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Cellular aspects of implantation

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Ultrastructure of Reproduction

Part of the book series: Electron Microscopy in Biology and Medicine ((EMBM,volume 2))

Abstract

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.

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References

  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. Aitken RJ: Embryonic diapause. Devi in Mammals 1: 307–359, 1977.

    CAS  Google Scholar 

  3. Beer AE, Billingham RE: Implantation, transplantation and epithelial-mesenchymal relationships in the rat uterus. J Exp Med 132: 721–736, 1970.

    Article  PubMed  CAS  Google Scholar 

  4. Beier HM: The role of uterine proteins in the establishment of the receptivity of the uterus. Prog Reprod Biol 7: 158–172, 1980.

    CAS  Google Scholar 

  5. Blandau RJ: The female reproductive system. In: Histology. Weiss Greep RO (eds) McGraw-Hill, 4th ed, 1977, pp 881–924.

    Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. Chávez DJ: Polar differences in trophoblast cells of peri-implantation mouse blastocysts. J Cell Biol 95: 143A, 1982.

    Google Scholar 

  9. Chávez DJ, Enders AC: Temporal changes in lectin binding of peri-implantation mouse blastocysts. Devel Biol 87: 267–286, 1981.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. Chen LT, Hsu YC: Development of mouse embryos in vitro: Pre-implantation to the limb bud stage. Science 218: 66–68, 1982.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  Google Scholar 

  15. Denker H-W: Role of proteinases in implantation. Prog Reprod Biol 7: 28–42, 1981.

    Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    CAS  Google Scholar 

  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. Enders AC: Anatomical aspects of implantation. J Reprod Fert, Suppl 25: 1–15, 1977.

    Google Scholar 

  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. 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. Enders AC, Schlafke S: Penetration of the uterine epithelium during implantation in the rabbit. Am J Anat 132: 219–240, 1971.

    Article  PubMed  CAS  Google Scholar 

  23. Enders AC, Schlafke S: Implantation in the ferret: epithelial penetration. Am J Anat 133: 291–313, 1972.

    Article  PubMed  CAS  Google Scholar 

  24. Enders AC, Schlafke S: Surface coats of the mouse blastocyst and uterus during the preimplantation period. Anat Ree 180: 31–46, 1974.

    Article  CAS  Google Scholar 

  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. Enders AC, Schlafke S: Differentiation of the blastocyst of the Rhesus Monkey. Am J Anat 162: 1–21, 1981.

    Article  PubMed  CAS  Google Scholar 

  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. 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. Given RL, Enders AC: Mouse uterine glands during the peri-implantation period. II Autoradiographic studies. Anat Rec 199: 109–127.

    Google Scholar 

  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. 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. Glenister TW: Embryo-endometrial relationships during nidation in organ culture. J Obstet Gynaecol Br Commonw 69: 809–814, 1962.

    Article  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  34. Hsu, Y-C: Post-blastocyst differentiation in vitro. Nature, London 231: 100, 1971.

    Article  CAS  Google Scholar 

  35. Hsu Y-C: Differentiation in vitro of mouse embryos beyond the implantation stage. Nature, London 239: 200, 1972.

    Article  CAS  Google Scholar 

  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. Humphrey KW: The induction of implantation in the mouse after ovariectomy. Steroids 19: 591–600, 1967.

    Article  Google Scholar 

  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. Jenkinson EJ, Searle RF: Cell surface changes on the mouse blastocyst at implantation. Exp Cell Res 106: 386–390.

    Google Scholar 

  40. Kirby DRS, Potts DM, Wilson LB: On the orientation of the implanting blastocyst. J Embryol Exp Morph 17: 527–532, 1967.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  42. McLaren A: Delayed loss of the zona pellucida from blastocysts of suckling mice. J Reprod Fert 14: 159–162, 1967.

    Article  CAS  Google Scholar 

  43. McLaren A: A study of blastocysts during delay and subsequent implantation in lactating mice. J Endocr 42: 453–463, 1968.

    Article  PubMed  CAS  Google Scholar 

  44. McLaren A: The fate of the zona pellucida in mice. J Embryol exp Morph 23: 1–19, 1970a.

    PubMed  CAS  Google Scholar 

  45. McLaren A: Early embryo-endometrial relationships. Ovo-Implantation. Human Gonadotropins and Prolactin. Karger, Basel. 1970b. pp 18–73.

    Google Scholar 

  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. Mintz B: Control of embryo implantation and survival. Adv Biosciences 6: 317–342, 1971.

    Google Scholar 

  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. Nilsson O: Ultrastructure of the trophoblast-epithelial junction at blastocyst implantation in the mouse. Exp Cell Res 94: 434–436, 1975.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  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. 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.

    Article  CAS  Google Scholar 

  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. Perrota CA: Initiation of cell proliferation in the vaginal and uterine epithelia of the mouse. Am J Anat 111: 195–204, 1962.

    Article  Google Scholar 

  56. Pinsker MC, Sacco AG, Mintz B: Implantation-associated proteinase in mouse uterine fluid. Devel Biol 38: 285–290, 1974.

    Article  CAS  Google Scholar 

  57. Potts M: The attachment phase of ovimplantation. Am J Obstet Gynec 96: 1122–1128, 1966.

    PubMed  CAS  Google Scholar 

  58. Potts DM: The ultrastructure of implantation in the mouse. J Anat 103: 77–90, 1968.

    PubMed  CAS  Google Scholar 

  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.

    CAS  Google Scholar 

  60. Psychoyos A, Casimiri V: Factors involved in uterine receptivity and refractoriness. Prog Reprod Biol 7: 143–157, 1980.

    Google Scholar 

  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.

    Article  Google Scholar 

  62. Renfree MD: Influence of the embryo on the Marsupial uterus. Nature (London) 240: 475–477, 1972.

    Article  CAS  Google Scholar 

  63. Roth S, White D: Intercellular contact and cell surface galactosyl transferase activity. Proc Nat Acad Sei USA 69: 485–489, 1972.

    Article  CAS  Google Scholar 

  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. Salomon DS, Sherman MI: Implantation and invasiveness of mouse blastocysts on uterine monolayers. Exp Cell Res 90: 261–268, 1975.

    Article  PubMed  CAS  Google Scholar 

  66. Sartor P: Cell proliferation and decidual morphogenesis. Prog reprod Biol 7: 115–124, 1980.

    Google Scholar 

  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. Schlafke S, Enders AC: Cellular basis of interaction between tropho-blast and uterus at implantation. Biol Reprod 12: 41–65, 1975.

    Article  PubMed  CAS  Google Scholar 

  69. Schmidt IG: Proliferation in the genital tract of the normal mature guinea pig treated with colchicine. Am J Anat 73: 59–80, 1980.

    Article  Google Scholar 

  70. Sellens MH, Sherman MI: Effects of culture conditions on the developmental programmes of mouse blastocysts. J Embryol exp Morph 56: 1–22, 1980.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  72. Shelesnyak MC: Decidualization: The decidua and the deciduoma. Perspect Biol Med 5: 503–518, 1962.

    PubMed  CAS  Google Scholar 

  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. 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. Steer, HW: Implantation of the rabbit blastocyst: The adhesive phase of implantation. J Anat 109: 215–228, 1971.

    PubMed  CAS  Google Scholar 

  76. Surani MAH: Radiolabeled rat uterine luminal proteins and’ their regulation by estradiol and progesterone. J Reprod Fertil 50: 289–296, 1977.

    Article  PubMed  CAS  Google Scholar 

  77. Surani MAH: Cellular and molecular approaches to blastocyst uterine interactions at implantation. Devel in Mammals 1: 245–305, 1977.

    CAS  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  83. Wimsatt Wa: Some comparative aspects of implantation. Biol Reprod 12: 1–40, 1975.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy School of Medicine, Southern Illinois University, 62901, Carbondale, IL, USA

    Daniel J. Chávez

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  1. Daniel J. Chávez
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Editors and Affiliations

  1. Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, Colorado, USA

    Jonathan Van Blerkom Ph.D.

  2. Department of Anatomy, Faculty of Medicine, University of Rome, Viale R. Elena 289, 00161, Rome, Italy

    Pietro M. Motta M.D., Ph. D.

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

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Chávez, D.J. (1984). Cellular aspects of implantation. In: Van Blerkom, J., Motta, P.M. (eds) Ultrastructure of Reproduction. Electron Microscopy in Biology and Medicine, vol 2. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-3867-3_20

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  • DOI: https://doi.org/10.1007/978-1-4613-3867-3_20

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  • Print ISBN: 978-1-4613-3869-7

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