Cellular aspects of implantation

  • Daniel J. Chávez
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 2)


Implantation is an essential and integral component of the reproductive process in all mammals except the Monotremes (egg layers). Several reviews treating morphological (19, 68, 25), comparative (83), and evolutionary (1) aspects of implantation have appeared in recent years. This chapter focuses on cellular and molecular interactions between the trophoblast and uterus of Metatherian (placental) mammals. Most of the present knowledge about implantation has been derived from experimentation with laboratory and domestic species, with occasional observations from wild animals and humans. There are fundamental similarities of implantation that are common to all mammals, and these similarities are discussed herein. A few examples of variation are cited for reasons of contrast, but for the most part, atypical variations are excluded.


Zona Pellucida Trophoblast Cell Luminal Epithelium Uterine Epithelium Mouse Blastocyst 
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  1. 1.
    Amoroso EC: Viviparity. In: Cellular and Molecular Aspects of Implantation. Glasser S, Bullock (eds) Plenum Press, New York and London, 1981, pp 3–25.Google Scholar
  2. 2.
    Aitken RJ: Embryonic diapause. Devi in Mammals 1: 307–359, 1977.Google Scholar
  3. 3.
    Beer AE, Billingham RE: Implantation, transplantation and epithelial-mesenchymal relationships in the rat uterus. J Exp Med 132: 721–736, 1970.PubMedCrossRefGoogle Scholar
  4. 4.
    Beier HM: The role of uterine proteins in the establishment of the receptivity of the uterus. Prog Reprod Biol 7: 158–172, 1980.Google Scholar
  5. 5.
    Blandau RJ: The female reproductive system. In: Histology. Weiss Greep RO (eds) McGraw-Hill, 4th ed, 1977, pp 881–924.Google Scholar
  6. 6.
    Booher C, Enders AC, Hendrickx AG, Hess DL: Structural characteristics of the corpus lutem during implantation in the Rhesus Monkey (Macaca mulatta) Am J Anat: 160: 17–36, 1981.PubMedCrossRefGoogle Scholar
  7. 7.
    Boving BG: Biomechanics of implantation. In: Biology of the Blastocyst. Blandau RJ (ed) The University of Chicago Press, Chicago and London, 1971, pp 423–442.Google Scholar
  8. 8.
    Chávez DJ: Polar differences in trophoblast cells of peri-implantation mouse blastocysts. J Cell Biol 95: 143A, 1982.Google Scholar
  9. 9.
    Chávez DJ, Enders AC: Temporal changes in lectin binding of peri-implantation mouse blastocysts. Devel Biol 87: 267–286, 1981.CrossRefGoogle Scholar
  10. 10.
    Chávez DJ, Enders AC: Lectin binding of mouse blastocyst: Appearance of Dolichos biflorus binding sites on the trophoblast during delayed implantation and their subsequent disappearance during implantation. Biol Reprod 26: 545–552, 1982.PubMedCrossRefGoogle Scholar
  11. 11.
    Chávez DJ, Van Blerkom J: In Vitro Attachment and Outgrowth of mouse Trophectoderm. In: Cellular and Molecular Aspects of Implantation, 1981.Google Scholar
  12. 12.
    Chen LT, Hsu YC: Development of mouse embryos in vitro: Pre-implantation to the limb bud stage. Science 218: 66–68, 1982.PubMedCrossRefGoogle Scholar
  13. 13.
    Cole RJ: Cinemicrographic observations on the trophoblast and zona pellucida of the mouse blastocyst. J Embryol exp Morph 17: 181–490, 1967.Google Scholar
  14. 14.
    De Bunilla H, Rasweiler JJ: Breeding activity, preimplantation development, and oviduct histology of the short-tailed fruit bat, Carollia in captivity. Anat Ree 179: 385–403, 1974.CrossRefGoogle Scholar
  15. 15.
    Denker H-W: Role of proteinases in implantation. Prog Reprod Biol 7: 28–42, 1981.Google Scholar
  16. 16.
    Dickmann Z, Dey SK, SenGupta J: A new concept: Control of early pregnancy by steroid hormones originating in the preimplantation embryo. Vitamins and Hormones 34: 215–242, 1976.PubMedCrossRefGoogle Scholar
  17. 17.
    Dupont H, Esnault C, Duluc AJ, Mayer G: Evolution de la polyploidie dans le deciduome experimental chez la ratte en grossesse unilaterale. Etude cytophotometrique. Cr hebd Seanc Acad Sci (Paris) 279: 501–504, 1974.Google Scholar
  18. 18.
    El-Sherdhaby AM, Hinchliffe JR: Epithelial autolysis during implantation of the mouse blastocyst an ultrastructural study. J Embryol exp Morph 33: 1067–1080, 1975.Google Scholar
  19. 19.
    Enders AC: Anatomical aspects of implantation. J Reprod Fert, Suppl 25: 1–15, 1977.Google Scholar
  20. 20.
    Enders AC: The fine structure of the blastocyst. In: The Biology of the Blastocyst Blandan RJ (ed) the University of Chicago Press, 1971, pp 71–88.Google Scholar
  21. 21.
    Enders AC, Chávez DJ, Schlafke S: Comparison of Implantation in utero and in vitro. Cellular and Molecular Aspects of Implantation. Glasser, Bullock (eds) Plenum, 1981, pp 365–382.Google Scholar
  22. 22.
    Enders AC, Schlafke S: Penetration of the uterine epithelium during implantation in the rabbit. Am J Anat 132: 219–240, 1971.PubMedCrossRefGoogle Scholar
  23. 23.
    Enders AC, Schlafke S: Implantation in the ferret: epithelial penetration. Am J Anat 133: 291–313, 1972.PubMedCrossRefGoogle Scholar
  24. 24.
    Enders AC, Schlafke S: Surface coats of the mouse blastocyst and uterus during the preimplantation period. Anat Ree 180: 31–46, 1974.CrossRefGoogle Scholar
  25. 25.
    Enders AC, Schlafke S: Comparative aspects of blastocyst-endometrial interactions at implantation. Maternal Recognition of Pregnancy CIBA Foundation Symposium 64 (new series) Heap B (ed) Excerpta Medica, 1979, pp 3–22.Google Scholar
  26. 26.
    Enders AC, Schlafke S: Differentiation of the blastocyst of the Rhesus Monkey. Am J Anat 162: 1–21, 1981.PubMedCrossRefGoogle Scholar
  27. 27.
    Fawcett DW, Wislocki GB, Waldo CM: The development of mouse ova in the anterior chamber of the eye and in the abdominal cavity. Amer J Anat 81: 413–433.Google Scholar
  28. 28.
    Gardner RL: Analysis of determination and differentiation in the early mammalian embryo using intra and interspecific chimeras. In: The Developmental Biology of Reproduction. -3rd Symposium of the Society for Developmental Biology. Markert EL, Papaconstantinon J (eds) Academic Press, Inc, 1975, pp 207–236.Google Scholar
  29. 29.
    Given RL, Enders AC: Mouse uterine glands during the peri-implantation period. II Autoradiographic studies. Anat Rec 199: 109–127.Google Scholar
  30. 30.
    Glass RH, Spindle AI, Pedersen RA: Mouse embryo attachment to substratum and interaction of trophoblast with cultured cells. J Exp Zool 208: 327–336.Google Scholar
  31. 31.
    Glasser SR Clark JH: A determinant role for progesterone in the development of uterine sensitivity to decidualization and ovo-implantation. The developmental Biology of Reproduction. Markert CL, Papaconstantinou J (eds) Academic Press, 1975, pp 311–345.Google Scholar
  32. 32.
    Glenister TW: Embryo-endometrial relationships during nidation in organ culture. J Obstet Gynaecol Br Commonw 69: 809–814, 1962.CrossRefGoogle Scholar
  33. 33.
    Gonda MA, Hsu Y-C: Correlative scanning electron, transmission electron, and light microscopic studies of the in vitro development of mouse embryos on a plastic substrate at the implantation stage. J Embryol exp Morph 56: 23–39, 1980.PubMedGoogle Scholar
  34. 34.
    Hsu, Y-C: Post-blastocyst differentiation in vitro. Nature, London 231: 100, 1971.CrossRefGoogle Scholar
  35. 35.
    Hsu Y-C: Differentiation in vitro of mouse embryos beyond the implantation stage. Nature, London 239: 200, 1972.CrossRefGoogle Scholar
  36. 36.
    Hsu Y-C, Baskar J, Stevens LC, Rash JE: Development in vitro of mouse embryos from the two-cell egg stage to the early somite stage. J Embryol Exp Morph 31: 235–245.Google Scholar
  37. 37.
    Humphrey KW: The induction of implantation in the mouse after ovariectomy. Steroids 19: 591–600, 1967.CrossRefGoogle Scholar
  38. 38.
    Jenkinson EJ: The in vitro blastocyst outgrowth system as a model for the analysis of peri-implantation development. In: Development in Mammals, Vol. 2 Johnson M (ed) Amsterdam, 1978. pp 151–172.Google Scholar
  39. 39.
    Jenkinson EJ, Searle RF: Cell surface changes on the mouse blastocyst at implantation. Exp Cell Res 106: 386–390.Google Scholar
  40. 40.
    Kirby DRS, Potts DM, Wilson LB: On the orientation of the implanting blastocyst. J Embryol Exp Morph 17: 527–532, 1967.PubMedGoogle Scholar
  41. 41.
    Lenton EA, Sulaiman R, Sobowale O, Cooke ID: The human menstrual cycle: plasma concentrations of prolactin, LH, FSH, oestradiol and progesterone in conceiving and non-conceiving women. J Reprod Fertil 65: 131–139, 1982.PubMedCrossRefGoogle Scholar
  42. 42.
    McLaren A: Delayed loss of the zona pellucida from blastocysts of suckling mice. J Reprod Fert 14: 159–162, 1967.CrossRefGoogle Scholar
  43. 43.
    McLaren A: A study of blastocysts during delay and subsequent implantation in lactating mice. J Endocr 42: 453–463, 1968.PubMedCrossRefGoogle Scholar
  44. 44.
    McLaren A: The fate of the zona pellucida in mice. J Embryol exp Morph 23: 1–19, 1970a.PubMedGoogle Scholar
  45. 45.
    McLaren A: Early embryo-endometrial relationships. Ovo-Implantation. Human Gonadotropins and Prolactin. Karger, Basel. 1970b. pp 18–73.Google Scholar
  46. 46.
    McLaren A: Blastocyst activation. In: The Regulation of Mammalian Reproduction Segal SJ, Corzier R, Corfman PA, Condliffe PG (eds) Thomas, Springfield, Ill, 1973, pp 321–334.Google Scholar
  47. 47.
    Mintz B: Control of embryo implantation and survival. Adv Biosciences 6: 317–342, 1971.Google Scholar
  48. 48.
    Mossman HW: Orientation and site of attachment of the blastocyst: A comparative study. In: The Biology of the Blastocyst Blandau RJ (ed) The University of Chicago Press, 1971, pp 49–58.Google Scholar
  49. 49.
    Nilsson O: Ultrastructure of the trophoblast-epithelial junction at blastocyst implantation in the mouse. Exp Cell Res 94: 434–436, 1975.PubMedCrossRefGoogle Scholar
  50. 50.
    Nilsson O: Ultrastructure of trophoblast-epithelium relations during implantation in the mouse. In: Reproductive Endocrinology. Proteins and Steroids in Early Mammalian Development (ICE Satellite Symposium, Aachen, 1976 ) Beier HM, Karlson P (eds) Springer-Verlag, New York, 1979.Google Scholar
  51. 51.
    Nilsson O, Lindqvist I, Ronquist G: Decreased surface charge of mouse blastocysts at implantation. Exp Cell Res 83: 421–423, 1973.CrossRefGoogle Scholar
  52. 52.
    Nilsson O, Naeslund G, Curman B: Polar differences of delayed and implanting mouse blastocysts in binding of alcian blue and Con-canavalin A. J Exp Zool 214: 117–180.Google Scholar
  53. 53.
    Orsini MW, McLaren A: Loss of the zona pellucida in mice, and the effect of tubal ligation and ovariectomy. J Reprod Fert 13: 485–499, 1967.CrossRefGoogle Scholar
  54. 54.
    Padykula HA: Shifts in Uterine Stromal Cell populations during pregnancy and regression. In: Cellular and Molecular Aspects of Implantation. Glasser SR, Bullock DW (eds) Plenum Press, 1980, pp 197–216.Google Scholar
  55. 55.
    Perrota CA: Initiation of cell proliferation in the vaginal and uterine epithelia of the mouse. Am J Anat 111: 195–204, 1962.CrossRefGoogle Scholar
  56. 56.
    Pinsker MC, Sacco AG, Mintz B: Implantation-associated proteinase in mouse uterine fluid. Devel Biol 38: 285–290, 1974.CrossRefGoogle Scholar
  57. 57.
    Potts M: The attachment phase of ovimplantation. Am J Obstet Gynec 96: 1122–1128, 1966.PubMedGoogle Scholar
  58. 58.
    Potts DM: The ultrastructure of implantation in the mouse. J Anat 103: 77–90, 1968.PubMedGoogle Scholar
  59. 59.
    Potts M, Psychoyos A: L’ultrastructure des relations ovoendometriales au cours du retard experimental de nidation chez la Souris. C R Acad Sei Paris 264: 956–958, 1967.Google Scholar
  60. 60.
    Psychoyos A, Casimiri V: Factors involved in uterine receptivity and refractoriness. Prog Reprod Biol 7: 143–157, 1980.Google Scholar
  61. 61.
    Rasweilier JJ: Reproduction in the long-tongued bat Glossophaga soricina. I. Preimplantation development and histology of the oviduct. J Reprod Fertil 31: 249–262, 1972.CrossRefGoogle Scholar
  62. 62.
    Renfree MD: Influence of the embryo on the Marsupial uterus. Nature (London) 240: 475–477, 1972.CrossRefGoogle Scholar
  63. 63.
    Roth S, White D: Intercellular contact and cell surface galactosyl transferase activity. Proc Nat Acad Sei USA 69: 485–489, 1972.CrossRefGoogle Scholar
  64. 64.
    Rumery EE, Blandau RJ: Loss of zona pellucida and prolonged gestation in delayed implantation in mice. Biology of the Blastocyst. Blandau R (ed) p 115. University of Chicago Press, Chicago, 1966.Google Scholar
  65. 65.
    Salomon DS, Sherman MI: Implantation and invasiveness of mouse blastocysts on uterine monolayers. Exp Cell Res 90: 261–268, 1975.PubMedCrossRefGoogle Scholar
  66. 66.
    Sartor P: Cell proliferation and decidual morphogenesis. Prog reprod Biol 7: 115–124, 1980.Google Scholar
  67. 67.
    Serra MJ, Baggett B, Rankin JC, Ledford BE: The artificially stimulated decidual cell reaction in the mouse uterus. Studies of RNA polymerases and histone modifications. Cellular and Molecular Aspects of Implantation. Glasser SR, Bullock DW (eds) Plenum Press, 1981, pp 291–306.Google Scholar
  68. 68.
    Schlafke S, Enders AC: Cellular basis of interaction between tropho-blast and uterus at implantation. Biol Reprod 12: 41–65, 1975.PubMedCrossRefGoogle Scholar
  69. 69.
    Schmidt IG: Proliferation in the genital tract of the normal mature guinea pig treated with colchicine. Am J Anat 73: 59–80, 1980.CrossRefGoogle Scholar
  70. 70.
    Sellens MH, Sherman MI: Effects of culture conditions on the developmental programmes of mouse blastocysts. J Embryol exp Morph 56: 1–22, 1980.PubMedGoogle Scholar
  71. 71.
    Shalgi R, Sherman Ml: Scanning electron microscopy of the surface of normal and implantation-delayed mouse blastocysts during development in vitro. J Exp Zool 210: 69–80, 1979.PubMedCrossRefGoogle Scholar
  72. 72.
    Shelesnyak MC: Decidualization: The decidua and the deciduoma. Perspect Biol Med 5: 503–518, 1962.PubMedGoogle Scholar
  73. 73.
    Sherman MI, Salomon DS: The relationships between the early mouse embryo and its environment. In: The Developmental Biology of Reproduction. Markert CL, Papaconstantinou J (eds) 33rd Symposium of the Society for Developmental Biology, Academic Press, NY, 1975 pp 277–310.Google Scholar
  74. 74.
    Sherman MI, Shalgi R, Rizzino A, Sellens MH, Gay S, Gay R: Changes in the surface of the mouse blastocyst at implantation. In: Maternal Recognition of Pregnancy. Ciba Symposium 64 (New Series) Heap B (ed) Elsevier/North-Holland, 1979, p 48–52.Google Scholar
  75. 75.
    Steer, HW: Implantation of the rabbit blastocyst: The adhesive phase of implantation. J Anat 109: 215–228, 1971.PubMedGoogle Scholar
  76. 76.
    Surani MAH: Radiolabeled rat uterine luminal proteins and’ their regulation by estradiol and progesterone. J Reprod Fertil 50: 289–296, 1977.PubMedCrossRefGoogle Scholar
  77. 77.
    Surani MAH: Cellular and molecular approaches to blastocyst uterine interactions at implantation. Devel in Mammals 1: 245–305, 1977.Google Scholar
  78. 78.
    Van Blerkom J, Chàvez DJ, Bell H: Molecular and cellular aspects of facultative delayed implantation in the mouse. In: Maternal Recognition of Pregnancy. Heap B (ed) Excepta Medica, New York, 1979, p 141–172.Google Scholar
  79. 79.
    Van Blerkom J, Chavez DJ: Morphodynamics of mouse trophoblast outgrowth in the presence and absence of a uterine epithelium mo-nolayer. Am J Anat 162: 143–155, 1981.PubMedCrossRefGoogle Scholar
  80. 80.
    Wartiovaara J, Leivo I, Vaheri A: Expression of the cell surface- associated glycoptrotein, fibronectin, in the early mouse embryo. Devel Biol 69: 247–257, 1979.CrossRefGoogle Scholar
  81. 81.
    Weitlauf HM: Effect of uterine flushings on RNA synthesis by ‘implanting’ and ‘delayed implanting’ mouse blastocysts in vitro. Biol Reprod 14: 566–571, 1976.PubMedCrossRefGoogle Scholar
  82. 82.
    Weitlauf HM: Factors in mouse uterine fluid that inhibit the in-corporation of 3H-uridine by blastocysts in vitro. J Reprod Fertil 52: 321–325, 1978.PubMedCrossRefGoogle Scholar
  83. 83.
    Wimsatt Wa: Some comparative aspects of implantation. Biol Reprod 12: 1–40, 1975.PubMedCrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Daniel J. Chávez
    • 1
  1. 1.Department of Anatomy School of MedicineSouthern Illinois UniversityCarbondaleUSA

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