The Implantation Reaction

  • Margaret B. Parr
  • Earl L. Parr


The evolution of the reproductive process has resulted in the development of elaborate adaptive mechanisms to ensure the survival of the offspring. In viviparous animals such adaptations include the development of complex and diverse forms of implantation and placentation in order to support the attachment and development of embryos in utero. The implantation process exhibits remarkable diversity among species, most prominently in the extent of trophoblastic invasion into the uterus. Yet the general aim of implantation is accomplished in all species: to attach the embryo to the uterine wall and to establish an intimate union between maternal and fetal tissues so that an exchange of nutrients and waste products can occur. The details of the earliest interactions between the blastocyst and endometrium have been the focus of extensive study. It is our purpose to summarize some of the more important developments in this field since the publication of Finn’s fine review of the subject in the second edition of this book (Finn, 1977). In this chapter we have chosen to discuss four aspects of the implantation process: (1) adhesion of the trophoblast to the uterine epithelium; (2) increased vascular permeability at implantation sites; (3) the decidual cell reaction; and (4) loss of epithelial cells surrounding the implanting blastocyst. Our discussion is based primarily on the results of investigations using common laboratory animals, namely, the rat, mouse, and rabbit. In addition, other recent reviews and symposia may be of interest to the reader (Weitlauf, 1979; Glasser and McCormack, 1981; Finn, 1980; Leroy et al., 1980; Glasser and Bullock, 1981; Dey and Johnson, 1980; Kearns and Lala, 1983; Bell, 1983; Kennedy, 1983a; Chévez, 1984; Enders et al., 1983, 1985; Enders and Schlafke, 1986; Yoshinaga et al., 1986).


Implantation Site Luminal Epithelium Decidual Cell Uterine Epithelium Mouse Blastocyst 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrahamsohn, P. A., 1983, Ultrastructural study of the mouse antimesometrial decidua, Anat. Embryol. 166: 263–274.PubMedCrossRefGoogle Scholar
  2. Abrahamsohn, P. A., Lundkvist, O., and Nilsson, O., 1983, Ultrastructure of the endometrial blood vessels during implantation of the rat blastocyst, Cell Tissue Res. 229: 169–280.CrossRefGoogle Scholar
  3. Anderson, T. L., and Hoffman, L. H., 1984, Alterations in epithelial glycocalyx of rabbit uteri during early pseudopregnancy and pregnancy, and following ovariectomy, Am. J. Anat. 171: 321–334.PubMedCrossRefGoogle Scholar
  4. Anderson, T. L., Olson, G. E., and Hoffman, L. H., 1986, Stage-specific alterations in the apical membrane glycoproteins of endometrial epithelial cells related to implantation in rabbits, Biol. Reprod. 34: 701–720.PubMedCrossRefGoogle Scholar
  5. Anteby, S. O., Bauminger, S., Zor, U., and Lindner, H. R., 1975, Prostaglandin synthesis in decidual tissue of the rat, Prostaglandins 10: 991–999.PubMedCrossRefGoogle Scholar
  6. Atienza-Samols, S. B., Pine, P. P., and Sherman, M. I., 1980, Effects of tunicamycin upon glycoprotein synthesis and development of early mouse embryos, Dev. Biol. 79: 19–32.PubMedCrossRefGoogle Scholar
  7. Basuray, R., and Gibori, G., 1980, Luteotropic action of the decidual tissue of the pregnant rat, Biol. Reprod. 23: 507–512.Google Scholar
  8. Basuray, R., Jaffee, R. C., and Gibori, G., 1983, Role of decidual luteotropin and prolactin in the control of luteal cell receptors for estradiol, Biol. Reprod. 28: 551–556.Google Scholar
  9. Bazer, F. W., and First, N. L., 1983, Pregnancy and parturition, J. Anim. Sci. 57 (Suppl. 2): 425–460.PubMedGoogle Scholar
  10. Beer, A. E., and Billingham, R. E., 1974, Host responses to intrauterine tissue, cellular and fetal allografts, J. Reprod. Fértil. ( Suppl. ) 21: 59–88.Google Scholar
  11. Bekairi, A. M., Sanders, R. B., and Yochim, J. M., 1984, Uterine adenylate cyclase activity during the estrous cycle and early progestation in the rat: Responses to fluoride activation and decidual induction, Biol. Reprod. 31: 742–751.PubMedCrossRefGoogle Scholar
  12. Bell, B. C., 1983, Decidualization: Regional differentiation and associated function, Oxford Rev. Reprod. Biol. 5: 220–271.Google Scholar
  13. Bell, S. C., and Searle, R. F., 1981, Differentiation of decidual cells in mouse endometrial cell cultures, J. Reprod. Fértil. 61: 425–433.PubMedCrossRefGoogle Scholar
  14. Bell, S. C., Reynolds, S., and Heald, P. J., 1977, Uterine protein synthesis during the early stages of pregnancy in the rat, J. Reprod. Fértil. 49: 177–181.PubMedCrossRefGoogle Scholar
  15. Bell, S. C., Hamer, J., and Heald, P. J., 1980, Induced protein and deciduoma formation in rat uterus, Biol. Reprod. 23: 935–940.PubMedCrossRefGoogle Scholar
  16. Bernard, O., and Rachman, F., 1980, Immunological aspects of the decidual cell reaction, in: Progress in Reproductive Biology, Volume 7 ( F. Leroy, C. A. Finn, A. Psychoyos, and P. O. Hubinont, eds.), S. Karger, Basel, pp. 135–142.Google Scholar
  17. Bernard, O., Scheid, M., Ripoche, M. A., and Bennett, D., 1978, Immunological studies of mouse decidual cells. I. Membrane markers of decidual cells in the days after implantation, J. Exp. Med. 148: 580–591.Google Scholar
  18. Biggers, J. D., Leonov, B. V., Baskar, J. F., and Fried, J., 1978, Inhibition of hatching of mouse blastocysts in vitro by prostaglandin antagonists, Biol. Reprod. 19: 519–533.Google Scholar
  19. Biggers, J. D., Baskar, J. F., and Torchianan, D. F., 1981, Reduction of fertility of mice by the intrauterine injection of prostaglandin antagonists, J. Reprod. Fértil. 63: 365–372.PubMedCrossRefGoogle Scholar
  20. Bill, A., Tornquist, P., and Aim, A., 1980, Permeability of the intraocular blood vessels, Trans. Ophthalmol. Soc. U. K. 100: 332–336.Google Scholar
  21. Bishop, C. J., and Whiting, V. A., 1983, The role of natural killer cells in the intravascular death of intravenously injected murine tumour cells, Br. J. Cancer 48: 441–444.PubMedCrossRefGoogle Scholar
  22. Boshier, D. P., 1970, The Pontamine Blue reaction in pregnant sheep uteri, J. Reprod. Fértil. 22: 595–596.PubMedCrossRefGoogle Scholar
  23. Boshier, D. P., 1976, Effects of the rat blastocyst on neutral lipids and nonspecific esterases in the uterine luminal epithelium at the implantation area, J. Reprod. Fértil. 46: 245–247.PubMedCrossRefGoogle Scholar
  24. Boshier, D. P., Fairclough, R. J., and Holloway, H., 1987, Assessment of sheep blastocyst effects on neutral lipids in the uterine caruncular epithelium, J. Reprod. Fértil. 79: 569–573.Google Scholar
  25. Boving, B. G., 1962, Anatomical analysis of rabbit trophoblast invasion, Contrib. Embryol. 37: 33–54.Google Scholar
  26. Bulmer, J. N., and Johnson, P. M., 1986, The T-lymphocyte population in first-trimester human decidua does not express the interleukin-2 receptor, Immunology 58: 685–687.PubMedGoogle Scholar
  27. Bulmer, D., Peel, S., and Stewart, I., 1987, The metrial gland, Cell Differ. 20: 77–86.PubMedCrossRefGoogle Scholar
  28. Buxton, L. E., and Murdoch, N. R., 1982, Lectins, calcium ionophore A 23187, and peanut oil as deciduogenic agents in the uterus of pseudopregnant mice: Effects of tranylcypromine, indomethacin, iproniazid, and propanol, Aust. J. Biol. Sci. 35: 63–72.PubMedGoogle Scholar
  29. Cao, Z. -D., Jones, M. A., and Harper, M. J. K., 1984, Prostaglandin translocation from the lumen of the rabbit uterus in vitro in relation to the day of pregnancy or pseudopregnancy, Biol. Reprod. 31: 505–519.PubMedCrossRefGoogle Scholar
  30. Carollo, J. R., and Weitlauf, H. M., 1981, Regional changes in the binding of (3H)concanavalin A to mouse blastocysts at implantation: An autoradiographic study, J. Exp. Zool. 218: 247–252.PubMedCrossRefGoogle Scholar
  31. Carpen, O., Virtanen, I., and Saksela, E., 1982, Ultrastructure of human natural killer cells: Nature of the cytolytic contacts in relation to cellular secretion, J. Immunol. 128: 2691–2697.Google Scholar
  32. Carson, D. C., Dutt, A., and Tang, J. P., 1987, Glycoconjugate synthesis during early pregnancy: Hyaluronate synthesis and function, Dev. Biol. 120: 228–235.PubMedCrossRefGoogle Scholar
  33. Castracane, V. D., Saksena, S. K., and Shaikh, A. A., 1974, Effect of IUDs, prostaglandins, and indomethacin on decidual cell reaction in the rat, Prostaglandins 6: 397–400.PubMedCrossRefGoogle Scholar
  34. Cecil, H. C., Hannum, J. A., Jr., and Bitman, J., 1966, Quantitation characterization of uterine vascular permeability changes with estrogen, Am. J. Physiol. 211: 1099–1102.Google Scholar
  35. Cerottini, J. -C., and Brunner, K. T., 1974, Cell-mediated cytotoxicity, allograft rejection, and tumor immunity, Adv. Immunol. 18: 67–87.PubMedCrossRefGoogle Scholar
  36. Chavez, D. J., 1984, Cellular aspects of implantation, in: Ultrastructure of Reproduction (J. Van Blerkom and P. M. Motta, eds.), Martinus Nijhoff, The Hague, Boston, pp. 247–259.CrossRefGoogle Scholar
  37. Chavez, D. J., 1986, Cell surface of mouse blastocysts at the trophectoderm-uterine interface during the adhesive stage of implantation, Am. J. Anat. 176: 153–158.PubMedCrossRefGoogle Scholar
  38. Chavez, D. J., and Anderson, T. L., 1985, The glycocalyx of the mouse uterine luminal epithelium during estrus, early pregnancy, the periimplantation period, and delayed implantation. I. Acquisition of Ricinus communis 1 binding sites during pregnancy, Biol. Reprod. 32: 1135–1142.PubMedCrossRefGoogle Scholar
  39. Chavez, D. J., and Enders, A. C., 1981, Temporal changes in lectin binding of peri-implantation mouse blastocysts, Develop. Biol. 87: 267–276.PubMedCrossRefGoogle Scholar
  40. Chavez, D. J., and Enders, A. C., 1982, Lectin binding of mouse blastocysts: Appearance of Dolichos bifloris binding sites on the trophoblast during delayed implantation and their subsequent disappearance during implantation, Biol. Reprod. 26: 545–552.PubMedCrossRefGoogle Scholar
  41. Chavez, D. J., Enders, A. C., and Schlafke, S., 1984, Trophectoderm cell subpopulations in the perimplantation mouse blastocyst, J. Exp. Zool. 231: 267–271.Google Scholar
  42. Clark, D. A., Brierley, J., Slapsys, R., Daya, S., Damji, N., Chaput, A., and Rosenthal, K., 1986, Trophoblast-dependent and trophoblast independent suppressor cells of maternal origin in murine and human decidua, in: Reproductive Immunology ( D. A. Clark and B. A. Croy, eds.), Elsevier, New York, pp. 219–226.Google Scholar
  43. Collawn, S. S., Rankin, J. C., Ledford, B. E., and Baggett, B., 1981, Ornithine decarboxylase activity in the artificially stimulated decidual cell reaction in the mouse uterus, Biol. Reprod. 24: 528–533.Google Scholar
  44. Cox, C., Cheng, H. C., and Dey, S. K., 1982, Phospholipase A2 activity in the rat uterus during early pregnancy, Prostaglandins Leukotrienes Med. 8: 375–381.CrossRefGoogle Scholar
  45. Craggs, R. I., and Peel, S., 1983, Immunological characterization of surface receptors on rat metrial gland cells, J. Reprod. Immunol. 5: 27–37.Google Scholar
  46. Craig, S. S., and Jollie, W. P., 1981, Epithelial ultrastructure during decidualization in rats, Anat. Embryol. 163: 215–222.CrossRefGoogle Scholar
  47. Damsky, C. H., 1984, Integral membrane glycoproteins in cell-cell and cell-substratum adhesion, in: The Biology of Glycoproteins ( R. J. Ivatt, eds.), Plenum Press, New York, pp. 1–64.Google Scholar
  48. Daniel, S. A. J., and Kennedy, T. G., 1987, Prostaglandin E2 enhances uterine stromal cell alkaline phosphatase activity in vitro, Prostaglandins 33: 241–252.PubMedCrossRefGoogle Scholar
  49. De Feo, V. J., 1967, Decidualization, in: Cellular Biology of the Uterus ( R. M. Wynn, ed.), Appleton-Century-Crofts, New York, 191–290.Google Scholar
  50. Denari, J. H., and Rosner, J. M., 1978, Studies on biochemical characteristics of early decidual protein, Int. J. Fertil. 23: 123–127.PubMedGoogle Scholar
  51. Denari, J. H., Germino, N. I., and Rosner, J. N., 1976, Early synthesis of uterine proteins after a decidual stimulus in the pseudopregnant rat, Biol. Reprod. 15: 1–8.PubMedCrossRefGoogle Scholar
  52. Denker, H. -W., 1977, Implantation: The role of proteinases and blockage of implantation by proteinase inhibitors, Adv. Anat. Embryol. Cell Biol. 53 (5): 1–123.Google Scholar
  53. Denker, H. -W., 1980, Role of proteinases in implantation, Prog. Reprod. Biol. 7: 28–42.Google Scholar
  54. Doktorcik, P. E., and Kennedy, T. G., 1986, 6-Keto-prostaglandin-E1 and the decidual cell reaction in rats, Prostaglandins 32: 679–690.Google Scholar
  55. Don, M. M., Abett, G., Bishop, C. J., Bundeson, P. G., Donald, K. J., Searle, J., and Kerr, J. F. R., 1977, Death of cells by apoptosis following attachment of specifically allergised lymphocytes in vitro, Aust. J. Exp. Biol Med. Sci. 55: 407–417.PubMedCrossRefGoogle Scholar
  56. Dutt, A., Tang, J. -P., Welply, J. K., and Carson, D. D., 1986, Regulation of N-linked glycoprotein asembly in uteri by steroid hormones, Endocrinology 118: 661–673.PubMedCrossRefGoogle Scholar
  57. Dutt, A., Tang, J. -P., and Carson, D. D., 1987, Lactosaminoglycans are involved in uterine epithelial cell adhesion in vitro, Dev. Biol. 119: 27–37.PubMedCrossRefGoogle Scholar
  58. Edelman, G. M., 1983, Cell adhesion molecules, Science 219: 450–457.PubMedCrossRefGoogle Scholar
  59. El-Banna, A. A., 1980, The degenerative effect on rabbit implantation sites by indomethacin. I. Timing of indomethacin action, possible effect on uterine proteins and the effect of replacement doses of PGF2ot, Prostaglandins 20: 587–599.PubMedCrossRefGoogle Scholar
  60. El-Shershaby, A. M., and Hinchliffe, J. R., 1975, Epithelial autolysis during implantation of the mouse blastocyst: An ultrastructural study, J. Embryol. Exp. Morphol. 33: 1067–1080.PubMedGoogle Scholar
  61. Enders, A. C., 1972, Mechanisms of implantation of the blastocyst, in: Biology of Reproduction. Basic and Clinical Studies III ( J. T. Velardo and B. A. Kasprow, eds.), Pan American Congress of Anatomy, New Orleans, pp. 313–334.Google Scholar
  62. Enders, A. C., and Nelson, D. M., 1973, Pinocytotic activity of the uterus of the rat, Am. J. Anat. 138: 277–300.PubMedCrossRefGoogle Scholar
  63. Enders, A. C., and Schlafke, S., 1967, A morphological analysis of the early implantation stages in the rat, Am. J. Anat. 120: 185–226.Google Scholar
  64. Enders, A. C., and Schlafke, S., 1969, Cytological aspects of trophoblast-uterine interaction in early implantation, Am. J. Anat. 125: 1–30.Google Scholar
  65. Enders, A. C., and Schlafke, S., 1972, Implantation in the ferret: Epithelial penetration, Am. J. Anat. 133: 291–316.Google Scholar
  66. Enders, A. C., and Schlafke, S., 1974, Surface coats of the mouse blastocyst and uterus during the preimplantation period, Anat. Rec. 180: 31–46.Google Scholar
  67. Enders, A. C., and Schlafke, S., 1979, Comparative aspects of blastocyst-endometrial interactions at implantation, in: Maternal Recognition of Pregnancy, Ciba Foundation Series 64 ( New Series), Excepta Medica, Amsterdam, pp. 3–32.Google Scholar
  68. Enders, A. C., and Schlafke, S., 1986, Implantation in nonhuman primates and in the human, in: Comparative Primate Biology, Volume 3, Reproduction and Development, Alan R. Liss, New York, pp. 291–310.Google Scholar
  69. Enders, A. C., Schlafke, S., and Welsh, A. O., 1980, Trophoblastic and uterine luminal epithelial surfaces at the time of blastocyst adhesion in the rat, Am. J. Anat. 159: 59–72.PubMedCrossRefGoogle Scholar
  70. Enders, A. C., Chavez, D. J., and Schlafke, S., 1981, Comparison of implantation in utero and in vitro, in: Cellular and Molecular Aspects of Implantation ( S. R. Glasser and D. W. Bullock, eds.), Plenum Press, New York, pp. 365–382.CrossRefGoogle Scholar
  71. Enders, A. C., Hendrickx, A. G., and Schlafke, S., 1983, Implantation in the rhesus monkey: Initial penetration of the endometrium, Am. J. Anat. 167: 275–298.Google Scholar
  72. Enders, A. C., Welsh, A. O., and Schlafke, S., 1985, Implantation in the rhesus monkey: Endometrial responses, Am. J. Anat. 173: 147–169.Google Scholar
  73. Evans, C. A., and Kennedy, T. G., 1978, The importance of prostaglandin synthesis for the initiation of blastocyst implantation in the hamster, J. Reprod. Fertil. 54: 255–261.PubMedCrossRefGoogle Scholar
  74. Fainstat, T., 1963, Extracellular studies of uterus. I. Disappearance of the discrete bundles in endometrial stroma during various reproductive stages in the rat, Am. J. Anat. 112: 337–370.CrossRefGoogle Scholar
  75. Feyles, V., and Kennedy, T. G., 1987, Inhibitory effect of the intrauterine infusion of phorbol 12-myristate 13-acetate and l-oleoyl-2-acetylglycerol on the decidual cell reaction in rats, Biol. Reprod. 37: 96–104.PubMedCrossRefGoogle Scholar
  76. Finn, C. A., 1965, Oestrogen and the decidual cell reaction of implantation in mice, J. Endocrinol. 32: 223–229.PubMedCrossRefGoogle Scholar
  77. Finn, C. A., 1977, The implantation reaction, in: Biology of the Uterus ( R. M. Wynn, ed.), Plenum Press, New York, pp. 245–308.CrossRefGoogle Scholar
  78. Finn, C. A., 1980, The endometrium during implantation, in: The Endometrium, ( F. A. Kimball, ed.), Spectrum, New York, pp. 43–56.Google Scholar
  79. Finn, C. A., and Bredl, J. C. S., 1973, Studies on the development of the implantation reaction in the mouse uterus: Influence of actinomycin D, J. Reprod. Fertil. 34: 247–253.PubMedCrossRefGoogle Scholar
  80. Finn, C. A., and Hinchliffe, J. R., 1964, The reaction of the mouse uterus during implantation and deciduoma formation as demonstrated by changes in the distribution of alkaline phosphatase, J. Reprod. Fertil. 8: 331–338.CrossRefGoogle Scholar
  81. Dey, S. K., and Hubbard, C. J., 1981, Role of histamine and cyclic nucleotides in implantation in the rabbit, Cell Tissue Res. 220: 549–554.PubMedCrossRefGoogle Scholar
  82. Dey, S. K., and Johnson, D. C., 1980, Réévaluation of histamine in implantation, in: The Endometrium ( F. A. Kimball, ed.), Spectrum, New York, pp. 269–282.Google Scholar
  83. Dey, S. K., Chien, S. M., Cox, C. L., and Crist, R. D., 1980, Prostaglandin synthesis in the rabbit blastocyst, Prostaglandins 19: 449–453.PubMedCrossRefGoogle Scholar
  84. Finn, C. A., and Hinchliffe, J. R., 1965, Histological and histochemical analysis of the formation of implantation chambers in the mouse uterus, J. Reprod. Fertil. 9: 301–309.CrossRefGoogle Scholar
  85. Finn, C. A., and Lawn, A. M., 1967, Specialized junctions between decidual cells in the uterus of the pregnant mouse, J. Ultrastruct. Res. 20: 321–327.PubMedCrossRefGoogle Scholar
  86. Finn, C. A., and McLaren, A., 1967, A study of the early stages of implantation in mice, J. Reprod. Fertil. 13: 259–267.Google Scholar
  87. Finn, C. A., and Porter, D. G., 1975, The Uterus, Publishing Sciences Group, Acton, UK.Google Scholar
  88. Flower, R. J., and Blackwell, G. J., 1976, The importance of phospholipase-A2 in prostaglandin biosynthesis, Biochem. Pharmacol. 25: 285–291.PubMedCrossRefGoogle Scholar
  89. Gilula, N. B., Reeves, O. R., and Steinback, A., 1972, Metabolic coupling, ionic coupling, and cell contacts, Nature 235: 262–265.PubMedCrossRefGoogle Scholar
  90. Glasser, S. R., 1985, Laboratory models of implantation, in: Reproductive Toxicology ( R. L. Dixon, ed.), Raven Press, New York, pp. 219–238.Google Scholar
  91. Glasser, S. R., and Bullock, D. W. (eds.), 1981, Cellular and Molecular Aspects of Implantation, Plenum Press, New York.Google Scholar
  92. Glasser, S. R., and Julian, J., 1986, Intermediate filament protein as a marker of uterine stromal cell decidualizatioin, Biol. Reprod. 35: 463–474.Google Scholar
  93. Glasser, S. R., and McCormack, S. A., 1981, Separated cell types as analytical tools in the study of decidualization and implantation, in: Cellular and Molecular Aspects of Implantation ( S. R. Glasser and D. W. Bullock, eds.), Plenum Press, New York, pp. 217–239.CrossRefGoogle Scholar
  94. Glasser, S. R., Lampelo, S., Munir, M. I., and Julian, J., 1987, Expression of desmin, laminin, and fibronectin during in situ differentiation (decidualization) of rat uterine stromal cells, Differentiation 35: 132–142.PubMedCrossRefGoogle Scholar
  95. Goldstein, L. J., and Hayes, C. E., 1979, The lectins: Carbohydrate-containing proteins of plants and animals, Adv. Carbohyd. Chem. Biochem. 35: 127–167.CrossRefGoogle Scholar
  96. Guillomot, M., Flechon, J. -E., and Wintenberger-Torres, S., 1981, Conceptus attachment in the ewe: An ultrastructural study, Placenta 2: 169–182.Google Scholar
  97. Guillomot, M., Flechon, J. -E., and Wintenberger-Torres, S., 1982, Cytochemical studies of uterine and trophoblastic surface coats during blastocyst attachment in the ewe, J. Reprod. Fertil. 65: 1–8.Google Scholar
  98. Hall, A. K., and Behrman, H. R., 1982, Prostaglandins: Biosynthesis, metabolism, and mechanism of cellular action, in: Prostaglandins ( J. B. Lee, ed.), Elsevier, New York, pp. 1–38.Google Scholar
  99. Harper, M. J. K., Norris, C. J., and Rajkumar, K., 1983, Prostaglandin release by zygotes and endometria of pregnant rabbits, Biol. Reprod. 28: 350–362.Google Scholar
  100. Hedlund, K., and Nilsson, O., 1971, Hormonal requirements for uterine attachment reaction and blastocyst implantation in the mouse, hamster and guinea pig, J. Reprod. Fertil. 47: 59–62.Google Scholar
  101. Hewitt, K., Beer, A. E., and Grinnell, F., 1979, Disappearance of anionic sites from the surface of the rat endometrial epithelium at the time of blastocyst implantation, Biol. Reprod. 21: 691–707.Google Scholar
  102. Hicks, J. J., and Guzman-Gonzalez, A. M., 1979, Inhibition of implantation by intraluminal administration of concanavalin A in mice, Contraception 20: 129–136.PubMedCrossRefGoogle Scholar
  103. Hoffman, L. H., and Hoos, P. C., 1984, Morphology of vascular leakage at rabbit implantation sites, Anat. Rec. 208: 75.Google Scholar
  104. Hoffman, L. H., Strong, G. B., Davenport, G. R., and Frolich, J. C., 1977, Deciduogenic effect of prostaglandins in the pseudopregnant rabbit, J. Reprod. Fertil. 50: 231–237.PubMedCrossRefGoogle Scholar
  105. Hoffman, L. H., DiPietro, D. L., and McKenna, T. J., 1978, Effects of indomethacin on uterine capillary permeability and blastocyst development in rabbits, Prostaglandins 15: 823–828.PubMedCrossRefGoogle Scholar
  106. Hoffman, L. H., Davenport, G. R., and Brash, A. R., 1984, Endometrial prostaglandins and phospholipase activity related to implantation in rabbits: Effects of dexamethasone, Biol. Reprod. 30: 544–555.PubMedCrossRefGoogle Scholar
  107. Holmes, P. V., and Gordashko, B. J., 1980, Evidence of prostaglandin involvement in blastocyst implantation, J. Embryol. Exp. Morphol. 55: 109–122.PubMedGoogle Scholar
  108. Hoos, P. C., and Hoffman, L. H., 1980, Temporal aspects of rabbit uterine vascular and decidual responses to blastocyst stimulation, Biol. Reprod. 23: 453–459.PubMedCrossRefGoogle Scholar
  109. Hoos, P. C., and Hoffman, L. H., 1983, Effect of histamine receptor antagonists and indomethacin on implantation in the rabbit, Biol. Reprod. 29: 833–840.PubMedCrossRefGoogle Scholar
  110. Hunt, J. S., Manning, L. S., Mitchell, D., Selanders, J. R., and Wood, G. W., 1985, Localization and characterization of macrophages in murine uterus, J. Leukocyte Biol. 38: 255–265.PubMedGoogle Scholar
  111. Huslig, R. L., Fogwell, R. L., and Smith, W. L., 1979, The prostaglandin forming cyclooxygenase of ovine uterus: Relationship to luteal function, Biol. Reprod. 21: 589–600.PubMedCrossRefGoogle Scholar
  112. Hyland, J. H., Manns, J. G., and Humphrey, W. D., 1982, Prostaglandin production by ovine embryos and endometrium in vitro, J. Reprod. Fertil. 65: 299–304.PubMedCrossRefGoogle Scholar
  113. Inoue, K., Tice, L. W., and Creveling, C. R., 1980, Immunocytochemical localization of catechol-O-methyltransferase in the pregnant rat uterus, Endocrinology 107: 1833–1837.PubMedCrossRefGoogle Scholar
  114. Irvine, R. F., 1982, How is the level of free arachidonic acid controlled in mammalian cells Biochem J. 204: 3–16.PubMedGoogle Scholar
  115. Jayatilak, R. G., Glaser, L. A., Warshaw, M. L., Herz, Z., Gruber, J. R., and Gibori, G., 1984, Relationship between luteinizing hormone and decidual luteotropin in the maintenance of luteal steroidogenesis, Biol. Reprod. 31: 556–564.Google Scholar
  116. Jeffrey, J. J., 1981, Collagen synthesis and degradation in the uterine deciduoma: Regulation of collagenase activity by progesterone, Coll. Relat. Res. 1: 257–268.Google Scholar
  117. Jenkinson, E. J., and Searle, R. F., 1977, Cell surface changes on the mouse blastocyst at implantation, Exp. Cell Res. 106: 386–390.PubMedCrossRefGoogle Scholar
  118. Johnston, M. E. A., and Kennedy, T. G., 1984, Estrogen and uterine sensitization for the decidual cell reaction in the rat: Role of prostaglandin E2 and adenosine 3’: 5’-cyclic monophosphate, Biol. Reprod. 31: 959–966.PubMedCrossRefGoogle Scholar
  119. Jollie, W. P., and Bencosme, S. A., 1965, Electron microscopic observations n primary decidua formation in the rat, Am. J. Anat. 116: 216–236.CrossRefGoogle Scholar
  120. Joshi, S. G., Szarowski, D. H., and Bank, J. F., 1981, Decidua-associated antigens in the baboon, Biol. Reprod. 25: 591–598.PubMedCrossRefGoogle Scholar
  121. Kearns, M., and Lala, P. K., 1983, Life history of decidual cells: A review, Am. J. Reprod. Immunol. 3: 78–82.Google Scholar
  122. Kennedy, T. G., 1977, Evidence for a role for prostaglandins in the initiation of blastocyst implantation in the rat, Biol. Reprod. 16: 286–291.PubMedCrossRefGoogle Scholar
  123. Kennedy, T. G., 1979, Prostaglandins and increased endometrial vascular permeability resulting from the application of an artificial stimulus to the uterus of the rat sensitized for the decidual cell reaction, Biol. Reprod. 20: 560–566.PubMedCrossRefGoogle Scholar
  124. Kennedy, T. G., 1980a, Estrogen and uterine sensitization for the decidual cell reaction: Role of prostaglandins, Biol. Reprod. 23: 955–962.PubMedCrossRefGoogle Scholar
  125. Kennedy, T. G., 1980b, Timing of uterine sensitivity for the decidual cell reaction: Role of prostaglandins, Biol. Reprod. 22: 519–525.PubMedGoogle Scholar
  126. Kennedy, T. G., 1983a, Embryonic signals and the initiation of blastocyst implantation, Aust. J. Biol. Sci. 36: 531–543.PubMedGoogle Scholar
  127. Kennedy, T. G., 1983b, Prostaglandin E2, adenosine 3’: 5’-cyclic monophosphate and changes in endometrial vascular permeability in rat uteri sensitized for the decidual cell reaction, Biol. Reprod. 29: 1069–1076.PubMedCrossRefGoogle Scholar
  128. Kennedy, T. G., 1985, Evidence for the involvement of prostaglandins throughout the decidual cell reaction in the rat, Biol. Reprod. 33: 140–16.PubMedCrossRefGoogle Scholar
  129. Kennedy, T. G., 1986, Intrauterine infusion of prostaglandins and decidualization in rats with uteri differentially sensitized for the decidual cell reaction, Biol. Reprod. 34: 327–335.PubMedCrossRefGoogle Scholar
  130. Kennedy, T. G., and Armstrong, D. T., 1981, The role of prostaglandins in endometrial vascular changes at implantation, in: Cellular and Molecular Aspects of Implantation ( S. R. Glasser and D. W. Bullock, eds.), Plenum Press, New York, pp. 349–364.CrossRefGoogle Scholar
  131. Kennedy, T. G., and Lukash, L. A., 1982, Induction of decidualization in rats by the ultrauterine infusion of prostaglandins, Biol. Reprod. 27: 253–260.PubMedCrossRefGoogle Scholar
  132. Kennedy, T. G., and Zamecnik, J., 1978, The concentration of 6-oxo-PGFla is markedly elevated at the site of blastocyst implantation in the rat, Prostaglandins 16: 599–605.PubMedCrossRefGoogle Scholar
  133. Kennedy, T. G., Martel, D., and Psychoyos, A., 1983a, Endometrial prostaglandin E2 binding: Characterization in rats sensitized for the decidual cell reaction and changes during pseudopregnancy, Biol. Reprod. 29: 556–564.Google Scholar
  134. Kennedy, T. G., Martel, D., and Psychoyos, A., 1983b, Endometrial prostaglandin E2 binding during the estrous cycle and its hormonal control in ovariectomized rats, Biol. Reprod. 29: 565–571.Google Scholar
  135. Kerr, J. F. R., Wyllie, A. H., and Currie, A. R., 1972, Apoptosis: A basic biological phenomenon with wide-ranging implication in tissue kinetics, Br. J. Cancer 26: 239–247.PubMedCrossRefGoogle Scholar
  136. Kerr, J. F. R., Bishop, C. J., and Searle, J., 1984, Apoptosis, Recent Adv. Histopathol. 12: 1–15.Google Scholar
  137. Keys, J. L., King, G. J., and Kennedy, T. G., 1986, Increased uterine vascular permeability at the time of embryonic attachment in the pig, Biol. Reprod. 34: 405–411.PubMedCrossRefGoogle Scholar
  138. Kirby, D. R. S., 1965, The “invasiveness” of the trophoblast, in: The Early Conceptus, Normal and Abnormal ( W. W. Park, ed.), E. S. Livingstone, Edinburgh, pp. 68–73.Google Scholar
  139. Kirby, D. R. S., and Cowell, T. P., 1968, Trophoblast-host interactions, in: Epithelial-MesenchtymalInteractions ( R. Fleischmajer and R. E. Billingham, eds.), Williams & Wilkins, Baltimore, pp. 64–77.Google Scholar
  140. Kirby, D. R. S., Billington, W. D., and James, D. A., 1966, Transplantation of eggs to the kidney and uterus of immunised mice, Transplantation 4: 713–718.PubMedCrossRefGoogle Scholar
  141. Kirchner, C., Hirchlauser, C., and Kionke, M., 1971, Protease activity in rabbit uterine secretion 24 hr before implantation, J. Reprod. Fertil. 27: 259–260.Google Scholar
  142. Kirkwood, K. J., 1981, Immunoglobulin and complement receptor-bearing cells in cultures of mouse decidual tissue, J. Reprod. Fertil. 62: 345–352.PubMedCrossRefGoogle Scholar
  143. Kleinfeld, R. G., Morrow, H. A., and De Feo, V. J., 1976, Intercellular junctions between decidual cells in the growing deciduoma of the pseudopregnant rat uterus, Biol. Reprod. 15: 593–603.PubMedCrossRefGoogle Scholar
  144. Konwinski, M., Vorbrodt, A., Solter, D., and Koprowski, H., 1977, Ultrastructural study of concanavalin A binding to the surface of preimplantation mouse embryos, J. Exp. Zool. 200: 311–324.Google Scholar
  145. Krehbiel, R. H., 1937, Cytological studies of the decidual reaction in the rat during early pregnancy and the production of deciduomata, Physiol. Zool. 10: 212–234.Google Scholar
  146. Kubota, T., Kumasaka, T., Yaoi, Y., Suzuki, A., and Saito, M., 1981, Study on immunoreactive prolactin of decidua in early pregnancy, Acta Endocrinol. 96: 258–264.PubMedGoogle Scholar
  147. Lacroix, M. C., and Kann, G., 1982, Comparative studies of prostaglandins F2a and E2 in late cyclic and early pregnant sheep: In vitro synthesis by endometrium and conceptus effects of in vivo indomethacin treatment on establishment of pregnancy, Prostaglandins 23: 507–526.Google Scholar
  148. Lala, P. K., Parhar, P. S., Kearns, M., Johnson, S., and Scodras, J. M., 1986, Immunologic aspects of the decidual response, in: Reproductive Immunology ( D. A. Clark and B. A. Croy, eds.), Elsevier, New York, pp. 190–198.Google Scholar
  149. Lampelo, S. A., Ricketts, A. D., and Bullock, D. W., 1985, Purification of rabbit endometrial plasma membranes from receptive and non-receptive uteri, J. Reprod. Fertil. 75: 475–484.PubMedCrossRefGoogle Scholar
  150. Lau, I. F., Saksena, S. K., and Chang, M. C., 1973, Pregnancy blockage by indomethacin, an inhibitor of prostaglandin synthesis: Its reversal by prostaglandins and progesterone in mice, Prostaglandins 4: 795–803.PubMedCrossRefGoogle Scholar
  151. Leavitt, W. W., MacDonald, R. G., and Shwaery, G. T., 1985, Characterization of deciduoma marker proteins in hamster uterus: Detection in decidual cell cultures, Biol. Reprod. 32: 631–643.PubMedCrossRefGoogle Scholar
  152. Lejeune, B., Van Hoeck, J., and Leroy, F., 1981, Transmitter role of the luminal uterine epithelium in the induction of decidualization in rats, J. Reprod. Fertil. 61: 235–240.Google Scholar
  153. Leroy, F., Vansande, J., Shetgen, G., and Brasseur, D., 1974, Cyclic AMP and the triggering of the decidual reaction, J. Reprod. Fertil. 39: 207–211.Google Scholar
  154. Leroy, F., Finn, C. A., Psychoyos, A., and Hubinont, P. O. (eds.), 1980, Progress in Reproductive Biology, Volume 7, S. Karger, Basel.Google Scholar
  155. Lewis, G. S., and Waterman, R. A., 1983, Metabolism of arachidonic acid in vitro by porcine blastocysts and endometrium, Prostaglandins 25: 871–880.PubMedCrossRefGoogle Scholar
  156. Lewis, G. S., Thatcher, W. W., Bazer, F. W., and Curl, J. S., 1982, Metabolism of arachidonic acid in vitro by bovine blastocysts and endometrium, Biol. Reprod. 27: 431–439.PubMedCrossRefGoogle Scholar
  157. Loewenstein, W. R., 1966, Permeability of membrane junctions, Ann. N. Y. Acad. Sci. 137: 441–472.PubMedCrossRefGoogle Scholar
  158. Lundkvist, O., 1979, Morphometric estimation of stromal edema during delayed implantation in the rat, Cell Tissue Res. 199: 339–348.PubMedCrossRefGoogle Scholar
  159. Lundkvist, O., and Ljungkvist, I., 1977, Morphology of the rat endometrial stroma at the appearance of the pontamine blue reaction during implantation after an experimental delay, Cell Tissue Res. 184: 453–466.PubMedCrossRefGoogle Scholar
  160. Lundkvist, O., and Nilsson, B. O., 1980, Ultrastructural changes of the trophoblast-epithelial complex in mice subjected to implantation blocking treatment with indomethacin, Biol. Reprod. 22: 719–726.PubMedGoogle Scholar
  161. Lundkvist, O., and Nilsson, B. O., 1982, Endometrial ultrastructure in the early uterine response to blastocysts and artificial deciduogenic stimuli in rats, Cell Tissue Res. 225: 355–364.PubMedCrossRefGoogle Scholar
  162. MacDonald, R. G., Morency, K. O., and Leavitt, W. W., 1983, Progesterone modulation of specific protein synthesis in the decidualized hamster uterus, Biol. Reprod. 28: 753–766.PubMedCrossRefGoogle Scholar
  163. Magnuson, T., and Stackpole, C. W., 1978, Lectin-mediated agglutination of preimplantation mouse embryos, Exp. Cell Res. 116: 466–469.CrossRefGoogle Scholar
  164. Marcus, G. J., 1981, Prostaglandin formation by the sheep embryo and endometrium as an indication of maternal recognition of pregnancy, Biol. Reprod. 25: 56–64.PubMedCrossRefGoogle Scholar
  165. Martel, D., Kennedy, T. G., Monier, M. N., and Psychoyos, A., 1985, Failure to detect specific binding sites for prostaglandin F2a in membrane preparations from rat endometrium, J. Reprod. Fertil. 75: 265–274.Google Scholar
  166. Martello, E. M. V. G., and Abrahamsohn, P. A., 1986, Collagen distribution in the mouse endometrium during decidualization, Acta Anat. 127: 146–150.PubMedCrossRefGoogle Scholar
  167. Martin, L., Finn, C. A., and Carter, J., 1970, Effects of progesterone and oestradiol-173 on the luminal epithelium of the mouse uterus, J. Reprod. Fertil. 21: 461–469.Google Scholar
  168. Martin, L., Hallowes, R. C., Finn, C. A., and West, D. G., 1973, Involvement of the uterine blood vessels in the refractory state of the uterine stroma which follows oestrogen stimulation in progesterone-treated mice, J. Endocrinol. 56: 309–314.PubMedCrossRefGoogle Scholar
  169. Martz, E., 1987, LFA-1 and other accessory molecules functioning in adhesion of T and B lymphocytes, Hum. Immunol. 18: 3–37.PubMedCrossRefGoogle Scholar
  170. Matter, A., 1979, Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes, Immunology 36: 179–190.PubMedGoogle Scholar
  171. Mayer, G., Nilsson, O., and Reinius, S., 1967, Cell membrane changes of uterine epithelium and trophoblast during blastocyst attachment in the rat, Z. Anat. Entwickl. Gesch. 126: 43–48.Google Scholar
  172. Miller, M. M., and O’Morchoe, C. C. C., 1982, Decidual cell reaction induced by prostaglandin F1 in the mature oophorectomized rat, Cell Tissue Res. 225: 189–200.PubMedCrossRefGoogle Scholar
  173. Milligan, S. R., and Lytton, F. D. C., 1983, Changes in prostaglandin levels in the sensitized and non-sensitized uterus of the mouse after the intrauterine instillation of oil or saline, J. Reprod. Fertil. 67: 373–377.PubMedCrossRefGoogle Scholar
  174. Milligan, S. R., and Mirembe, F. M., 1985, Intraluminally injected oil induces changes in vascular permeability in the “sensitized” and “nonsensitized” uterus of the mouse, J. Reprod. Fertil. 74: 95–104.PubMedCrossRefGoogle Scholar
  175. Morris, J. E., and Potter, S. W., 1984, A comparison of developmental changes in surface charge in mouse blastocysts and uterine epithelium using DEAE beads and dextran sulfate in vitro, Dev. Biol. 103: 190–199.PubMedCrossRefGoogle Scholar
  176. Morris, J. E., Potter, S. W., Rynd, L. S., and Buckley, P. M., 1983, Adhesion of mouse blastocysts to uterine epithelium in culture: A requirement for mutual surface interactions, J. Exp. Zool. 225: 467–479.PubMedCrossRefGoogle Scholar
  177. Mossman, H. W., 1937, Comparative morphogenesis of the fetal membranes and accessory uterine structures, Contrib. Embryol. Carnegie Inst. 26: 129–246.Google Scholar
  178. Moulton, B. C., 1974, Ovum implantation and uterine lysosomal enzyme activity, Biol. Reprod. 10: 543–548.PubMedCrossRefGoogle Scholar
  179. Moulton, B. C., 1984, Epithelial cell function during blastocyst implantation, J. Biosci. 6 (Suppl. 2): 11–21.CrossRefGoogle Scholar
  180. Moulton, B. C., and Elangovan, S., 1981, Lysosomal mechanisms in blastocyst implantation and early decidualization, in: Cellular and Molecular Aspects of Implantation ( S. R. Glasser and D. W. Bullock, eds.), Plenum Press, New York, pp. 335–344.CrossRefGoogle Scholar
  181. Moulton, B. C., and Koenig, B. B., 1986, Hormonal control of phospholipid methylation in uterine epithelial cells during sensitivity to deciduogenic stimuli, Endocrinology 118: 244–249.PubMedCrossRefGoogle Scholar
  182. Moulton, B. C., Koenig, B. B., and Borkan, S. C., 1978, Uterine lysosomal enzyme activity during ovum implantation and early decidualization, Biol. Reprod. 19: 167–170.PubMedCrossRefGoogle Scholar
  183. Moulton, B. C., Schuler, J. A., and Leftwich, J. B., 1987, Effect of a deciduogenic stimulus on arachidonic acid turnover in uterine phospholipids, Biol. Reprod. 36 (Suppl. 1): 66.Google Scholar
  184. Murphy, C. R., and Bradbury, S., 1984, Colloidal iron hydroxide staining of surface carbohydrates after glycerol treatment of uterine epithelial cells, Histochemistry 80: 45–48.PubMedCrossRefGoogle Scholar
  185. Murphy, C. R., and Rogers, A. W., 1981, Effects of ovarian hormones on cell membranes in the rat uterus: III. The surface carbohydrates at the apex of the luminal epithelium, Cell Biophys. 3: 305–320.Google Scholar
  186. Murphy, C. R., and Swift, J. G., 1983, Relationships between intramembranous particles and surface coat carbohydrates in cells of a compact tissue, J. Cell Sci. 64: 123–136.PubMedGoogle Scholar
  187. Murphy, C. R., Swift, J. G., Mukherjee, T. M., and Rogers, A. W., 1979, Effects of ovarian hormones on cell membranes in the rat uterus. I. Freeze-fracture studies of the apical membrane of the luminal epithelium, Cell Biophys. 1: 181–193.CrossRefGoogle Scholar
  188. Murphy, C. R., Swift, J. G., Mukherjee, T. M., and Rogers, A. W., 1982, Changes in the fine structure of the apical plasma membrane of endometrial epithelial cells during implantation in the rat, J. Cell. Sci. 55: 1–12.PubMedGoogle Scholar
  189. Nilsson, B. O., and Njerten, S., 1982, Electrophoretic quantification of the changes in the average net negative surface charge density of mouse blastocysts implanting in vivo and in vitro, Biol. Reprod. 27: 485–493.Google Scholar
  190. Nilsson, O., 1966a, Estrogen-induced increase of adhesiveness in uterine epithelium of mouse and rat, Exp. Cell Res. 43: 239–241.PubMedCrossRefGoogle Scholar
  191. Nilsson, O., 1966b, Structural differentiation of luminal membrane in rat uterus during normal and experimental implantations, Z. Anat. Entwickl. 125: 152–159.CrossRefGoogle Scholar
  192. Nilsson, O., 1972, Ultrastructure of the process of secretion in the rat uterine epithelium at preimplantation, J. Ultrastruct. Res. 40: 572–580.PubMedCrossRefGoogle Scholar
  193. Nilsson, O., 1974, Changes of the luminal surface of the rat uterus of blastocyst implantation, Z. Anat. Entwickl. 144: 337–342.CrossRefGoogle Scholar
  194. Nilsson, O., Lindqvist, I., and Ronquist, G., 1973, Decreased surface charge of mouse blastocysts at implantation, Exp. Cell Res. 83: 421–423.Google Scholar
  195. Nilsson, O., Lindqvist, I., and Ronquist, G., 1975, Blastocyst surface charge and implantation in the mouse, Contraception 11: 441–450.PubMedCrossRefGoogle Scholar
  196. Nilsson, O., Naeslund, G., and Curman, B., 1980, Polar differences of delayed and implanting mouse blastocysts in binding of alcian blue and concanavalin A, J. Exp. Zool. 214: 177–180.Google Scholar
  197. Nimura, S., and Ishida, K., 1987, Immunohistochemical demonstration of prostaglandin E2 in preimplantation mouse embryos, J. Reprod. Fertil. 80: 505–508.Google Scholar
  198. Obrink, B., 1986, Epithelial cell adhesion molecules, Exp. Cell Res. 163: 1–21.PubMedCrossRefGoogle Scholar
  199. Oettel, M., Koch, M., Kurischko, A., and Schubert, K., 1979, A direct evidence for the involvement of prostaglandin F2ot in the first step of estrone-induced blastocyst implantation in the spayed rat, Steroids 33: 1–8.PubMedCrossRefGoogle Scholar
  200. Ohta, Y., 1985, Histochemical localization of prostaglandin synthetase in the rat endometrium with reference to decidual cell reaction, Proc. Jpn. Acad. [B] 61: 467–470.CrossRefGoogle Scholar
  201. Orsini, M. W., 1964, Implantation: A comparison of conditions in the pregnant and pseudopregnant hamster, in: 5th International Congress on Animal Reproduction and Artificial Insemination, Volume 7, Trento, 309–319.Google Scholar
  202. Orsini, M. W., and Donovan, B. T., 1971, Implantation and induced decidualization of the uterus in the guinea pig, as indicated by Pontamine Blue, Biol. Reprod. 5: 270–2811.Google Scholar
  203. Orsini, M. W., Wynn, R. M., Harris, J. A., and Bulmash, J. M., 1970, Comparative ultrastructure of the decidua in pregnancy and pseudopregnancy, Am. J. Obstet. Gynecol. 106: 14–25.PubMedGoogle Scholar
  204. O’Shea, J. D., Kleinfeld, R. G., and Morrow, H. A., 1983, Ultrastructure of decidualization in the pseudopregnant rat, Am. J. Anat. 166: 271–298.PubMedCrossRefGoogle Scholar
  205. Pakrasi, P. L., and Dey, S. K., 1982, Blastocyst is the source of prostaglandins in the implantation site in the rabbit, Prostaglandins 24: 73–77.PubMedCrossRefGoogle Scholar
  206. Paria, B. C., Sengupta, J., and Manchanda, S. K., 1981, Involvement of lysosomal enzymes in mouse embryo implantation: Effect of the antioestrogen, CI-628 citrate, J. Endocrinol. 90: 83–88.PubMedCrossRefGoogle Scholar
  207. Parkening, T., 1976, An ultrastructural study of implantation in the golden hamster. III. Initial formation and differentiation of decidual cells, J. Anat. 122: 485–498.PubMedGoogle Scholar
  208. Parr, E. L., and Kirby, W. M., 1979, An immunoferritin labeling study of H-2 antigens on dissociated epithelial cells, J. Histochem. Cytochem. 27: 1327–1336.PubMedCrossRefGoogle Scholar
  209. Parr, E. L., Tung, H. N., and Parr, M. B., 1987a, Apoptosis as the mode of uterine epithelial cell death embryo implantation in mice and rats, Biol. Reprod. 36: 211–225.PubMedCrossRefGoogle Scholar
  210. Parr, E. L., Parr, M. B., and Young, J. D. -E., 1987b, Localization of a pore-forming protein (perforin) in granulated metrial gland cells, Biol. Reprod. 37: 1327–1335.PubMedCrossRefGoogle Scholar
  211. Parr, M. B., 1980, Endocytosis in the uterine epithelium during early pregnancy, Prog. Reprod. Biol. 7: 81–91.Google Scholar
  212. Parr, M. B., 1983, Relationship of uterine closure to ovarian hormones and endocytosis in the rat, J. Reprod. Fertil. 68: 185–188.PubMedCrossRefGoogle Scholar
  213. Parr, M. B., and Parr, E. L., 1974, Uterine luminal epithelium: Protrusions mediate endocytosis not apocrine secretion in the rat, Biol. Reprod. 11: 220–233.PubMedCrossRefGoogle Scholar
  214. Parr, M. B., and Parr, E. L., 1977, Endocytosis in the uterine epithelium of the mouse, J. Reprod. Fertil. 50: 151–153.PubMedCrossRefGoogle Scholar
  215. Parr, M. B., and Parr, E. L., 1986, Permeability of the primary decidual zone in the rat uterus: Studies using fluorescein-labeled proteins and dextrans, Biol. Reprod. 34: 393–403.PubMedCrossRefGoogle Scholar
  216. Parr, M. B., Tung, H. N., and Parr, E. L., 1986, The ultrastructure of the rat primary decidual zone, Am. J. Anat. 176: 423–436.PubMedCrossRefGoogle Scholar
  217. Parr, M. B., Parr, E. L., Munaretto, K., Clark, M. R., and Dey, S. K., 1988, Immunohistochemical localization of prostaglandin synthase in the rat uterus and embryo during the per-implantation period, Biol. Reprod. 38: 333–343.PubMedCrossRefGoogle Scholar
  218. Phillips, C. A., and Poyser, N. L., 1981, Studies on the involvement of prostaglandins in implantation in the rat, J. Reprod. Fertil. 62: 73–81.PubMedCrossRefGoogle Scholar
  219. Pierce, M., Turley, E. A., and Roth, S., 1980, Cell surface glycosyltransferase activities, Int. Rev. Cytol. 65: 1–47.Google Scholar
  220. Pinsker, M. C., and Mintz, B., 1973, Change in cell-surface glycoproteins of mouse embryos before implantation, Proc. Nat. Acad. Sci. USA 70: 1645–1648.Google Scholar
  221. Pinsker, M. C., Sacco, A. G., and Mintz, B., 1974, Implantation-associated proteinase in mouse uterine fluid, Dev. Biol. 38: 285–290.Google Scholar
  222. Pisam, M., and Ripoche, P., 1976, Redistribution of surface macromolecules in dissociated epithelial cells, J. Cell Biol. 71: 907–920.PubMedCrossRefGoogle Scholar
  223. Podack, E. R., 1985, The molecular mechanism of lymphocyte mediated tumor cell lysis, Immunol. Today 6: 21–27.CrossRefGoogle Scholar
  224. Poelmann, R. E., 1975, An ultrastructural study of implanting mouse blastocysts: Coated vesicles and epithelium formation, J. Anat. 119: 421–434.PubMedGoogle Scholar
  225. Pollard, R. M., and Finn, C. A., 1972, Ultrastructure of the uterine epithelium during hormonal induction of sensitivity and insensitivity to a decidual stimulus in the mouse, J. Endocrinol. 55: 293–298.PubMedCrossRefGoogle Scholar
  226. Psychoyos, A., 1960, La réaction déciduale est précédée de modifications précoces de la perméabilité capillaire de l’utérus, C. R. Seances Soc. Biol. 154: 1384.Google Scholar
  227. Psychoyos, A., 1973, Endocrine control of egg implantation, in: Handbook of Physiology, Section 7, Volume 2, Part 2, ( R. O. Greep, E. B. Astwood, and S. R. Geiger, eds.), Williams & Wilkins, Baltimore, MD, pp. 187–215.Google Scholar
  228. Psychoyos, A., and Mandon, P., 1971a, Etude de la surface de l’épithélium utérin au microscope électronique à balayage. Observations chez la ratte au 4e et au 5e jour de la gestation, C. R. Hebd. Seances Acad. Sci. ( Paris ) 272: 2723–2725.Google Scholar
  229. Psychoyos, A., and Mandon, P., 1971b, Scanning electron microscopy of the surface of the rat uterine epithelium during delayed implantation, J. Reprod. Fertil. 26: 137–138.Google Scholar
  230. Rachman, F., Bernard, O., Scheid, M. P., and Bennett, D., 1981, Immunological studies of mouse decidual cells. II. Studies of cells in artificialy induced decidua, J. Reprod. Immunol. 3: 41–48.Google Scholar
  231. Racowsky, C., and Biggers, J. D., 1983, Are blastocyst prostaglandins produced endogenously? Biol. Reprod. 29: 379–388.CrossRefGoogle Scholar
  232. Rankin, J. C., Ledford, B. E., and Baggett, B., 1977, Early involvement of cyclic nucleotides in the artificially stimulated decidual cell reaction in the mouse uterus, Biol. Reprod. 17: 549–554.Google Scholar
  233. Rankin, J. C., Ledford, B. E., Jansson, H. T., and Baggett, B., 1979, Prostaglandins, indomethacin and the decidual cell reaction in the mouse uterus, Biol. Reprod. 20: 399–404.Google Scholar
  234. Rankin, J. C., Ledford, B. E., and Baggett, B., 1981, The role of prostaglandins and cyclic nucleotides in artificially stimulated decidual cell reaction in the mouse uterus, in: Cellular and Molecular Aspects of Implantation ( S. R. Glasser and D. W. Bullock, eds.), Plenum Press, New York, pp. 428–430.CrossRefGoogle Scholar
  235. Reinius, S., 1967, Ultrastructure of blastocyst attachment in the mouse, Z. Zellforsch. Mikrosk. Anat. 77: 257–266.PubMedCrossRefGoogle Scholar
  236. Ricketts, A. P., Scott, D. W., and Bullock, D. W., 1984, Radioiodinated surface proteins of separated cell types from rabbit endometrium in relation to the time of implantation, Cell Tissue Res. 236: 421–429.PubMedCrossRefGoogle Scholar
  237. Rogers, P. A. W., Murphy, C. R., Rogers, A. W., and Gannon, B. J., 1983, Capillary patency and per-meability in the endometrium surrounding the implanting rat blastocyst, Int. J. Microcirc. Clin. Exp. 2: 241–249.Google Scholar
  238. Roseman, S., 1970, The synthesis of complex carbohydrates by multiglycosyltransferase systems and the potential function in intercellular adhesion, Chem. Phys. Lipids 5: 270–299.PubMedCrossRefGoogle Scholar
  239. Roth, S., McGuire, J. E., and Roseman, S., 1971, Evidence for cell-surface glycosyltransferases-potential role in cellular recognition, J. Cell Biol. 51: 536–547.PubMedCrossRefGoogle Scholar
  240. Rowinski, J., Solter, D., and Kaprowski, H., 1976, Changes of concanavalin A induced agglutinability during preimplantation mouse development, Exp. Cell Res. 100: 404–408.Google Scholar
  241. Roy, S. K., Sengupta, J., and Manchanda, S. K., 1983, Histochemical study of beta-glucuronidase in the rat uterus during implantation and pseudopregnancy, J. Reprod. Fertil. 68: 161–164.PubMedCrossRefGoogle Scholar
  242. Saksena, S. K., Lau, I. F., and Chang, M. C., 1976, Relationship between oestrogen, prostaglandin F2a, and histamine in delayed implantation in the mouse, Acta Endocrinol. 91: 801–807.Google Scholar
  243. Salazar-Rubio, M., Gil-Recasens, M. E., Hicks, J. J., and Gonzalez-Angulo, Y. A., 1980, High resolution cytochemical study of uterine epithelial cell surface of the rat at identified sites previous to blastocyst-endometrial contact, Arch. Invest. Méd. ( Méx. ) 11: 117–127.Google Scholar
  244. Sananes, N., and Le Goascogne, C., 1976, Decidualization in prepuberal rat uterus, Differentiation 5: 133–144.PubMedCrossRefGoogle Scholar
  245. Sananes, N., Baulieu, E. -E., and Le Goascogne, C., 1976, Prostaglandin(s) as inductive factor of decidualization in the rat uterus, Mol. Cell. Endocrinol. 6: 153–158.Google Scholar
  246. Sananes, N., Weiller, S., Baulieu, E. -E., and Le Goascogne, C., 1980, Decidualization in vitro, Prog. Reprod. Biol. 7: 125–134.Google Scholar
  247. Sananes, N., Baulieu, E. -E., and Le Goascogne, C., 1981, A role for prostaglandins in decidualization of the rat uterus, J. Endocrinol. 89: 25–33.PubMedCrossRefGoogle Scholar
  248. Sanders, R. B., Bekairi, A. M., and Yochim, J. M., 1983, Estrogen sensitive uterine adenylate cyclase in the rat, Fed. Proc. 42: 1852.Google Scholar
  249. Sanders, R. B., Bekairi, A. M., Abulaban, F. S., and Yochim, J. M., 1986, Uterine adenylate cyclase in the rat: Responses to a decidual-inducing stimulus, Biol. Reprod. 35: 100–105.PubMedCrossRefGoogle Scholar
  250. Schatz, F., Markiewicz, L., and Gurpide, E., 1987, Differential effects of estradiol, arachidonic acid, and A 23187 on prostaglandin F2a output by epithelial and stromal cells of human endometrium, Endocrinology 120: 1465–1471.PubMedCrossRefGoogle Scholar
  251. Schlafke, S., and Enders, A. C., 1975, Cellular basis of interaction between trophoblast and uterus at implantation, Biol. Reprod. 12: 41–65.PubMedCrossRefGoogle Scholar
  252. Schlafke, S., Welsh, A. O., and Enders, A. C., 1985, Penetration of the basal lamina of the uterine luminal epithelium during implantation in the rat, Anat. Rec. 212: 47–56.PubMedCrossRefGoogle Scholar
  253. Searle, R. F., 1986, Intrauterine immunization, in: Reproductive Immunology ( D. A. Clark and B. A. Croy, eds.), Elsevier, New York, pp. 211–218.Google Scholar
  254. Searle, R. F., Bell, S. C., and Billington, W. D., 1983, la antigen-bearing decidual cells and macrophages in cultures of mouse decidual tissue, Placenta 4: 139–148.Google Scholar
  255. Sengupta, J., Roy, S. K.. and Manchanda, S. K., 1979, Hormonal control of implantation: A possible role of lysosomal function in th embryo-uterus interaction, J. Steroid Biochem. 11: 729–744.PubMedCrossRefGoogle Scholar
  256. Sengupta, J., Paria, B. C., and Manchanda, S. K., 1981, Effect of an oestrogen antagonist on implantation and uterine leucylnaphylamidase activity in the ovariectomized hamster, J. Reprod. Fertil. 62: 437–440.PubMedCrossRefGoogle Scholar
  257. Sharma, S. C., 1979, Temporal changes in PGE, PGFa, oestradiol-17p and progesterone in uterine venous plasma and endometrium of rabbits during early pregnancy, INSERM Symp. 91: 243–264.Google Scholar
  258. Shemesh, M., Milaguir, F., Ayalon, N., and Hansel, W., 1979, Steroidogenesis and prostaglandin synthesis by cultured bovine blastocysts, J. Reprod. Fertil. 56: 181–185.Google Scholar
  259. 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. Tauber, eds.), Georg Thieme, Stuttgart, pp. 179–180.Google Scholar
  260. Shur, B. D., 1982, Evidence that galactosyltransferase is a surface receptor for poly(N)-acetyl lactosamine glycoconjugates on embryonal carcinoma cells, J. Biol. Chem. 257: 6871–6878.PubMedGoogle Scholar
  261. Shur, B. D., 1983, Embryonal carcinoma cell adhesion: The role of surface galactosyltransferase and its 90K lactosaminoglycan substrate, Dev. Biol. 99: 360–372.PubMedCrossRefGoogle Scholar
  262. Shur, B. D., 1984, The receptor function of galactosyltransferases during cellular interactions, Mol. Cell. Biochem. 61: 143–158.PubMedCrossRefGoogle Scholar
  263. Smith, A. F., and Wilson, I. B., 1974, Cell interaction at the maternal-embryonic interface during implantation in the mouse, Cell Tissue Res. 152: 525–542.PubMedGoogle Scholar
  264. Smith, R. E., and Farquhar, M. G., 1966, Lysosome function in the regulation of the secretory process in cells of the anterior pituitary glands, J. Cell Biol. 31: 319–347.PubMedCrossRefGoogle Scholar
  265. Sobel, J. S., and Nebel, L., 1976, Concanavalin A agglutinability of developing mouse trophoblast, J. Reprod. Fertil. 47: 399–402.Google Scholar
  266. Sobel, J. S., and Nebel, L., 1978, Changes in concanavalin A agglutinability during development of the inner cell mass and trophoblast of mouse blastocysts in vitro, J. Reprod. Fertil. 52: 239–248.Google Scholar
  267. Stacey, N. H., Bishop, C. J., Halliday, J. W., Halliday, W. J., Cooksley, W. G. E., Powell, L. W., and Kerr, J. F. R., 1985, Apoptosis as the mode of cell death in antibody-dependent lymphocytotoxicity, J. Cell Sci. 74: 169–179.PubMedGoogle Scholar
  268. Stewart, I., and Peel, S., 1981, Granulated metrial gland cells in the virgin and early pregnant mouse uterus, J. Anat. 133: 535–541.PubMedGoogle Scholar
  269. Surani, M. A. H., 1979, Glycoprotein synthesis and inhibition of glycosylation by tunicamycin in preimplantation mouse embryos: Compaction and trophoblast adhesion, Cell 18: 217–227.PubMedCrossRefGoogle Scholar
  270. Tachi, C., and Tachi, S., 1974, Cellular aspects of ovum implantation and decidualization in the rat, in: Physiology and Genetics of Reproduction, Part B ( E. M. Coutinho and F. Fuchs, eds.), Plenum Press, New York, pp. 263–286.Google Scholar
  271. Tachi, C., Tachi, S., Knyszynski, A., and Lindner, H. R., 1981, Possible involvement of macrophages in embryo-maternal relationships during ovum implantation in the rat, J. Exp. Zool. 217: 81–92.PubMedCrossRefGoogle Scholar
  272. Tachi, S., Tachi, C., and Lindner, H. R., 1970, Ultrastructural features of blastocyst attachment and trophoblastic invasion in rat, J. Reprod. Fertil. 21: 37–56.PubMedCrossRefGoogle Scholar
  273. Tawfik, O. W., Hunt, J. S., and Wood, G. W., 1986, Implication of prostaglandin E2 in soluble factor-mediated immune suppression by murine decidual cells, Am. J. Reprod. Immunol. Microbiol. 12: 111–117.PubMedGoogle Scholar
  274. Thie, M., Bochskanl, R., and Kirchner, C., 1986, Glycoproteins in rabbit uterus during implantation. Differential localization visualized using 3H-N-acetyl-glucosamine labeling and FITC-conjugated lectins, Histochemistry 84: 73–79.PubMedCrossRefGoogle Scholar
  275. Tobert, J. A., 1976, A study of the possible role of prostaglandins in decidualization using a nonsurgical method for the instillation of fluids into the uterine lumen, J. Reprod. Fertil. 47: 391–393.PubMedCrossRefGoogle Scholar
  276. Tung, H. N., Parr, M. B., and Parr, E. L., 1986, The permeability of the primary decidual zone in the rat uterus: An ultrastructural tracer and freeze-fracture study, Biol. Reprod. 35: 1045–1058.PubMedCrossRefGoogle Scholar
  277. Umapathysivam, K., and Jones, W. R., 1978, An investigation of decidual specific proteins in the rat, Int. J. Fertil. 23: 138–142.PubMedGoogle Scholar
  278. Velardo, J. T., Dawson, A. B., Olsen, A. G., and Hisaw, F. L., 1953, Sequence of histological changes in the uterus and vagina of the rat during prolongation of pseudopregnancy associated with the presence of deciduomata, Am. J. Anat. 93: 273–305.CrossRefGoogle Scholar
  279. Watson, J., and Patek, E. E., 1979, Steroid and prostaglandin secretion by the corpus luteum, endometrium and embryos of cyclic and pregnant pigs, J. Endocrinol. 82: 425–428.PubMedCrossRefGoogle Scholar
  280. Webb, C. G., and Duskin, D., 1981, Involvement of glycoproteins in the development of early mouse embryos: Effect of tunicamycin and a, a’-dipyridyl in vitro, Differentiation 20: 81–86.Google Scholar
  281. Weitlauf, H., 1979, Implantation, in: Animal Models for Research on Conception and Fertility ( N. J. Alexander, ed.), PARFR Series on Fertility Regulation, Harper & Row, Hagerstown, MD, pp. 238–252.Google Scholar
  282. Welsh, A. O., and Enders, A. C., 1985, Light and electron microscopic examination of the mature decidual cells of the rat with emphasis on the antimesometrial decidua and its degeneration, Am. J. Anat. 172: 1–29.PubMedCrossRefGoogle Scholar
  283. Welsh, A. O., and Enders, A. C., 1987, Trophoblast-decidual cell interactions and establishment of maternal blood circulation in the parietal yolk sac placenta of the rat, Anat. Rec. 217: 203–219.PubMedCrossRefGoogle Scholar
  284. Wordinger, R. J., and Amsler, K. R., 1980, Histochemical identification of the glycocalyx layer in the bovine oviduct and endometrium, Anim. Reprod. Sci. 3: 189–193.CrossRefGoogle Scholar
  285. Wu, J. T., 1980a, Concanavalin A binding capacity of preimplantation mouse embryos, J. Reprod. Fertil. 58: 455–461.PubMedCrossRefGoogle Scholar
  286. Wu, J. T., 1980b, Concanavalin A binding capacity of preimplanation rat embryos, J. Exp. Zool. 213: 377–382.CrossRefGoogle Scholar
  287. Wu, J. T., and Chang, M. C., 1978, Increase in concanavalin A binding sites in mouse blastocysts during implantation, J. Exp. Zool. 105: 447–453.CrossRefGoogle Scholar
  288. Wu, J. T., and Gu, Z., 1981, The effect of intrauterine injection of concanavalin A on implantation in mice and rats, Contraception 23: 667–676.PubMedCrossRefGoogle Scholar
  289. Wyllie, A. H., 1981, Cell death: A new classification separating apoptosis from necrosis, in: Cell Death in Biology and Pathology ( I. D. Bowen and R. A. Lockshin, eds.), Chapman and Hall, London, pp. 9–34.CrossRefGoogle Scholar
  290. Wyllie, A. H., Kerr, J. F. R., and Currie, A. R., 1980, Cell death: The significance of apoptosis, Int. Rev. Cytol. 68: 251–306.PubMedCrossRefGoogle Scholar
  291. Yamamoto, A., 1982, Purification and assay of PGH synthase from bovine seminal vesicles, Methods Enzymol. 86: 55–60.PubMedCrossRefGoogle Scholar
  292. Yanagimachi, R., and Nicolson, G. L., 1976, Lectin-binding properties of hamster egg zona pellucida and plasma membrane during maturation, Exp. Cell Res. 100: 249–257.PubMedCrossRefGoogle Scholar
  293. Yoshinaga, K., 1972, Rabbit antiserum to rat deciduoma, Biol. Reprod. 6: 51–57.Google Scholar
  294. Yoshinaga, K., 1974, Interspecific cross-reactivity of deciduoma antiserum: Interaction between mouse deciduoma and antiserum to rat deciduoma, Biol. Reprod. 11: 50–55.PubMedCrossRefGoogle Scholar
  295. Yoshinaga, K. (ed.), 1986, Annals of the New York Academy of Sciences, Volume 476, Nidation, New York Academy of Sciences, New York.Google Scholar
  296. Young, J. D. -E., and Cohn, Z. A., 1986, Cell-mediated killing: A common mechanism, Cell 46: 641–642.PubMedCrossRefGoogle Scholar
  297. Zorn, T. M. T., Bevilacqua, E. M. A. F., and Abrahamsohn, P. A., 1986, Collagen remodeling during decidualization in the mouse, Cell Tissue Res. 244: 443–448.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Publishing Corporation 1989

Authors and Affiliations

  • Margaret B. Parr
    • 1
  • Earl L. Parr
    • 1
  1. 1.Department of AnatomySchool of Medicine, Southern Illinois UniversityCarbondaleUSA

Personalised recommendations