and Peck, E. J., 1976, Nuclear retention of receptor-estrogen complex and nuclear acceptor sites. Nature (London) 260: 635.CrossRefADSGoogle Scholar
  4. Clark, J. H., Peck, E. J., and Glasser, S. R., 1977, Mechanism of action of sex steroids in the female, in: Reproduction in Domestic Animals ( H. H. Cole and P. T. Cupps, eds.), 3rd ed., p. 143, Academic Press, New York.Google Scholar
  5. Clark, J. H., McCormack, S. A., Padykula, H., Markaverich, B., and Hardin, J. W., 1979, Biochemical and morphological changes stimulated by the nuclear binding of the estrogen receptor, in: Effects of Drugs on the Cell Nucleus (H. Busch, S. T. Crooke, and Y. Daskal, eds.), p. 381, Academic Press, New York. Cunha, G. R., 1976, Epithelial-stromal interactions in development of the urogenital tract. Int. Rev. Cytol. 47: 137.Google Scholar
  6. Enders, A. C., and Schlafke, S., 1971, Penetration of the uterine epithelium during implantation in the rabbit. Am. J. Anat. 132: 219.CrossRefGoogle Scholar
  7. Finn, C. A., 1974, the induction of implantation in mice by actinomycin D, J. Endocrinol. 60: 199.Google Scholar
  8. Finn, C. A., and Martin, L., 1973, Endocrine control of gland proliferation in the mouse uterus, Biol. Reprod. 8: 585.Google Scholar
  9. Galand, P., Leroy, F., and Cretien, J., 1971, Effect of oestradiol on cell proliferation and histological changes in the uterus and vagina of mice, J. Endocrinol. 49: 243.CrossRefGoogle Scholar
  10. Gerschenson, L. E., and Beriiner, J. A., 1976, Further studies on the regulation of cultured rabbit endometrial cells by diethylstilbestrol and progesterone, J. Steroid Biochem. 7: 159.CrossRefGoogle Scholar
  11. Gerschenson, L. E., Berliner,, J., and Yang, J., 1974, Diethystilbestrol and progesterone regulation of cultured rabbit endometrial cell growth, Cancer Res. 34: 2873.Google Scholar
  12. Glasser, S. R., and Clark, J. H., 1975, A determinant role for progesterone in the development of uterine sensitivity to decidualization and ovoimplantation, in: The Developmental Biology of Reproduction ( C. Markert and J. Papaconstantinou, eds.), p. 311, Academic Press, New York.Google Scholar
  13. Glasser, S. R., and McCormack, S. A., 1979, Estrogen-modulated uterine gene transcription in relation to decidualization, Endocrinology 104: 1112.CrossRefGoogle Scholar
  14. Glasser, S. R., and McCormack, S. A., 1980a, Functional development of rat trophoblast and decidual cells during establishment of the hemochorial placenta, in: The Development of Responsiveness to Steroid Hormones ( A.M. Kaye and M. Kaye, eds.), p. 165, Pergamon, London.Google Scholar
  15. Glasser, S. R., and McCormack, S. A., 1980b, Analyses of hormonal responses of the rat endometrium by the use of separated uterine cell types, in: The Endometrium: Eighth Brook Lodge Conference on Problems of Reproductive Physiology (F. A. Kimball, ed. ), Spectrum Publications, p. 173.Google Scholar
  16. Glasser, S. R., and McCormack, S. A., 1980b, Analyses of hormonal responses of the rat endometrium by the use of separated uterine cell types, in: The Endometrium: Eighth Brook Lodge Conference on Problems of Reproductive Physiology (F. A. Kimball, ed. ), Spectrum Publications, p. 173.Google Scholar
  17. Gorski, J., DeAngelo, A. B., and Bamea, A., 1971, Estrogen actions: The role of specific RNA and protein synthesis, in: The Sex Steroids ( K. W. McKems, ed.), p. 181, Appleton-Century-Crofts, New York.Google Scholar
  18. Heald, P. J., Govan, A. D. T., and O’Grady, J. E., 1975, A simple method for the preparation of luminal epithelial and stromal cells from rat uterus, J. Reprod. Fertil. 42: 593.CrossRefGoogle Scholar
  19. Hsueh, A. J. W., Peck, E. J., and Clark, J. H., 1976, Control of uterine estrogen receptor levels by progesterone. Endocrinology 98: 438.CrossRefGoogle Scholar
  20. Jackson, V., and Chalkley, R., 1974, The binding of estradiol-17/8 to the bovine endometrial nuclear membrane, J. Biol. Chem. 249: 1615.Google Scholar
  21. Kirk, D., King, R. J. B., Heyes, J., Peachey, L., Hirsch, P. J., and Taylor, W. T., 1978, Normal human endometrium in cell culture. I. Separation and characterization of epithelial stromal components. In Vitro 14: 651.CrossRefGoogle Scholar
  22. Kirkland, J. L., La Pointe, L., Justin, E., and Stancel, G. M., 1979, Effects of estrogen on mitosis in individual cell types of the immature rat uterus, Biol. Reprod. 21: 269.CrossRefGoogle Scholar
  23. Koligan, K. B., and Stormshak, F., 1977, Nuclear and cytoplasmic estrogen receptors in ovine endometrium during the estrous cycle. Endocrinology 101: 524.CrossRefGoogle Scholar
  24. Lamerton, L. F., 1973, The mitotic cycle and cell population control, in: The Cell and Cancer (A. R. Currie, ed.), J. Clin. Pathol. Suppl. 7, p. 19.Google Scholar
  25. Leroy, F. C., Bogaert, C., and Van Hoek, J., 1976, Stimulation of cell division in the endometrial epithelium of the rat by uterine distention, J. Endocrinol. 70: 517.CrossRefGoogle Scholar
  26. Liszczak, T. M., Richardson, G. S., MacLaughlin, D. T., and Komblith, P. L., 1977, Ultrastructure of human endometrial epithelium in monolayer culture with and without steroid hormones. In Vitro 13: 344.CrossRefGoogle Scholar
  27. McCormack, S. A., and Glasser, S. R., 1976, A high affinity estrogen binding protein in rat placental trophoblast, Endocrinology 99: 701.CrossRefGoogle Scholar
  28. McCormack, S. A., and Glasser, S. R., 1978, Ontogeny and regulation of a rat placental estrogen receptor, Endocrinology 102: 273.CrossRefGoogle Scholar
  29. McCormack, S. A., and Glasser, S. R., 1980a, Differential response of individual uterine cell types from immature rats treated with estradiol. Endocrinology 106: 1634.CrossRefGoogle Scholar
  30. McCormack, S. A., and Glasser, S. R., 1980b, Hormone production by rat blastocysts and mid-gestation trophoblast in vitro, in: The Endometrium: Eighth Brook Lodge Conference on Problems of Reproductive Physiology (F. A. Kimball, ed. ). Spectrum Publications, p. 145.Google Scholar
  31. Makler, A., and Eisenfeld, A. J., 1974, In vitro binding of 3H-estradiol to macromolecules from the human endometrium, J. Clin. Endocrinol. Metab. 38: 1974.CrossRefGoogle Scholar
  32. Martel, D., and Psychoyos, A., 1976, Endometrial content of nuclear estrogen receptor and receptivity for ovoimplantation in the rat. Endocrinology 99: 470.CrossRefGoogle Scholar
  33. Martel, D., and Psychoyos, A., 1978, Progesterone-induced oestrogen receptors in the rat uterus, J. Endocrinol. 76: 145.CrossRefGoogle Scholar
  34. Martin, L., and Finn, C. A., 1968, Hormonal regulation of cell divisron in epithelial and connective tissues of the mouse utems, J. Endocrinol. 41: 363.CrossRefGoogle Scholar
  35. Martin, L., Finn, C. A., and Trinder, G., 1973a, Hypertrophy and hyperplasia in the mouse uterus after oestrogen treatment: An auto-radiographic study, J. Endocrinol. 56: 133.CrossRefGoogle Scholar
  36. Martin, L., Finn, C. A., and Trinder, G., 1973b, DNA synthesis in the endometrium of progesterone-treated mice, J. Endocrinol. 56: 303.CrossRefGoogle Scholar
  37. Martin, L., Das, R. M., and Finn, C. A., 1973c, The inhibition by progesterone of uterine proliferation in the mouse, J. Endocrinol. 57: 549.CrossRefGoogle Scholar
  38. Martin, L., Pollard, J. W., and Fagg, B., 1976, Oestriol, oestradiol-17β and the proliferation and death of uterine cells, J. Endocrinol. 69: 103.CrossRefGoogle Scholar
  39. Meyers, K., 1970, Hormonal requirements for the maintenance of oestradiol-induced inhibition of uterus sensitivity in the ovariectomized rat, J. Endocrinol. 46: 341.CrossRefGoogle Scholar
  40. Nilsson, O., 1970, Some ultrastructural aspects of ovo-implantation, in: Ovo-implantation, Human Gonadotropins and Prolactin P. O. Hubinont, F. Leroy, C. Robyn, and P. Leleux, eds.), p. 52, Karger, Basel.Google Scholar
  41. O’Malley, B. W., and Means, A. R., 1974, Female steroid hormones and target cell nuclei. Science 183: 610.CrossRefADSGoogle Scholar
  42. Peel, S., and Bulmer, D., 1975, A study of proliferative activity of the uterine epithelium of the pregnant rat in relationship to morphogenesis of the new lumen, J. Reprod. Fertil. 42: 189.CrossRefGoogle Scholar
  43. Pietras, R. J., and Szego, C. M., 1975a, Steroid hormone responsive isolated endometrial cells. Endocrinology 96: 946.CrossRefGoogle Scholar
  44. Pietras, R. J., and Szego, C. M., 1975b, Surface modifications evoked by estradiol and diethylstilbestrol in isolated endometrial cells: Evidence from lectin probes and extracellular release of lysomal protease. Endocrinology 97: 1447.CrossRefGoogle Scholar
  45. Pollard, J. W., and Martin, L., 1975, Cystoplasmic and nuclear non-histone proteins and mouse uterine cell proliferation, Mol. Cell. Endocrinol. 2: 183.CrossRefGoogle Scholar
  46. Psychoyos, A., 1973, Endocrine control of egg implantation, in: Handbook of Physiology (Sect. 7, Endocrinology, Vol. II, Part 2) ( R. O. Creep and E. B. Astwood, eds.), p. 187, Am. Physiol. Soc., Washington, D.C.Google Scholar
  47. Psychoyos, A., 1974, Hormonal control of ovo-implantation, Vitam. Horm. 32: 201.CrossRefGoogle Scholar
  48. Sananes, N., Weiller, S., Baulieu, E./E., and LeGaoscagne, C., 1978,/n vitro decidualization of rat endometrial cells. Endocrinology 103: 86.Google Scholar
  49. Schlafke, S., and Enders, A. C., 1975, Cellular basis of interaction between trophoblast and uterus at implantation, Reprod. 12: 41.CrossRefGoogle Scholar
  50. Sherman, M. I., and Wudl, L. R., 1976, The implanting mouse blastocyst, in: The Cell Surface in Animal Embryogenesis and Development ( C. Poste and C. L. Nicholson, eds.), p. 81, North-Holland, Amsterdam.Google Scholar
  51. Smith, J. A., and Martin, L., 1974, Regulation of cell proliferation, in: Cell Cycle Controls ( C. M. Padilla, I. L. Cameron, and A. Zimmerman, eds.), p. 43, Academic Press, New York.Google Scholar
  52. Smith, J. A., Martin, L., King, R. J. B., and Vertes, M., 1970, Effects of oestradiol-17β and progesterone on total and nuclear-protein synthesis in epithelial and stromal tissues of the mouse uterus, and of progesterone on the ability of these tissues to bind oestradiol-17β, Biochem. J. 119: 773.Google Scholar
  53. Sonnenschein, C., Weiller, S., Farookhi, R., and Soto, A. M., 1974, Characterization of an estrogen-sensitive cell line established from normal rat endometrium, Cancer Res. 34: 3147.Google Scholar
  54. Tachi, C., Tachi, S., and Lindner, H. R., 1972, Modification by progesterone of oestradinol-induced cell proliferation, RNA synthesis and oestradiol distribution in the rat uterus, J. Reprod. Fertil. 31: 59.CrossRefGoogle Scholar
  55. Tseng, L., 1978, Steroid specificity in the stimulation of human endometrial estradiol dehydragenase, Endocrinology 102: 1398.CrossRefGoogle Scholar
  56. Vladimirsky, F., Chen, L., Amsterdam, A., Zor, U., and Lindner, H. R., 1977, Differentiation of decidual cells in cultures of rat endometrium, J. Reprod. Fertil. 49: 61.CrossRefGoogle Scholar
  57. West, N. B., Norman, R. L., Sandow, B. A., and Brenner, R. M., 1978, Hormonal control of nuclear estradiol receptor content and the luminal epithelium in the uterus of the golden hamster. Endocrinology 103: 1732.CrossRefGoogle Scholar
  58. Williams, D., and Gorski, J., 1973, Preparation and characterization of free cell suspensions from the immature rat uterus. Biochemistry 12: 297.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Stanley R. Glasser
    • 1
  • Shirley A. McCormack
    • 1
  1. 1.Department of Cell BiologyBaylor College of MedicineHoustonUSA

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