Skip to main content

The Implantation Reaction

  • Chapter

Abstract

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).

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abrahamsohn, P. A., 1983, Ultrastructural study of the mouse antimesometrial decidua, Anat. Embryol. 166: 263–274.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Anteby, S. O., Bauminger, S., Zor, U., and Lindner, H. R., 1975, Prostaglandin synthesis in decidual tissue of the rat, Prostaglandins 10: 991–999.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Basuray, R., and Gibori, G., 1980, Luteotropic action of the decidual tissue of the pregnant rat, Biol. Reprod. 23: 507–512.

    Google Scholar 

  • 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 

  • Bazer, F. W., and First, N. L., 1983, Pregnancy and parturition, J. Anim. Sci. 57 (Suppl. 2): 425–460.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bell, B. C., 1983, Decidualization: Regional differentiation and associated function, Oxford Rev. Reprod. Biol. 5: 220–271.

    Google Scholar 

  • Bell, S. C., and Searle, R. F., 1981, Differentiation of decidual cells in mouse endometrial cell cultures, J. Reprod. Fértil. 61: 425–433.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bell, S. C., Hamer, J., and Heald, P. J., 1980, Induced protein and deciduoma formation in rat uterus, Biol. Reprod. 23: 935–940.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Bill, A., Tornquist, P., and Aim, A., 1980, Permeability of the intraocular blood vessels, Trans. Ophthalmol. Soc. U. K. 100: 332–336.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Boshier, D. P., 1970, The Pontamine Blue reaction in pregnant sheep uteri, J. Reprod. Fértil. 22: 595–596.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Boving, B. G., 1962, Anatomical analysis of rabbit trophoblast invasion, Contrib. Embryol. 37: 33–54.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Bulmer, D., Peel, S., and Stewart, I., 1987, The metrial gland, Cell Differ. 20: 77–86.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Carson, D. C., Dutt, A., and Tang, J. P., 1987, Glycoconjugate synthesis during early pregnancy: Hyaluronate synthesis and function, Dev. Biol. 120: 228–235.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Cerottini, J. -C., and Brunner, K. T., 1974, Cell-mediated cytotoxicity, allograft rejection, and tumor immunity, Adv. Immunol. 18: 67–87.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Chavez, D. J., and Enders, A. C., 1981, Temporal changes in lectin binding of peri-implantation mouse blastocysts, Develop. Biol. 87: 267–276.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Craig, S. S., and Jollie, W. P., 1981, Epithelial ultrastructure during decidualization in rats, Anat. Embryol. 163: 215–222.

    Article  Google Scholar 

  • 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 

  • Daniel, S. A. J., and Kennedy, T. G., 1987, Prostaglandin E2 enhances uterine stromal cell alkaline phosphatase activity in vitro, Prostaglandins 33: 241–252.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Denari, J. H., and Rosner, J. M., 1978, Studies on biochemical characteristics of early decidual protein, Int. J. Fertil. 23: 123–127.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Denker, H. -W., 1980, Role of proteinases in implantation, Prog. Reprod. Biol. 7: 28–42.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Edelman, G. M., 1983, Cell adhesion molecules, Science 219: 450–457.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Enders, A. C., and Nelson, D. M., 1973, Pinocytotic activity of the uterus of the rat, Am. J. Anat. 138: 277–300.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Enders, A. C., and Schlafke, S., 1969, Cytological aspects of trophoblast-uterine interaction in early implantation, Am. J. Anat. 125: 1–30.

    Google Scholar 

  • Enders, A. C., and Schlafke, S., 1972, Implantation in the ferret: Epithelial penetration, Am. J. Anat. 133: 291–316.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Finn, C. A., 1965, Oestrogen and the decidual cell reaction of implantation in mice, J. Endocrinol. 32: 223–229.

    Article  PubMed  CAS  Google Scholar 

  • Finn, C. A., 1977, The implantation reaction, in: Biology of the Uterus ( R. M. Wynn, ed.), Plenum Press, New York, pp. 245–308.

    Chapter  Google Scholar 

  • Finn, C. A., 1980, The endometrium during implantation, in: The Endometrium, ( F. A. Kimball, ed.), Spectrum, New York, pp. 43–56.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Dey, S. K., Chien, S. M., Cox, C. L., and Crist, R. D., 1980, Prostaglandin synthesis in the rabbit blastocyst, Prostaglandins 19: 449–453.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Finn, C. A., and Porter, D. G., 1975, The Uterus, Publishing Sciences Group, Acton, UK.

    Google Scholar 

  • Flower, R. J., and Blackwell, G. J., 1976, The importance of phospholipase-A2 in prostaglandin biosynthesis, Biochem. Pharmacol. 25: 285–291.

    Article  PubMed  CAS  Google Scholar 

  • Gilula, N. B., Reeves, O. R., and Steinback, A., 1972, Metabolic coupling, ionic coupling, and cell contacts, Nature 235: 262–265.

    Article  PubMed  CAS  Google Scholar 

  • Glasser, S. R., 1985, Laboratory models of implantation, in: Reproductive Toxicology ( R. L. Dixon, ed.), Raven Press, New York, pp. 219–238.

    Google Scholar 

  • Glasser, S. R., and Bullock, D. W. (eds.), 1981, Cellular and Molecular Aspects of Implantation, Plenum Press, New York.

    Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Goldstein, L. J., and Hayes, C. E., 1979, The lectins: Carbohydrate-containing proteins of plants and animals, Adv. Carbohyd. Chem. Biochem. 35: 127–167.

    Article  Google Scholar 

  • Guillomot, M., Flechon, J. -E., and Wintenberger-Torres, S., 1981, Conceptus attachment in the ewe: An ultrastructural study, Placenta 2: 169–182.

    Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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 

  • Hicks, J. J., and Guzman-Gonzalez, A. M., 1979, Inhibition of implantation by intraluminal administration of concanavalin A in mice, Contraception 20: 129–136.

    Article  PubMed  CAS  Google Scholar 

  • Hoffman, L. H., and Hoos, P. C., 1984, Morphology of vascular leakage at rabbit implantation sites, Anat. Rec. 208: 75.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Holmes, P. V., and Gordashko, B. J., 1980, Evidence of prostaglandin involvement in blastocyst implantation, J. Embryol. Exp. Morphol. 55: 109–122.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Irvine, R. F., 1982, How is the level of free arachidonic acid controlled in mammalian cells Biochem J. 204: 3–16.

    PubMed  CAS  Google Scholar 

  • 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 

  • Jeffrey, J. J., 1981, Collagen synthesis and degradation in the uterine deciduoma: Regulation of collagenase activity by progesterone, Coll. Relat. Res. 1: 257–268.

    CAS  Google Scholar 

  • Jenkinson, E. J., and Searle, R. F., 1977, Cell surface changes on the mouse blastocyst at implantation, Exp. Cell Res. 106: 386–390.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Jollie, W. P., and Bencosme, S. A., 1965, Electron microscopic observations n primary decidua formation in the rat, Am. J. Anat. 116: 216–236.

    Article  Google Scholar 

  • Joshi, S. G., Szarowski, D. H., and Bank, J. F., 1981, Decidua-associated antigens in the baboon, Biol. Reprod. 25: 591–598.

    Article  PubMed  CAS  Google Scholar 

  • Kearns, M., and Lala, P. K., 1983, Life history of decidual cells: A review, Am. J. Reprod. Immunol. 3: 78–82.

    CAS  Google Scholar 

  • Kennedy, T. G., 1977, Evidence for a role for prostaglandins in the initiation of blastocyst implantation in the rat, Biol. Reprod. 16: 286–291.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, T. G., 1980a, Estrogen and uterine sensitization for the decidual cell reaction: Role of prostaglandins, Biol. Reprod. 23: 955–962.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, T. G., 1980b, Timing of uterine sensitivity for the decidual cell reaction: Role of prostaglandins, Biol. Reprod. 22: 519–525.

    PubMed  CAS  Google Scholar 

  • Kennedy, T. G., 1983a, Embryonic signals and the initiation of blastocyst implantation, Aust. J. Biol. Sci. 36: 531–543.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, T. G., 1985, Evidence for the involvement of prostaglandins throughout the decidual cell reaction in the rat, Biol. Reprod. 33: 140–16.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Kennedy, T. G., and Lukash, L. A., 1982, Induction of decidualization in rats by the ultrauterine infusion of prostaglandins, Biol. Reprod. 27: 253–260.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Kerr, J. F. R., Bishop, C. J., and Searle, J., 1984, Apoptosis, Recent Adv. Histopathol. 12: 1–15.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Kirkwood, K. J., 1981, Immunoglobulin and complement receptor-bearing cells in cultures of mouse decidual tissue, J. Reprod. Fertil. 62: 345–352.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • Leroy, F., Finn, C. A., Psychoyos, A., and Hubinont, P. O. (eds.), 1980, Progress in Reproductive Biology, Volume 7, S. Karger, Basel.

    Google Scholar 

  • Lewis, G. S., and Waterman, R. A., 1983, Metabolism of arachidonic acid in vitro by porcine blastocysts and endometrium, Prostaglandins 25: 871–880.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Loewenstein, W. R., 1966, Permeability of membrane junctions, Ann. N. Y. Acad. Sci. 137: 441–472.

    Article  PubMed  CAS  Google Scholar 

  • Lundkvist, O., 1979, Morphometric estimation of stromal edema during delayed implantation in the rat, Cell Tissue Res. 199: 339–348.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Magnuson, T., and Stackpole, C. W., 1978, Lectin-mediated agglutination of preimplantation mouse embryos, Exp. Cell Res. 116: 466–469.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Martello, E. M. V. G., and Abrahamsohn, P. A., 1986, Collagen distribution in the mouse endometrium during decidualization, Acta Anat. 127: 146–150.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Martz, E., 1987, LFA-1 and other accessory molecules functioning in adhesion of T and B lymphocytes, Hum. Immunol. 18: 3–37.

    Article  PubMed  CAS  Google Scholar 

  • Matter, A., 1979, Microcinematographic and electron microscopic analysis of target cell lysis induced by cytotoxic T lymphocytes, Immunology 36: 179–190.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Mossman, H. W., 1937, Comparative morphogenesis of the fetal membranes and accessory uterine structures, Contrib. Embryol. Carnegie Inst. 26: 129–246.

    Google Scholar 

  • Moulton, B. C., 1974, Ovum implantation and uterine lysosomal enzyme activity, Biol. Reprod. 10: 543–548.

    Article  PubMed  CAS  Google Scholar 

  • Moulton, B. C., 1984, Epithelial cell function during blastocyst implantation, J. Biosci. 6 (Suppl. 2): 11–21.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Nilsson, O., 1966a, Estrogen-induced increase of adhesiveness in uterine epithelium of mouse and rat, Exp. Cell Res. 43: 239–241.

    Article  PubMed  CAS  Google Scholar 

  • Nilsson, O., 1966b, Structural differentiation of luminal membrane in rat uterus during normal and experimental implantations, Z. Anat. Entwickl. 125: 152–159.

    Article  CAS  Google Scholar 

  • Nilsson, O., 1972, Ultrastructure of the process of secretion in the rat uterine epithelium at preimplantation, J. Ultrastruct. Res. 40: 572–580.

    Article  PubMed  CAS  Google Scholar 

  • Nilsson, O., 1974, Changes of the luminal surface of the rat uterus of blastocyst implantation, Z. Anat. Entwickl. 144: 337–342.

    Article  CAS  Google Scholar 

  • Nilsson, O., Lindqvist, I., and Ronquist, G., 1973, Decreased surface charge of mouse blastocysts at implantation, Exp. Cell Res. 83: 421–423.

    Google Scholar 

  • Nilsson, O., Lindqvist, I., and Ronquist, G., 1975, Blastocyst surface charge and implantation in the mouse, Contraception 11: 441–450.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Nimura, S., and Ishida, K., 1987, Immunohistochemical demonstration of prostaglandin E2 in preimplantation mouse embryos, J. Reprod. Fertil. 80: 505–508.

    Google Scholar 

  • Obrink, B., 1986, Epithelial cell adhesion molecules, Exp. Cell Res. 163: 1–21.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Parr, M. B., 1980, Endocytosis in the uterine epithelium during early pregnancy, Prog. Reprod. Biol. 7: 81–91.

    Google Scholar 

  • Parr, M. B., 1983, Relationship of uterine closure to ovarian hormones and endocytosis in the rat, J. Reprod. Fertil. 68: 185–188.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Parr, M. B., and Parr, E. L., 1977, Endocytosis in the uterine epithelium of the mouse, J. Reprod. Fertil. 50: 151–153.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Pierce, M., Turley, E. A., and Roth, S., 1980, Cell surface glycosyltransferase activities, Int. Rev. Cytol. 65: 1–47.

    Google Scholar 

  • 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 

  • Pinsker, M. C., Sacco, A. G., and Mintz, B., 1974, Implantation-associated proteinase in mouse uterine fluid, Dev. Biol. 38: 285–290.

    Google Scholar 

  • Pisam, M., and Ripoche, P., 1976, Redistribution of surface macromolecules in dissociated epithelial cells, J. Cell Biol. 71: 907–920.

    Article  PubMed  CAS  Google Scholar 

  • Podack, E. R., 1985, The molecular mechanism of lymphocyte mediated tumor cell lysis, Immunol. Today 6: 21–27.

    Article  CAS  Google Scholar 

  • Poelmann, R. E., 1975, An ultrastructural study of implanting mouse blastocysts: Coated vesicles and epithelium formation, J. Anat. 119: 421–434.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • Racowsky, C., and Biggers, J. D., 1983, Are blastocyst prostaglandins produced endogenously? Biol. Reprod. 29: 379–388.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • Reinius, S., 1967, Ultrastructure of blastocyst attachment in the mouse, Z. Zellforsch. Mikrosk. Anat. 77: 257–266.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Roseman, S., 1970, The synthesis of complex carbohydrates by multiglycosyltransferase systems and the potential function in intercellular adhesion, Chem. Phys. Lipids 5: 270–299.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Sananes, N., and Le Goascogne, C., 1976, Decidualization in prepuberal rat uterus, Differentiation 5: 133–144.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Sananes, N., Weiller, S., Baulieu, E. -E., and Le Goascogne, C., 1980, Decidualization in vitro, Prog. Reprod. Biol. 7: 125–134.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Schlafke, S., and Enders, A. C., 1975, Cellular basis of interaction between trophoblast and uterus at implantation, Biol. Reprod. 12: 41–65.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Shur, B. D., 1983, Embryonal carcinoma cell adhesion: The role of surface galactosyltransferase and its 90K lactosaminoglycan substrate, Dev. Biol. 99: 360–372.

    Article  PubMed  CAS  Google Scholar 

  • Shur, B. D., 1984, The receptor function of galactosyltransferases during cellular interactions, Mol. Cell. Biochem. 61: 143–158.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sobel, J. S., and Nebel, L., 1976, Concanavalin A agglutinability of developing mouse trophoblast, J. Reprod. Fertil. 47: 399–402.

    Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Stewart, I., and Peel, S., 1981, Granulated metrial gland cells in the virgin and early pregnant mouse uterus, J. Anat. 133: 535–541.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Umapathysivam, K., and Jones, W. R., 1978, An investigation of decidual specific proteins in the rat, Int. J. Fertil. 23: 138–142.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Wu, J. T., 1980a, Concanavalin A binding capacity of preimplantation mouse embryos, J. Reprod. Fertil. 58: 455–461.

    Article  PubMed  CAS  Google Scholar 

  • Wu, J. T., 1980b, Concanavalin A binding capacity of preimplanation rat embryos, J. Exp. Zool. 213: 377–382.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Wyllie, A. H., Kerr, J. F. R., and Currie, A. R., 1980, Cell death: The significance of apoptosis, Int. Rev. Cytol. 68: 251–306.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto, A., 1982, Purification and assay of PGH synthase from bovine seminal vesicles, Methods Enzymol. 86: 55–60.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga, K., 1972, Rabbit antiserum to rat deciduoma, Biol. Reprod. 6: 51–57.

    CAS  Google Scholar 

  • Yoshinaga, K., 1974, Interspecific cross-reactivity of deciduoma antiserum: Interaction between mouse deciduoma and antiserum to rat deciduoma, Biol. Reprod. 11: 50–55.

    Article  PubMed  CAS  Google Scholar 

  • Yoshinaga, K. (ed.), 1986, Annals of the New York Academy of Sciences, Volume 476, Nidation, New York Academy of Sciences, New York.

    Google Scholar 

  • Young, J. D. -E., and Cohn, Z. A., 1986, Cell-mediated killing: A common mechanism, Cell 46: 641–642.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1989 Plenum Publishing Corporation

About this chapter

Cite this chapter

Parr, M.B., Parr, E.L. (1989). The Implantation Reaction. In: Wynn, R.M., Jollie, W.P. (eds) Biology of the Uterus. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5589-2_9

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-5589-2_9

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-5591-5

  • Online ISBN: 978-1-4684-5589-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics