Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T16:31:21.115Z Has data issue: false hasContentIssue false
  • English
  • Français

Trophoblast invasion

Published online by Cambridge University Press:  02 March 2009

R Pijnenborg
R Pijnenborg*
Affiliation:
UZ Gasthuisberg, Katholieke Universiteit Leuven, Leuven, Belgium
*
R Pijnenborg, Department of Obstetrics and Gynaecology, UZ Gasthuisberg, Katholieke Universiteit Leuven, B3000 Leuven, Belgium.
Get access Rights & Permissions [Opens in a new window]

Extract

The establishment of a pregnancy depends upon mechanisms of forming close contacts between embryonic/fetal and maternal tissues. The starting point is the attachment of the blastocyst to the uterine wall, and this critical step is followed by a series of different morphogenetic events leading to placentation. These processes depend on the invasive properties of extra-embryonic trophectoderm-derived cells that show their highest expression in species with haemochorial placentation, i.e. Insectivores, rodents, and primates including the human. In this review we will concentrate upon the human with occasional reference to other species.

Type
Articles
Information
Reproductive Medicine Review , Volume 3 , Issue 1 , March 1994 , pp. 53 - 73
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Billington, WD. The placenta and the tumour: variations on an immunological enigma. In: Beaconsfield, F, Villee, C eds. Placenta: a neglected experimental animal. Oxford: Pergamon Press, 1979: 267–83.CrossRefGoogle Scholar
2Psychoyos, A. Methods for studying changes in capillary permeability of the rat endometrium. In: Daniel, JC Jr ed. Methods in mammalian embryology. San Francisco: WH Freeman, 1971: 334–38.Google Scholar
3Hertig, AT. Human trophoblast. Springfield, IL: Charles C Thomas, 1968: 363.Google Scholar
4Heuser, CH, Streeter, GL. Development of the macaque embryo. Contrib Embryol 1941; 29: 15–55.Google Scholar
5Enders, AC, Hendrickx, AG, Schlafke, S. Implantation in the Rhesus monkey: initial penetration of endometrium. Am J Anat 1983; 176: 275–98.CrossRefGoogle Scholar
6Hamilton, WJ, Boyd, JD. Development of the human placenta in the first three months of gestation. J Anat 1960; 94: 297–328.Google ScholarPubMed
7Boyd, JD, Hamilton, WJ. Development and structure of the human placenta from the end of the 3rd month of gestation. J Obstet Gynaec Br Cwlth 1967; 74: 161–226.CrossRefGoogle ScholarPubMed
8Pijnenborg, R, Dixon, G, Robertson, WB, Brosens, I. Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy. Placenta 1980; 1: 3–19.CrossRefGoogle ScholarPubMed
9Pijnenborg, R, Bland, JM, Robertson, WB, Dixon, G, Brosens, I. The pattern of interstitial trophoblastic invasion of the myometrium in early human pregnancy. Placenta 1981; 2: 303–16.CrossRefGoogle ScholarPubMed
10Pijnenborg, R, Bland, JM, Robertson, WB, Brosens, I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta 1983; 4: 397–414.CrossRefGoogle ScholarPubMed
11Khong, TY, Chambers, HM. Alternative method of sampling placentas for the assessment of Uteroplacental vasculature. J Clin Pathol 1992; 45: 925–27.CrossRefGoogle ScholarPubMed
12Pijnenborg, R, Robertson, WB, Brosens, I. Trophoblast invasion and the formation of the basal plate in the human placenta. In: Kaufmann, P, King, BF eds. Structural and functional organization of the placenta. Basel: Karger, 1982: 69–73.Google Scholar
13Labarrere, CA, Faulk, WP. Diabetic placentae: studies of the battlefield after the war. Diabetes/Metabolism Reviews 1991; 7: 253–63.CrossRefGoogle ScholarPubMed
14Robertson, WB, Brosens, I, Pijnenborg, R, De Wolf, F. The making of the placental bed. Eur J Obstet Gynec Reprod Biol 1984; 18: 255–66.CrossRefGoogle ScholarPubMed
15Robertson, WB, Khong, TY, Brosens, I, De Wolf, F, Sheppard, BL, Bonnar, J. The placental bed biopsy: review from three European centers. Am J Obstet Gynecol 1986; 155: 401–12.CrossRefGoogle ScholarPubMed
16Meekins, JW, Pijnenborg, R, Hanssens, M, McFadyen, IR, Van Assche, FA. Immunohistochemical identification of placental bed biopsies and the implications for the inclusion of specimens when studying the spiral artery response to pregnancy. Hypertens Pregnancy 1994 (in press).CrossRefGoogle Scholar
17Robertson, WB, Manning, PJ. Elastic tissue in uterine blood vessels. J Path 1974; 112: 237–43.CrossRefGoogle ScholarPubMed
18Loke, YW, Butterworth, BH. Heterogeneity of human trophoblast populations. In: Gill, TJ, Wegmann, TG eds. Immunoregulation and fetal survival. New York: Oxford University Press, 1987: 197–209.Google Scholar
19Wells, M, Bulmer, JN. The human placental bed: histology, immunohistochemistry and pathology. Histopathology 1988; 13: 483–98.CrossRefGoogle ScholarPubMed
20Anderson, DJ, Johnson, PM, Alexander, NJ, Jones, WR, Griffin, PD. Monoclonal antibodies to human trophoblast and sperm antigens. J Reprod Immunol 1987; 10: 231–57.CrossRefGoogle ScholarPubMed
21Sasagawa, M, Watanabe, S, Ohmomo, Y, Honma, S, Kanazawa, K, Takeuchi, S. Reactivity of two monoclonal antibodies (Troma 1 and CAM 5.2) on human tissue sections: analysis of their usefulness as a histological trophoblast marker in normal pregnancy and trophoblastic disease. Int J Gynecol Pathol 1986; 5: 345–56.CrossRefGoogle ScholarPubMed
22Daya, D, Sabet, L. The use of cytokeratin as a sensitive and reliable marker for trophoblastic tissue. Am J Clin Pathol 1991; 95: 137–41.CrossRefGoogle ScholarPubMed
23Khong, TY, Lane, EB, Robertson, WB. An immunocytochemical study of fetal cells at the maternal-placental interface using monoclonal antibodies to keratins, vimentin and desmin. Cell Tissue Res 1986; 246: 189–95.CrossRefGoogle ScholarPubMed
24Bulmer, JN, Wells, M, Bhabra, K, Johnson, PM. Immunohistological characterization of endometrial gland epithelium and extravillous fetal trophoblast in third-trimester human placental bed tissues. Br J Obstet Gynaec 1986; 93: 823–32.CrossRefGoogle ScholarPubMed
25Robertson, WB, Warner, B. The ultrastructure of the human placental bed. J Path 1974; 112: 203–11.CrossRefGoogle ScholarPubMed
26Sheppard, BL, Bonnar, J. The ultrastructure of the arterial supply of the human placenta in early and late pregnancy. J Obstet Gynaec Br Cwlth 1974; 81: 497–511.CrossRefGoogle ScholarPubMed
27Sheppard, BL, Bonnar, J.The ultrastructure of the arterial supply of the human placenta in pregnancy complicated by fetal growth retardation. Br J Obstet Gynaecol 1976; 83: 948–59.CrossRefGoogle ScholarPubMed
28Sheppard, BL, Bonnar, J.An ultrastructural study of Uteroplacental spiral arteries in hypertensive and normotensive pregnancy and fetal growth retardation. Br J Obstet Gynaecol 1981; 88: 695–705.CrossRefGoogle ScholarPubMed
29De Wolf, F, Brosens, I, Robertson, WB. Ultrastructure of Uteroplacental arteries. Contr Gynec Obstet 1982; 9: 86–99.CrossRefGoogle ScholarPubMed
30De Wolf, F, De Wolf-Peeters, C, Brosens, I. Ultrastructure of the spiral arteries in the human placental bed at the end of normal pregnancy. Am J Obstet Gynecol 1973; 117: 833–48.CrossRefGoogle ScholarPubMed
31De Wolf, F, De Wolf-Peeters, C, Brosens, I, Robertson, WB. The human placental bed: electron microscopic study of trophoblastic invasion of spiral arteries. Am J Obstet Gynecol 1980; 137: 58–70.CrossRefGoogle ScholarPubMed
32Hoshina, M, Boothby, M, Boime, I. Cytological localization of chorionic gonadotropin α and placental lactogen mRNAs during development of the human placenta. J Cell Biol 1982; 93: 190–98.CrossRefGoogle ScholarPubMed
33Chen, HL, Yang, Y, Hu, XL, Yelavarthi, KK, Fishback, JL, Hunt, JS. Tumour necrosis factor alpha mRNA and protein are present in human placental and uterine cells at early and late stages of gestation. Am J Pathol 1991; 139: 327–35.Google ScholarPubMed
34Kanzaki, H, Yui, J, Iwai, M et al. The expression and localization of mRNA for colony-stimulating factor (CSF)-1 in human term placenta. Hum Reprod 1992; 7: 563–67.CrossRefGoogle ScholarPubMed
35Enders, AC, Chavez, DJ, Schlafke, S. Comparisons of implantation in utero and in vivo. In: Glasser, SR, Bullock, DW eds. Cellular and molecular aspects of implantation. New York: Plenum Press, 1981: 365–82.CrossRefGoogle Scholar
36Wilson, IB, Jenkinson, EJ. Blastocyst differentiation in vitro. J Reprod Fertil 1974; 39: 243–49.CrossRefGoogle ScholarPubMed
37Hsu, YC. Differentiation in vitro of mouse embryos beyond the implantation stage. Nature 1972; 239: 200–202.CrossRefGoogle ScholarPubMed
38Glasser, SR, Julian, JA, Decker, GL, Tang, J-Y, Carson, DD. Development of morphological and functional polarity in primary cultures of immature rat uterine epithelial cells. J Cell Biol 1988; 107: 2409–423.CrossRefGoogle ScholarPubMed
39Fishel, S, Edwards, RG, Evans, CJ. Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro. Science 1984; 223: 816–18.CrossRefGoogle ScholarPubMed
40Lindenberg, S, Hyttel, P, Sjogren, A, Greve, T. A comparative study of attachment of human, bovine and mouse blastocysts to uterine epithelial monolayer. Human Reproduction 1989; 4: 446–56.CrossRefGoogle ScholarPubMed
41New, DAT. Studies on mammalian fetuses in vitro during the period of organogenesis. In: Austin, CR ed. The mammalian fetus in vitro. London: Chapman and Hall, 1973: 15–65.CrossRefGoogle Scholar
42Ungar, L, Csonka, E, Kazy, Z, Siklos, P, Hercz, P. The use of pregnancy serum to obtain trophoblastic cell cultures. Placenta 1987; 8: 639–46.CrossRefGoogle ScholarPubMed
43Bambra, CS. Characterization of dispersed baboon placental cells grown in vitro using monoclonal antibodies. J Reprod Immunol 1989; 16: 217–24.CrossRefGoogle ScholarPubMed
44Genbacev, O, Schubach, SA, Miller, RK. Villous culture of first trimester human placenta – Model to study extravillous trophoblast differentiation. Placenta 1992; 13: 439–61.CrossRefGoogle Scholar
45Loke, YW, Gardner, L, Burland, K, King, A. Laminin in human trophoblast-decidua interaction. Hum Reprod 1989; 4: 457–63.CrossRefGoogle ScholarPubMed
46Loke, YW, Gardner, L, Grabowska, A. Isolation of human extravillous trophoblast cells by attachment to laminin-coated magnetic beads. Placenta 1989; 10: 407–15.CrossRefGoogle ScholarPubMed
47Loke, YW, Butterworth, BH, Margetts, JJ, Burland, K. Identification of cytotrophoblast colonies in cultures of human placental cells using monoclonal antibodies. Placenta 1986; 7: 221–31.CrossRefGoogle ScholarPubMed
48Butterworth, BH, Loke, YW. Immunocytochemical identification of cytotrophoblast from other mononuclear cell populations isolated from first-trimester human chorionic villi. J Cell Sci 1985; 76: 189–97.CrossRefGoogle ScholarPubMed
49Loke, YW, Bulmer, JN, Grivaux, C et al. Evaluation of a monoclonal antibody, BC-1, which identifies an antigen expressed on the surface membrane of human extravillous trophoblast. Am J Reprod Immun 1992; 27: 77–81.CrossRefGoogle ScholarPubMed
50Cotte, G, Easty, GC, Neville, AM, Monaghan, P. Preparation of highly purified cytotrophoblast from human placenta with subsequent modulation to form syncytiotrophoblast in monolayer cultures. In Vitro 1980; 16: 639–46.CrossRefGoogle ScholarPubMed
51Nelson, DM, Meister, RK, Ortman-Nabi, J, Sparks, S, Stevens, VC. Differentiation and secretory activities of cultured human placental cytotrophoblast. Placenta 1986; 7: 1–16.CrossRefGoogle ScholarPubMed
52Kliman, HJ, Nestler, JE, Sermasi, E, Sanger, JM, Strauss, JF III. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 1986; 118: 1567–82.CrossRefGoogle ScholarPubMed
53Feinberg, RF, Kao, LC, Haimowitz, JE et al. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. PAI-1 is an immunocytochemical marker of invading trophoblasts. Lab Invest 1989; 61: 20–25.Google ScholarPubMed
54Kliman, HJ, Feinberg, RF. Human trophoblast-extracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity. Proc Natl Acad Sci USA 1990; 87: 3057–61.CrossRefGoogle ScholarPubMed
55Kliman, HJ, Feinberg, RF, Haimowitz, JE. Human trophoblast-endometrial interactions in an in vitro suspension culture system. Placenta 1990; 11: 349–67.CrossRefGoogle Scholar
56Fisher, SJ, Cui, TY, Zhang, L et al. Adhesive and degradative properties of human placental cytotrophoblast cell. in vitro. J Cell Biol 1989; 109: 891–902.CrossRefGoogle Scholar
57Fisher, SJ, Leiten, MS, Kantor, MS, Basbaum, CB, Kramer, RH. Degradation of extracellular matrix by the trophoblastic cells of first-trimester human placentas. J Cell Biochem 1985; 27: 31–41.CrossRefGoogle ScholarPubMed
58Librach, CL, Werb, Z, Fitzgerald, ML et al. 92-kD Type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol 1991; 113: 437–49.CrossRefGoogle ScholarPubMed
59Graham, CH, Lysiak, JJ, McCrae, KR, Lala, PK. Localization of transforming growth factor β (TGF β) at the human fetomaternal interface: role on trophoblast growth and differentiation. Biol Reprod 1992; 46: 561–72.CrossRefGoogle Scholar
60Graham, CH, Lala, PK. Mechanisms of placental invasion of the uterus and their control. Biochem Cell Biol 1992; 70: 867–74.CrossRefGoogle ScholarPubMed
61Schlafke, S, Enders, AC. Cellular basis of interaction between trophoblast and uterus at implantation. Biol Reprod 1975; 12: 41–65.CrossRefGoogle ScholarPubMed
62Enders, AC, Welsh, AO, Schlafke, S. Implantation in the Rhesus monkey: endometrial responses. Am J Anat 1985; 173: 147–69.CrossRefGoogle ScholarPubMed
63Enders, AC. Trophoblast differentiation during the transition from trophoblastic plate to lacunar stage of implantation in the Rhesus monkey and human. Am J Anat 1989; 186: 85–98.CrossRefGoogle ScholarPubMed
64Knoth, M, Larsen, JF. Ultrastructure of a human implantation site. Acta Obstet Gynec Scand 1972; 51: 385–93.CrossRefGoogle ScholarPubMed
65Boyd, JD, Hamilton, WJ. The human placenta. Cambridge: W Heffer & Sons, 1970: 365.CrossRefGoogle Scholar
66Larsen, JF, Knoth, M. Ultrastructure of the anchoring villi and trophoblastic shell in the second week of placentation. Acta Obstet Gynec Scand 1971; 50: 117–28.CrossRefGoogle ScholarPubMed
67Blankenship, TN, Enders, AC, King, BF. Distribution of laminin, type IV collagen, and fibronectin in the cell columns and trophoblastic shell of early macaque placentas. Cell Tissue Res 1992; 270: 241–48.CrossRefGoogle ScholarPubMed
68Earl, U, Estlin, C, Bulmer, JN. Fibronectin and laminin in the early human placenta. Placenta 1990; 11: 223–31.CrossRefGoogle ScholarPubMed
69Korhonen, M, Ylinne, J, Laitinen, L, Cooper, HM, Quaranta, V, Virtanen, I. Distribution of the α1—α6 integrin subunits in human developing and term placenta. Lab Invest 1991; 65: 347–56.Google Scholar
70Damsky, CH, Fitzgerald, ML, Fisher, SJ. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway in vivo. J Clin Invest 1992; 89: 210–22.CrossRefGoogle ScholarPubMed
71Aplin, JD, Charlton, AK, Ayad, S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res 1988; 253: 231–40.CrossRefGoogle ScholarPubMed
72Boyd, JD, Hamilton, WJ. The giant cells of the pregnant human uterus. J Obstet Gynaec Br Empire 1960; 67: 208–18.CrossRefGoogle ScholarPubMed
73Kurman, RJ, Main, CS, Chen, HC. Intermediate trophoblast: a distinctive form of trophoblast with specific morphological, biochemical and functional features. Placenta 1984; 5: 349–70.CrossRefGoogle ScholarPubMed
74Feinberg, RF, Kao, LC, Haimowitz, JE et al. Plasminogen activator inhibitor types 1 and 2 in human trophoblasts. Lab Invest 1989; 61: 20–26.Google ScholarPubMed
75Hofmann, GE, Drews, MR, Scott, RT Jr, Navot, D, Heller, D, Deligdisch, L. Epidermal growth factor and its receptor in human implantation trophoblast: immunohistochemical evidence for autocrine/paracrine function. J Clin End Metab 1992; 74: 981–88.Google ScholarPubMed
76Bulmer, JN, Thrower, S, Wells, M. Expression of epidermal growth factor receptor and transferrin receptor by human trophoblast populations. Am J Reprod Immunol 1989; 21: 87–93.CrossRefGoogle ScholarPubMed
77Enders, AC, King, BF. Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon. Am J Anat 1991; 192: 329–46.CrossRefGoogle ScholarPubMed
78Hustin, J, Schaaps, JP. Echocardiographic and anatomic studies of the maternotrophoblastic border during the first trimester of pregnancy. Am J Obstet Gynecol 1987; 157: 162–68.CrossRefGoogle Scholar
79Hustin, J, Jauniaux, E, Schaaps, JP. Histological study of the materno-embryonic interface in spontaneous abortion. Placenta 1990; 11: 477–86.CrossRefGoogle ScholarPubMed
80Harris, JWS, Ramsey, EM. The morphology of human uteroplacental vasculature. Contrib Embryol 1966; 38: 43–58.Google Scholar
81De Wolf, F, De Wolf-Peeters, C, Brosens, I, Robertson, WB. The human placental bed: electron microscopic study of trophoblastic invasion of spiral arteries. Am J Obstet Gynecol 1980; 137: 58–70.CrossRefGoogle ScholarPubMed
82Pijnenborg, R, Vercruysse, L, Ballegeer, V et al. The distribution of fibronectin in the placental bed in normotensive and hypertensive human pregnancies. Trophoblast Research 1992; 6: 343–50.Google Scholar
83Redman, CWG, McMichael, AJ, Stirrat, GM, Sunderland, CA. Class I major histocompatibility complex antigens on human extravillous trophoblast. Immunology 1984; 52: 457–68.Google Scholar
84Pijnenborg, R, Robertson, WB, Brosens, I, Dixon, G. Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 1981; 2: 71–92.CrossRefGoogle ScholarPubMed
85Ramsey, EM, Houston, ML, Harris, JWS. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am J Obstet Gynecol 1976; 124: 647–52.CrossRefGoogle ScholarPubMed
86Maruo, T, Matsuo, H, Murata, K, Mochizuki, M. Gestational age-dependent dual action of epidermal growth factor on human placenta early in gestation. J Clin Endocr Metab 1992; 75: 1362–67.Google ScholarPubMed
87Yagel, S, Casper, RF, Powell, W, Parhar, RS, Lala, PK. Characterization of pure human first-trimester cytotrophoblast cells in long term culture: growth pattern, markers, and hormone production. Am J Obstet Gynecol 1989; 160: 938–45.CrossRefGoogle ScholarPubMed
88Yagel, S, Lala, PK, Powell, WA, Casper, RF. Interleukin-1 stimulates human chorionic gonadotropin secretion by first trimester human trophoblast. J Clin Endocr Metab 1989; 68: 992–95.CrossRefGoogle ScholarPubMed
89Yagel, S, Parhar, RS, Lala, PK. Trophic effects of first trimester human trophoblasts and human chorionic gonadotropin on lymphocyte proliferation. Am J Obstet Gynecol 1989; 160: 946–53.CrossRefGoogle ScholarPubMed
90Yagel, S, Parhar, RS, Jeffrey, JJ, Lala, PK. Normal nonmetastatic human trophoblast cells share in vitro invasive properties of malignant cells. J Cell Physiol 1988; 136: 455–62.CrossRefGoogle ScholarPubMed
91Moll, UM, Lane, BL. Proteolytic activity of first trimester human placenta: localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 1990; 94: 555–60.CrossRefGoogle ScholarPubMed
92Contractor, SF, Routledge, A, Sooranna, SR. Identification and estimation of cell types in mixed primary cell cultures of early and term human placenta. Placenta 1984; 5: 41–54.CrossRefGoogle ScholarPubMed
93Vettenranta, K, Von Koskull, H, Heikinheimo, H, Raivio, KO. Cytoskeletal markers and specific protein production in cells cultured from human first and third trimester placentae. In Vitro Cell Dev Biol 1986; 22: 100–106.CrossRefGoogle ScholarPubMed
94Loke, YW, Burland, K. Human trophoblast cells cultured in modified medium and supported by extracellular matrix. Placenta 1988; 9: 173–82.CrossRefGoogle ScholarPubMed
95Yeger, H, Lines, LD, Wong, PY, Silver, MM. Enzymatic isolation of human trophoblast and culture on various substrates: comparison of first trimester with term trophoblast. Placenta 1989; 10: 137–51.CrossRefGoogle ScholarPubMed
96Daniels-McQueen, S, Krichevsky, A, Boime, I. Isolation and characterization of human cytotrophoblast cells. Trophoblast Research 1987; 2: 423–45.Google Scholar
97Dodeur, M, Malassine, A, Bellet, D, Mensier, A, Evain-Brion, D. Characterization and differentiation of human first trimester placental trophoblastic cells in culture. Reprod Nutr Dev 1990; 30: 183–92.CrossRefGoogle ScholarPubMed
98Lai, WH, Guyda, HJ. Characterization and regulation of epidermal growth factor receptors in human placental cell cultures. J Clin Endocrinol Metab 1984; 58: 344–52.CrossRefGoogle ScholarPubMed
99Truman, P, Ford, HC. The effect of substrate and epidermal growth factor on human placental trophoblast cells in culture. In Vitro Cell Dev Biol 1986; 22: 525–28.CrossRefGoogle ScholarPubMed
100Masuhiro, K, Matsuzaki, N, Nishino, E et al. Trophoblast-derived interleukin-1 (IL-1) stimulates the release of human chorionic gonadotropin by activating IL-6 and IL-6-receptor system in first trimester human trophoblasts. J Clin Endocrinol Metab 1991; 72: 594–601.CrossRefGoogle ScholarPubMed
101Steele, GI, Currie, WD, Leung, EH, Yuen, BH, Leung, PCK. Rapid stimulation of human chorionic gonadotropin secretion by interleukin 1 from perfused first trimester trophoblast. J Clin Endocrinol Metab 1992; 75: 783–88.Google ScholarPubMed
102Li, Y, Matsuzaki, N, Masuhiro, K et al. Trophoblast-derived tumor necrosis factor alpha induces release of human chorionic gonadotropin using interleukin 6 and IL-6-receptor dependent system in the normal human trophoblasts. J Clin Endocrinol Metab 1992; 74: 184–91.Google ScholarPubMed
103Loke, YW, King, A, Gardner, L, Carter, NP. Evidence for the expression of granulocyte-macrophage colony stimulating factor receptors by human first trimester extravillous trophoblast and its response to this cytokine. J Reprod Immunol 1992; 22: 33–45.CrossRefGoogle ScholarPubMed
104Burrows, TD, King, A, Loke, YW. Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin. Hum Reprod 1993; 8: 475–84.CrossRefGoogle ScholarPubMed
105Martin, O, Arias, F. Plasminogen activator production by trophoblast cells in vitro: effect of steroid hormones and protein synthesis inhibitors. Am J Obstet Gynecol 1982; 142: 402–409.CrossRefGoogle ScholarPubMed
106Bischof, P, Martelli, M. Proteolysis in the penetration phase of the implantation process. Placenta 1992; 13: 17–24.CrossRefGoogle ScholarPubMed
107Emonard, H, Christiane, Y, Smet, M, Grimaud, JA, Foidart, JM. Type IV and interstitial collagenolytic activities in normal and malignant trophoblast cells are specifically regulated by the extracellular matrix. Invasion Metastasis 1990; 10: 170–77.Google ScholarPubMed
108Graham, CH, Lala, PK. Mechanism of control of trophoblast invasion in situ. J Cell Physiol 1991; 148: 228–34.CrossRefGoogle ScholarPubMed
109King, A, Birkby, C, Loke, YW. Early human decidual cells exhibit NK activity against the K562 cell line but not against first trimester trophoblast. Cell Immunol 1989; 118: 337–44.CrossRefGoogle Scholar
110King, A, Loke, YW. Effect of Interferon gamma and interferon alpha on killing of human trophoblast by decidual LAK cells. J Reprod Immunol 1993; 23: 51–62.CrossRefGoogle ScholarPubMed
111King, A, Loke, YW. Uterine large granular lymphocytes: a possible role in embryonic implantation? Am J Obstet Gynecol 1990; 162: 308–10.CrossRefGoogle ScholarPubMed
112Brosens, IA. The utero-placental vessels at term – the distribution and extent of the physiological changes. Trophoblast Research 1988; 3: 61–67.Google Scholar
113Brosens, I, Robertson, WB, Dixon, HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Path Bact 1967; 93: 569–79.CrossRefGoogle ScholarPubMed
114Weir, PE. Immunofluorescent studies of the uteroplacental arteries in normal pregnancy. Br J Obstet Gynaecol 1981; 88: 301–307.CrossRefGoogle ScholarPubMed
115Gosseye, S, Fox, H. An immunohistological comparison of the secretory capacity of villous and extravillous trophoblast in the human placenta. Placenta 1984; 5: 329–48.CrossRefGoogle ScholarPubMed
116Babalola, GO, Coutifaris, C, Soto, EA, Kliman, HJ, Shuman, H, Strauss, JF III. Aggregation of dispersed human cytotrophoblastic cells: lessons relevant to the morphogenesis of the placenta. Dev Biol 1990; 137: 100–108.CrossRefGoogle Scholar
117Douglas, GC, King, BF. Differentiation of human trophoblast cells in vitro as revealed by immunocytochemical staining of desmoplakin and nuclei. J Cell Sci 1990; 96: 131–41.CrossRefGoogle ScholarPubMed
118Farmer, DR, Nelson, DM. A fibrin matrix modulates the proliferation, hormone secretion and morphologic differentiation of cultured human placental trophoblast. Placenta 1992; 13: 163–77.CrossRefGoogle ScholarPubMed
119Kao, LC, Caltabiano, S, Wu, S, Strauss, FJ III, Kliman, HJ. The human villous cytotrophoblast: interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Dev Biol 1988; 130: 693–702.CrossRefGoogle ScholarPubMed
120Ulloa-Aguirre, A, August, AM, Golos, TG et al. 8-Bromo-adenosine 3′, 5′- monophosphate regulates expression of chorionic gonadotropin and fibronectin in human cytotrophoblasts. J Clin Endocrinol Metab 1987; 64: 1002–1009.CrossRefGoogle ScholarPubMed
121Brosens, IA, Robertson, WB, Dixon, HG. The role of spiral arteries in the pathogenesis of preeclampsia. In: Wynn, RM ed. Obstetrics and Gynecology Annual. New York: Appleton-Century-Crofts, 1972: 177–91.Google Scholar
122Robertson, WB. Discussion. Pathology of the uteroplacental bed. In: Sharp, F, Symonds, EM eds. Hypertension in pregnancy. New York: Perinatology Press, 1987: 115.Google Scholar
123Gerretsen, G, Huisjes, HJ, Hardonk, MJ, Elema, JD. Trophoblast alterations in the placental bed in relation to physiological changes in spiral arteries. Br J Obstet Gynaecol 1983; 90: 34–39.CrossRefGoogle ScholarPubMed
124Pijnenborg, R, Anthony, J, Davey, DA et al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991; 98: 648–55.CrossRefGoogle ScholarPubMed
125Robertson, WB, Brosens, I, Dixon, HG. The pathological response of the vessels of the placental bed to hypertensive pregnancy. J Path Bact 1967; 93: 581–92.CrossRefGoogle ScholarPubMed
126De Wolf, F, Robertson, WB, Brosens, I. The ultrastructure of acute atherosis in hypertensive pregnancy. Am J Obstet Gynecol 1975; 123: 164–74.CrossRefGoogle ScholarPubMed
127Khong, TY, De Wolf, F, Robertson, WB, Brosens, I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93: 1049–59.CrossRefGoogle ScholarPubMed
128Robertson, WB, Brosens, I, Dixon, G. Uteroplacental vascular pathology. Eur J Obstet Gynecol Reprod Biol 1975; 5: 47–65.CrossRefGoogle ScholarPubMed
129Labarrere, CA. Acute atherosis. A histopathological hallmark of immune aggression? Placenta 1988; 9: 95–108.CrossRefGoogle ScholarPubMed
130Meekins, JW, Pijnenborg, R, Hanssens, M, McFadyen, IR, Van Assche, A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies using histological and immunohistochemical techniques. Br J Obstet Gynaecol 1994 (in press).CrossRefGoogle Scholar
131Davey, DA, MacGillivray, I. The classification and definition of the hypertensive disorders of pregnancy. Am J Obstet Gynecol 1988; 158: 892–98.CrossRefGoogle ScholarPubMed
132Brosens, I, Dixon, HG, Robertson, WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977; 84: 656–63.CrossRefGoogle ScholarPubMed
133Khong, TY, Liddell, HS, Robertson, WB. Defective haemochorial placentation as a cause of miscarriage: a preliminary study. Br J Obstet Gynaecol 1987; 94: 649–55.CrossRefGoogle ScholarPubMed
134Zhou, Y, Damsky, CH, Chiu, K, Roberts, JM, Fisher, SJ. Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 1993; 91: 950–60.CrossRefGoogle ScholarPubMed
135Aplin, JD. Expression of integrin α6 β4 in human trophoblast and its loss from extravillous cells. Placenta 1993; 14: 203–15.CrossRefGoogle ScholarPubMed
136Pijnenborg, R, Robertson, WB, Brosens, I. Morphological aspects of placental ontogeny and phylogeny. Placenta 1985; 6: 155–62.CrossRefGoogle ScholarPubMed
137McParland, P, Pearce, JM. Doppler blood flow in pregnancy. Placenta 1988; 9: 427–50.CrossRefGoogle ScholarPubMed