Advertisement

The Interaction of Trophoblast with Endometrial Stroma

  • John D. Aplin
  • Stanley R. Glasser
Part of the Reproductive Biology book series (RBIO)

Abstract

Implantation involves initial interaction between the embryo and uterine epithelium. Where placentation is chorio-epithelial, this relationship continues throughout gestation. In other cases in which invasion occurs, the embryo interacts with mesenchymal elements of the uterus. In species showing interstitial implantation, the embryo-stromal inter-relationship is much more long-lived than the embryo-epithelial interaction and arguably more important in the success of the pregnancy since it is the means by which the embryo gains access to nutrients supplied through the maternal blood stream (Mossman, 1987). The intention of this short article is not to review decidualisation or placentation, but to comment on model systems that may offer promise for an improved understanding of morphogenesis in the trophoblastic interaction with maternal stroma in rodent and primate.

Keywords

Decidual Cell Trophoblast Invasion Extravillous Trophoblast Human Trophoblast Decidual Tissue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aplin, J.D., and Foden, L.J., 1985, Defective adhesion to extracellular matrix leads to altered social behaviour in cultured fibroblasts, J. Cell Sci. 76:199.PubMedGoogle Scholar
  2. Aplin, J.D. Charlton, A.K., and Ayad, S., 1988, An innnunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy, Cell Tissue Res. 253:235.CrossRefGoogle Scholar
  3. Aplin, J.D., 1989, Cellular biochemistry of the endometrium, in: “Biology of the Uterus,” R.M. Wynn, W.P. Jollie, eds., Plenum Press, New York.Google Scholar
  4. Aplin, J.D., and Jones, C.J.P., 1989, Extracellular matrix in endometrium and decidua, in: “Placenta as a Model and Source,” O. Genbacev, A. Klopper, R. Beaconsfield eds., Plenum Press, New York.Google Scholar
  5. Aplin, J.D., and Charlton, A.K., 1990, The role of matrix macromolecules in te invasion of deciua by trophoblast: model studies using BeWo cells, in: “Trophoblast Invasion and Endometrial Receptivity”, H.-W. Denker, J.D. Aplin, eds. Trophoblast Research vol. 4, pp 139–158, Plenum Medical, New York.CrossRefGoogle Scholar
  6. Aplin, J.D., 1991, Implantation, trophoblast differentiation and haemochorial placentation: mechanistic evidence in vivo and in vitro, J. Cell Sci. 99:681.PubMedGoogle Scholar
  7. Aplin, J.D., Sattar, A., and Mould, A.P., 1992, Variant choriocarcinoma (BeWo) cells with differing adhesion and migration to fibronectin display conserved patterns of integrin expression, J. Cell Sci. 103:435.PubMedGoogle Scholar
  8. Aplin, J.D., 1993 Expression of integrin α6β4 in human trophoblast and its loss from extravillous cells, Placenta, 14:203.PubMedCrossRefGoogle Scholar
  9. Aplin, J.D., Sattar, A., and Vicovac, L., 1993, Cell interactions in trophoblast invasion, Serono symposium, in press.Google Scholar
  10. Armant, D.R., Kaplan, H.A., and Lennarz, W.I., 1986, Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts, Dev. Biol. 116:519.PubMedCrossRefGoogle Scholar
  11. Autio-Harmainen, H., Hurskainen, T., Niskasaari, K., Hoyhtya, M., and Tryggvason, K., 1992, Simultaneous expression of 70kDa type IV collagenase and type IV collagen α1(IV) chain genes by cells of early human placenta and gestational endometrium, Lab. Invest. 67:191.PubMedGoogle Scholar
  12. Babiarz, B.S., Romagnano, L.C., and Kurilla, G.M., 1992, Interaction of mouse ectoplacental cone trophoblast and uterine decidua in vitro, In Vitro Cell Dev. Biol. 28A:500.PubMedCrossRefGoogle Scholar
  13. Behrendtsen, O., Alexander, C.M., and Werb, Z., 1992, Metalloproteinases mediate extracellular matrix degradation by cells from mouse blastocyst outgrowths. Development, 114: 447.PubMedGoogle Scholar
  14. Bell, S.C., 1983, Decidualisation: regional differentiation and associated function, in: “Oxford Reviews of Reproductive Biology”, 5:220.Google Scholar
  15. Bell, S.C., 1988, Synthesis and secretion of proteins by the endometrium and decidua. in:“Implantation. Biological and Clinical Aspects”, M. Chapman, G. Gruzinskas and T. Chard, eds., Springer-Verlag, London.Google Scholar
  16. Bell, S.C., 1989 Decidualisation and IGF-BP: implications for its role in stromal cell differentiation and the decidual cell in haemochorial placentation. Human Reprod. 4:125.Google Scholar
  17. Benirschke, K., and Kaufman, P., 1990, Pathology of the Human Placenta (2nd ed.) Springer-Verlag, New York.Google Scholar
  18. Bevilacqua, E.M.A.F., Faria, M.R., and Abrahamsohn, P.A., 1991, Growth of mouse ectoplacental cone cells in subcutaneous tissues. Development of placental-like cells, Am. J. Anat. 192:382.PubMedCrossRefGoogle Scholar
  19. Bischof, P., Friedli, E., Martelli, M., and Campana, A., 1991, Expression of extracellular matrix-degrading metalloproteinases by cultured human cytotrophoblast cells: effects of cell adhesion and immunopurification. Am. J. Obstet. Gynecol. 165:1791.PubMedGoogle Scholar
  20. Blankenship, T.N., Enders, A.C., and King, B.F., 1993, Trophoblastic invasion and the development of uteroplacental arteries in the macaque, Cell Tissue Res. 272:227.PubMedCrossRefGoogle Scholar
  21. Brown, J.J.G., and Papaioannou, V.E., 1992, Ontogeny of hyaluronan expression during preimplantation differentiation of the mouse endometrium. Differentiation 52:61.PubMedCrossRefGoogle Scholar
  22. Burrows, T.D., King, A., and Loke, Y.W., 1993, Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin, Human Reprod. 8:475.Google Scholar
  23. Carson, D.D., Tang, J.-P., and Gay, S., 1988, Collagens support embryo attachment and outgrowth in vitro: effects of the RGD sequence. Dev. Biol. 127:368.PubMedCrossRefGoogle Scholar
  24. Carson, D.D., Julian, J., and Jacobs, A.L., 1992, Uterine stromal cell chondroitin sulphate proteoglycans bind to collagen type I and inhibit outgrowth in vitro, Dev. Biol. 149:307.PubMedCrossRefGoogle Scholar
  25. Cowell, T.P., 1969, Implantation and development of mouse eggs transferred to the uteri of non-progestational mice. J. Reprod. Fert. 19:239.CrossRefGoogle Scholar
  26. Damsky, C.H., Fitzgerald, M.L, and Fisher, S.J., 1992, Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotophoblast differentiation along the invasive pathway in vivo, J. Clin. Invest. 89:210.PubMedCrossRefGoogle Scholar
  27. Davies, J., and Glasser, S.R., 1967, Histological and fine structural observations on the placenta of the rat. Acta Anat. 69:542.CrossRefGoogle Scholar
  28. De Feo, V.J., 1967, Decidualisation, in: “Cellular Biology of the Uterus”, R.M. Wynn, ed. North-Holland, Amsterdam.Google Scholar
  29. Enders, A.C., 1991, Current topic: structural responses of the primate endometrium to implantation, Placenta 12:309.PubMedCrossRefGoogle Scholar
  30. Enders, A.C., and King, B.F., 1991, Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon, Am. J. Anat. 192:329.PubMedCrossRefGoogle Scholar
  31. Faber, M., Wewer, U.M., Berthelsen, J.G., Liotta, L.A., and Albrechtsen, R., 1986, Laminin production by human endometrial stromal cells relates to the cyclic and pathological state of the endometrium, Am. J. Pathol. 124:384.PubMedGoogle Scholar
  32. Farrar, J.D., and Carson, D.D., 1992, Differential temporal and spatial expression of mRNA encoding extracellular matrix components in decidua during the peri-implantation period, Biol. Reprod. 46:1095.PubMedCrossRefGoogle Scholar
  33. Feinberg, R.F., Kao, L.-C., Haimowitz, J.E., Queenan, J.T., Wun, T-C., Strauss, J.F., and Kliman, H.J., 1989, Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts, Lab. Invest. 61:20.PubMedGoogle Scholar
  34. Feinberg, R.F., Kliman, H.J., and Lockwood, C.J., 1991, Is oncofetal fibronectin a trophoblast glue for human implantation? Am. J. Pathol. 138:537.PubMedGoogle Scholar
  35. Fernandez, P.L., Merino, M.J., Nogales, F.F., Charonis, A.S., Stetler-Stevenson, W., and Liotta, L., 1992, Immunohistochemical profile of basement membrane proteins and 72kDa type IV collagenase in the implantation placental site, Lab. Invest. 66:572.PubMedGoogle Scholar
  36. Fernandez-Shaw, S., Shorter, S.C., Naish, C.E., Barlow, D.H., and Starkey, P.M., 1992, Isolation and purification of human endometrial stromal and glandular cells using immunomagnetic microspheres, Human Reprod. 7:156.Google Scholar
  37. Finn, C.A., and Porter, D.G., 1975, “The Uterus”, Elek Science, London.Google Scholar
  38. Fisher, S.J., Leitch, M.S., Kantor, M.S., Basbaum, C.B., and Kramer, R.H., 1985, Degradation of extracellular matrix by the trophoblastic cells of first-trimester human placentas, J. Cell. Biochem. 27:31.PubMedCrossRefGoogle Scholar
  39. Fisher, S.J., Cui, T.-y., Zhang, L., Hartman, L., Grahl, K., Guo-Yang, Z., Tarpey, J., and Damsky, C.H., 1989, Adhesive and degradative properties of human placental cytotrophoblast cells in vitro, J. Cell Biol. 109:891.PubMedCrossRefGoogle Scholar
  40. Genbacev, O., Sshubach, S., and Miller, R.K., 1992, Villous culture of first trimester human placenta — model to study extravillous trophoblast differentiation, Placenta 13:439.PubMedCrossRefGoogle Scholar
  41. Glass, R.H., Aggeler, J., Spindle, A.I., Pederson, R.A., and Werb, Z., 1983, Degradation of extracellular matrix by mouse trophoblast outgrowths: a model for implantation. J. Cell Biol. 96:1108.PubMedCrossRefGoogle Scholar
  42. Glasser, S.R., 1990, Biochemical and structural changes in uterine endometrial cell types following natural or artificial deciduogenic stimuli, Trophoblast Res. 4:377.Google Scholar
  43. Glasser, S.R., and Julian, J., 1986, Intermediate filament protein as a marker of uterine stromal cell decidualisation, Biol. Reprod. 35:463.PubMedCrossRefGoogle Scholar
  44. Glasser, S.R., Lampelo, S., Munir, M.I. and Julian, J.A., 1987, Expression of desmin, laminin and fibronectin during in situ differentiation (decidualisation) of rat uterine stromal cells, Differentiation 35:132.PubMedCrossRefGoogle Scholar
  45. Graham, C.H., McCrae, K.R., and Lala, P.K., 1993, Molecular mechanisms controlling trophoblast invasion of the uterus, Trophoblast Res. 7:237.Google Scholar
  46. Gu, Y., Jayatilak, P.G., Parmer, T.G., Gauldie, J., Fey, G.H., and Gibori, G., 1992, α2-macroglobulin expression in the mesometrial decidua and its regulation by decidual luteotropin and prolactin, Endocrinology 131:1321.PubMedCrossRefGoogle Scholar
  47. Haimovici, F, and Anderson, D.J., 1993, Effects of growth factors and growth factor-extracellular matrix interactions on mouse trophoblast outgrowth in vitro. Biol. Reprod. 49:124.PubMedCrossRefGoogle Scholar
  48. He, C., Wilhelm, S.M., Pentland, A.P., Marker, B.L., Grant, G.A., Eisen, A.Z., and Goldberg, G.I., 1989, Tissue cooperation in a proteolytic cascade activating human interstitial collagenase, Proc. Nat. Acad. Sci. USA 86: 2632.PubMedCrossRefGoogle Scholar
  49. Hees, H., Moll, W., Wrobel, K.-H., and Hees, I., 1987, Pregnancy-induced structural changes and trophoblastic invasion in the segmental mesometrial arteries of the guinea pig, Placenta 8:609.PubMedCrossRefGoogle Scholar
  50. Hertig, A.T., Rock, J., and Adams, J., 1956, A description of 34 human ova within the first 17 days of development, Am. J. Anat. 98:435.PubMedCrossRefGoogle Scholar
  51. Herz, J., Clouthier, D.E., and Hammer, R.E., 1992, LDL receptor-related protein internalises and degrades uPA-PAI-1 complexes and is essential for embryo implantation, Cell 71:411.PubMedCrossRefGoogle Scholar
  52. Irwin, J.C., Utian, W.H., and Eckert, R.L., 1991, Sex steroids and growth factors differentially regulate the growth and differentiation of cultured human endometrial stromal cells, Endocrinology 129:2385.PubMedCrossRefGoogle Scholar
  53. Jayatilak, P.G., Puryear, T.K., Herz, Z., Fazleabas, A., and Gibori, G., 1989, Protein secretion by mesometrial and antimesometrial rat decidual tissue: evidence for differential gene expression, Endocrinology 125:659.PubMedCrossRefGoogle Scholar
  54. Jones, C.J.P., Aplin, J.D., Mulholland, J., and Glasser, R., 1993, Patterns of sialylation in differentiating rat decidual cells as revealed by lectin histochemistry, J. Reprod. Fert., in press.Google Scholar
  55. Kisalus, L., and Herr, J.C., 1988, Immunocytochemical localisation of heparan sulphate proteoglycan in human decidual cell secretory bodies and placental fibrinoid. Biol. Reprod. 39:419.PubMedCrossRefGoogle Scholar
  56. Kirby, D.R.S., 1963a, The development of mouse blastocysts tranferred to the spleen, J. Reprod. Fert. 5:1.CrossRefGoogle Scholar
  57. Kirby, D.R.S., 1963b, The development of the mouse blastocyst transferred to the cryptorchid and scrotal testis, J. Anat. 97:119.PubMedGoogle Scholar
  58. Kliman, H.J., Feinberg, R.F., and Haimowitz, J.E., 1990, Human trophoblast-endometrial interactions in an in vitro suspension culture system, Placenta 11:349.PubMedCrossRefGoogle Scholar
  59. Kliman, H.J., and Feinberg, R.F., 1992, Differentiation of the trophoblast, in: “The First Twelve Weeks of Pregnancy”, E.R. Barnea, J. Hustin, and E. Jauniaux, eds., Springer-Verlag, Berlin.Google Scholar
  60. Korhonen, M., Ylanne, J., Laitinen, L., Cooper, H.M., Quaranta, V., and Virtanen, I., 1991, Distribution of the α16 integrin subunits in human developing and term placenta, Lab. Invest. 65:347.PubMedGoogle Scholar
  61. 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.Google Scholar
  62. Lala, P.K., and Graham, C.H., 1990, Mechanisms of trophoblast invasiveness and their control: the role of proteases and protease inhibitors, Cancer Metast. Rev. 9:369.CrossRefGoogle Scholar
  63. Librach, C.L., Werb, Z., Fitzgerald, M.L., Chiu, K., Corwin, N.M., Esteves, R.A., Grobelny, D., Galardy, R., Damsky, C.H., and Fisher, S.J., 1991, 92-kD type IV collagenase mediates invasion of human cytotrophoblasts, J. Cell Biol. 113:437.PubMedCrossRefGoogle Scholar
  64. Logan, S.K., Fisher, S.J., and Damsky, C.H., 1992, Human placental cells with temperature-sensitive simian virus 40 are immortalised and mimic the phenotype of invasive cytotrophoblasts at both permissive and nonpermissive temperatures, Cancer Res. 52:6001.PubMedGoogle Scholar
  65. Mani, S.K., Julian, J., Lampelo, S., and Glasser, S.R., 1992, Initiation and maintenance of in vitro decidualisation are independent of hormonla sensitization in vivo, Biol. Reprod. 47:785.PubMedCrossRefGoogle Scholar
  66. Mareel, M.M.K., 1979, Is invasiveness in vitro characteristic of malignant cells? Cell Biol. Int. Rep. 3:627.PubMedCrossRefGoogle Scholar
  67. Martin, O., and Aarias, F., 1982, Plasminogen activator production by trophoblast cells in vitro: effect of steroid hormones and protein synthesis inhibitors, Am. J. Obstet. Gynecol. 142:402.PubMedGoogle Scholar
  68. Mitchell, M.D., Trautmann, M.S., and Dudley, D.J., 1993, Cytokine networking in the placenta, Placenta 14:249.PubMedCrossRefGoogle Scholar
  69. Moll, U.M., and Lane, B.L., 1990, Proteolytic activity of first trimester human placenta: localization of interstitial collagenase in villous and extravillous trophoblast, Histochemistry 94:555.PubMedCrossRefGoogle Scholar
  70. Mossman, H.W., 1987, Vertebrate Fetal Membranes. MacMillan, London.Google Scholar
  71. Mulholland, J., Aplin, J.D., Ayad, S., Hong, S., and Glasser S.R., 1992, Loss of type VI collagen from rat endometrium during decidualisation, Biol. Reprod. 46:1136.PubMedCrossRefGoogle Scholar
  72. Myers, D.B., Clark, D.E., and Hurst, P.R., 1990, Decreased collagen concentration in rat uterine implantation sites compared with non-implantation tissue at days 6–11 of pregnancy, Reprod. Fert. Dev. 2:607.CrossRefGoogle Scholar
  73. O’Shea, J.D., Kleinfeld, R.G., and Morrow, H.A., 1983, Ultrastructure of decidualisation in the pseudopregnant rat, Am. J. Anat. 166:271.PubMedCrossRefGoogle Scholar
  74. Parr, M.B., Tung, H.N., and Parr, E.L., 1986, The ultrastructure of the rat primary decidual zone, Am. J. Anat. 176:423.PubMedCrossRefGoogle Scholar
  75. Pijnenborg, R., 1990, Trophoblast invasion and placentation in the human: morphological aspects, in; Trophoblast Invasion and Endometrial Receptivity, H.-W. Denker and J.D. Aplin, eds, Trophoblast Research Vol. 4, pp 33–47, Plenum Medical, New York, London.CrossRefGoogle Scholar
  76. Pijnenborg, R., Dixon, G., Robertson, W.B., and Brosens, I., 1980, Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy, Placenta 1:3.PubMedCrossRefGoogle Scholar
  77. Pijnenborg, R., Robertson, W.B., Brosens, I., and Dixon, G. 1981, Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals, Placenta 2:71.PubMedCrossRefGoogle Scholar
  78. Puistola, U., Ronnberg, L. Martikainen, H., and Turpeenniemi-Hujanen, T. (1989) The human embryo produces basement membrane collagen (type IV collagen)-degrading protease activity, Human Reprod. 4:309.Google Scholar
  79. Randall, S., Buckley, C.H., and Fox, H., 1987, Placentation in the Fallopian tube, Int. J. Gynaecol. Pathol. 6:132.CrossRefGoogle Scholar
  80. Romagnano, L., and Babiarz, B., 1993, Mechanisms of murine trophoblast interaction with laminin, Biol. Reprod. 49:374.PubMedCrossRefGoogle Scholar
  81. Salamonsen, L.A., Nagase, H., and Wooley, D.E., 1991, Production of matrix metalloproteinase 3 (stromelysin) by cultured ovine endometrial cells, J. Cell Sci. 100:381.PubMedGoogle Scholar
  82. Samuel, C.A., and Perry, J.S., 1972, The ultrastructure of pig trophoblast transplanted to an ectopic site in the uterine wall, J. Anat. 113:139.PubMedGoogle Scholar
  83. 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.PubMedCrossRefGoogle Scholar
  84. Shelesnyak, M.C., 1986, A history of research on nidation, Ann. N.Y. Acad. Sci. 476:5.PubMedCrossRefGoogle Scholar
  85. Soares, M.J., Faria, T.N., Roby, K.F., and Deb, S., 1991, Pregnancy and the prolactin family of hormones: coordination of anterior pituitary, uterine and placental expression, Endocrine Rev. 12:402.CrossRefGoogle Scholar
  86. Starkey, P.M., 1993, The decidua and factors controlling placentation, in; “The Human Placenta”, C.W.G. Redman, I.L. Sargent, P.M. Starkey, eds, Blackwell Scientific Publications, Oxford.Google Scholar
  87. Starkey, P.M., Sargent, I.L., and Redman, C.W.G., 1988, Cell populations in human early pregnancy decidua: characterisation and isolation of large granular lymphocytes by flow cytometry, Immunology 65:129.PubMedGoogle Scholar
  88. Strickland, S., Reich, E., and Sherman, M.I., 1976, Plasminogen activator in early embryogenesis: enzyme production by trophoblast and parietal endoderm, Cell 9: 231.PubMedCrossRefGoogle Scholar
  89. Tabibzadeh, S., 1991, Human endometrium: an active site of cytokine production and action, Endocrine Rev. 12:272.CrossRefGoogle Scholar
  90. Thomas, T., 1993, Distribution of α2-macroglobulin and α1-acid glycoprotein mRNA show regional specialisation in rat decidua, Placenta 14:417.PubMedCrossRefGoogle Scholar
  91. Trinkaus, J.P., 1984, Cells into Organs: the Forces that Shape the Embryo, 2nd edition, Prentice-Hall, New York.Google Scholar
  92. Turpeenniemi-Hujanen, T., Ronnberg, L., Kauppila, A., and Puistola, U., 1992, Lamininin the human embryo implantation: analogy to invasion by malignant cells, Fertil Steril. 58:105.PubMedGoogle Scholar
  93. Vicovac, Lj., Papic, N., and Aplin, J.D., 1993, Tissue interactions in first trimester trophoblast-decidua cocultures, Trophoblast Res. 7:223.Google Scholar
  94. Vicovac, Lj., Jones, C.J.P., and Aplin, J.D., 1994, Trophoblast differentiation during anchoring villus formation in a coculture model of the human implantation site in vitro, Submitted.Google Scholar
  95. Wegmann, T.G., Lin, H., Guilbert, L., and Mossmann, T.R., 1993, Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunology Today 14:353.PubMedCrossRefGoogle Scholar
  96. Welsh, A.O., and Enders, A.C., 1985, Light and electron microscopic examination of mature decidual cells of the rat with emphasis on the antimesometrial decidua and its degeneration, Am. J. Anat. 172:1.PubMedCrossRefGoogle Scholar
  97. 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.PubMedCrossRefGoogle Scholar
  98. Welsh, A.O., and Enders, A.C., 1991, Chorioallantoic placenta formation in the rat: II. Angiogenesis and maternal blood circulation in the mesometrial region of the implantation chamber prior to placenta formation, Am. J. Anat. 192:347.PubMedCrossRefGoogle Scholar
  99. Wewer, U.M., Faber, M., Liotta, L.A., and Albrechtsen, R., 1985, Immunochemical and ultrastructural assessment of the nature of the pericellular basement membrane of human decidual cells, Lab. Invest. 53:624.PubMedGoogle Scholar
  100. Winterhager, E., Stutenkemper, R., Traub, O., Beyer, E., and Willecke, K., 1991, Expression of different connexin genes in rat uterus during decidualisation and at term, Eur. J. Cell Biol. 55:133.PubMedGoogle Scholar
  101. Wynn, R.M., 1974, Ultrastructural development of the human decidua, Am. J. Obstet. Gynecol. 118:652.PubMedGoogle Scholar
  102. Yagel, S., Parhar, R.S., Jeffrey, J.J., and Lala, P.K., 1988, Normal nonmetastatic human trophoblast cells share in vitro invasive properties of malignant cells, J. Cell Physiol. 136:455.PubMedCrossRefGoogle Scholar
  103. Yelian, F.D., Edgeworth, N.A., Dong, L.-J., Chung, A.E., and Armant, D.R., 1993, Recombinant entactin promotes mouse primary trophoblast cell adhesion and migration through the RGD recognition sequence, J. Cell Biol. 121:923.PubMedCrossRefGoogle Scholar
  104. Zorn, T.M.T., Bevilacqua, E.M.A.F., and Abrahamsohn, P.A., 1986, Collagen remodelling during decidualisation in the mouse, Cell Tissue Res. 244:443.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • John D. Aplin
    • 1
  • Stanley R. Glasser
    • 2
  1. 1.Department of Ob/Gyn and School of Biological SciencesUniversity of ManchesterUK
  2. 2.Department of Cell BiologyBaylor College of Medicine HoustonUSA

Personalised recommendations