Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-27T04:50:50.652Z Has data issue: false hasContentIssue false
  • English
  • Français

Trophoblast infiltration

Published online by Cambridge University Press:  02 March 2009

Harvey J Kliman
Harvey J Kliman*
Affiliation:
Developmental and Perinatal Pathology Unit, Yale University School of Medicine, Connecticut, USA
*
Harvey J Kliman, Developmental and Perinatal Pathology Unit, Departments of Pathology and Obstetrics and Gynecology, B130 Brady Laboratory, 310 Cedar Street, POB 208023, New Haven, CT 06520–8023, USA.
Get access Rights & Permissions [Opens in a new window]

Extract

Sexual reproduction in the ocean necessitates only the combination of gametes, followed by absorption of nutrients and oxygen from the surrounding watery medium. As life moved from the sea to the land, reproductive strategies required compensation for the loss of this aquatic environment. For the mammals, and scattered other animals, the solution to this problem was the development of the placenta, the means by which the fetus extracts nutrients from its environment. As the animals that utilized the placenta evolved from small rodent-like creatures with short gestations to larger animals with prolonged gestations, the demands of the developing fetus grew. Whereas the placenta of the fetal pig, with a gestational period of a little less than four months, can extract sufficient nutrients from the mother by simple diffusion across the uterus to the placenta, the human fetus needs a far more complex uteroplacental relationship.

Type
Articles
Information
Reproductive Medicine Review , Volume 3 , Issue 2 , July 1994 , pp. 137 - 157
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

1 Benirschke, K, Kaufmann, P. Pathology of the human placenta. New York: Springer-Verlag, 1990: 585–613.Google Scholar
2 Naeye, RL. Pregnancy hypertension, placental evidences for low uteroplaental blood flow, and spontaneous premature delivery. Hum Pathol 1989; 20:441–44.Google Scholar
3 Vander, AJ, Sherman, JH, Luciano, DS. Human physiology: the mechanisms of body function. New York: MacGraw-Hill, 1970; 264.Google Scholar
4 Hertig, AT, Rock, J. A description of 34 human ova within the first 17 days of development. Am J Anat 1956; 98: 435–94.CrossRefGoogle ScholarPubMed
5 Conley, AJ, Mason, JI. Placental steroid hormones. Baillieres Clin Endocrinol Metab 1990; 4: 249–72.Google Scholar
6 Petraglia, F, Calza, L, Garuti, GC, Giardino, L, De, RB, Angioni, S. New aspects of placental endocrinology. J Endocrinol Invest 1990; 13: 353–71.CrossRefGoogle ScholarPubMed
7 Kliman, HJ, Nestler, JE, Sermasi, E, Sanger, JM, Strauss JF3. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology 118: 1567–82.CrossRefGoogle Scholar
8 Feinberg, 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: 20–26.Google ScholarPubMed
9 Jara, CS, Salud, AT, Bryantgreenwood, GD, Pirens, G, Hennen, G, Frankenne, F. Immunocytochemical localization of the human growth hormone variant in the human placenta. J Clin Endocrinol Metab 1989; 69: 1069–72.Google Scholar
10 Moll, UM, Lane, BL. Proteolytic activity of 1st trimester human placenta – localization of interstitial collagenase in villous and extravillous trophoblast. Histochemistry 1990; 94: 555–60.CrossRefGoogle ScholarPubMed
11 Maruyama, I, Bell, CE, Majerus, PW. Thrombomodulin is found on endothelium of arteries, veins, capillaries, and lymphatics, and on syncytiotrophoblast of human placenta. J Cell Biol 1985; 101: 363–71.CrossRefGoogle ScholarPubMed
12 Ohtani, H, Maruyama, I, Yonezawa S. Ultrastructural immunolocalization of thrombomodulin in human placenta with microwave fixation. Act Hist Cyt 1989; 22: 393–95.Google Scholar
13 Posner, BI. Insulin receptors in human and animal placental tissue. Diabetes 1974; 23: 209–17.Google Scholar
14 Uzumaki, H, Okabe, T, Sasaki, N et al. Identification and characterization of receptors for granulocyte colony-stimulating factor on human placenta and trophoblastic cells. Proc Natl Acad Sci USA 1989; 86: 9323–26.Google Scholar
15 Kawagoe, K, Akiyama, J, Kawamoto, T, Morishita, Y, Mori, S. Immunohistochemical demonstration of epidermal growth factor (EGF) receptors in normal human placental villi. Placenta 1990; 11: 7–15.Google Scholar
16 Feinberg, RF, Kliman, HJ, Lockwood, CJ. Oncofetal fibronectin: a trophoblast ‘glue’ for human implantation? Am J Pathol 1991; 138: 537–43.Google ScholarPubMed
17 Ohlsson, R, Larson, E, Nilsson, O, Wahlstrom P. Blastocyst implantation precedes induction of insulin-like growth factor II gene expression in human trophoblasts. Development 1989; 106: 555–59.CrossRefGoogle ScholarPubMed
18 Lindenberg, S. infrastructure in human implantation: transmission and scanning electron microscopy. Baillieres Clin Obstet Gynaecol 1991; 5: 1–14.Google Scholar
19 Kurman, RJ, Main, CS, Chen H-C. Intermediate trophoblast: a distinctive form of trophoblast with specific morphological, biochemical and functional features. Placenta 1984; 5: 349–70.Google Scholar
20 Kurman RJ. The morphology, biology, and pathology of intermediate trophoblast: A look back to the present. Human Pathol 1991; 22: 847–55.CrossRefGoogle Scholar
21 Pijnenborg R. Trophoblast invasion. Reprod Med Rev 1994; 3: 53–73.Google Scholar
22 Kovats, S, Main, EK, Librach, C, Stubblebine, M, Fisher, SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990; 248: 220–23.Google Scholar
23 Pijnenborg, R, Robertson, WB, Brosens, I, Dixon, G. Trophoblast invasion and the establishment of hemochorial placentation in man and laboratory animals. Placenta 1981; 2: 71–92.Google Scholar
24 Robertson, WB, Brosens, I, Pijnenborg, R, DeWolf, F. The making of the placental bed. Europ J Obstet Gynec Reprod Biol 1984; 18: 255–66.CrossRefGoogle ScholarPubMed
25 Enders, AC. Trophoblast differentiation during the transition from trophoblastic plate to lucunar stage of implantation in the rhesus monkey and human. Am J Anat 1989; 186: 85–98.Google Scholar
26 Enders, 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.Google Scholar
27 Blankenship, 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
28 Rodesch, F, Simon, P, Donner, C, Jauniaux, E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Ob Gyn 1992; 80: 283–85.Google ScholarPubMed
29 Jenkinson, EJ. The in vitro blastocyst outgrowth system as a model for the analysis of periimplantation development. In: Johnson, M ed. Development in mammals, Volume 2. Amsterdam: North-Holland, 1978; 157.Google Scholar
30 Armant, DR, Kaplan, HA, Lennarz, WJ. Fibronectin and laminin promote in vitro attachment and outgrowth of mouse blastocysts. Dev Biol 1986; 116: 519–23.CrossRefGoogle ScholarPubMed
31 Farach, MC, Tang, JP, Decker, GL, Carson, DD. Heparin/heparan sulfate is involved in attachment and spreading of mouse embryos in vitro. Dev Biol 1987; 123: 401–10.Google Scholar
32 Carson, DD, Tang, JP, Gay, S. Collagens support embryo attachment and outgrowth in vitro: effects of the Arg-Gly-Asp sequence. Dev Biol 1988; 127: 368–75.Google Scholar
33 Glass, RH, Spindle, AI, Pedersen, RA. Mouse embryo attachment to substratum and interaction of trophoblast with cultured cells. J Exp Zool 1979; 208: 327.Google Scholar
34 Sengupta, J, Given, RL, Carey, JB, Weitlauf, HM. Primary culture of mouse endometrium on floating collagen gels: a potential in vitro model for implantation. Ann N Y Acad Sci 976: 75–94.Google Scholar
35 Cammarata, PR, Oakford, L, Canta-Crouch, D, Wordinger, R. Attachment of blastocysts to lens capsule: A model system for trophoblast-epithelial cell interactions on a natural basement membrane. Cell Tissue Res 1987; 250: 633–40.Google Scholar
36 Glenister, TW. Organ culture as a new method for studying the implantation of mammalian blastocysts. Proc Royal Soc B 1961; 154: 428–31.Google Scholar
37 Grant, PS, Ljungkvist, I, Nilsson, O. The hormonal control and morphology of blastocyst invasion in the mouse uterus in vitro. J Embryol Exp Morphol 1975; 34: 310.Google Scholar
38 Bulletti, C, Jasonni, VM, Tabanelli, S et al. Early human pregnanc. in vitro utilizing an artifically perfused uterus. Fertil Steril 1988; 49: 991–96.CrossRefGoogle Scholar
39 Kishimoto, Y, Tominaga, T, Aso, T, Kinoshita, M, Mori, T. Human trophoblast and endometrial interactions in vitro. Acta Obst Gynaec Jpn 1987; 39: 463.Google ScholarPubMed
40 Lindenberg, S, Hyttel, P, Lenz, S, Holmes, PV. Ultrastructure of the early human implantation in vitro. Hum Reprod 1986; 1: 533–38.Google Scholar
41 Kliman, HJ, Coutifaris, C, Babalola, GO et al. The human trophoblast: homotypic and heterotypic cell-cell interactions. Prog Clin Biol Res 1989; 294: 425–34.Google Scholar
42 Kliman, HJ, Feinberg, RF, Haimowitz, JE. Human trophoblast-endometrial interactions in an in vitro suspension culture system. Placenta 1990; 11: 349–67.CrossRefGoogle Scholar
43 Kliman, HJ, Feinberg, RF. Human trophoblastextracellular matrix (ECM) interactions in vitro: ECM thickness modulates morphology and proteolytic activity. Proc Natl Acad Sci USA 1990; 87: 3057–61.Google Scholar
44 Glasser, SR, Mulholland, J. Receptivity is a polarity dependent special function of hormonally regulated uterine epithelial cells. Microsc Res Tech 1993; 25: 106–20.CrossRefGoogle ScholarPubMed
45 Kleinman, HK, McGarvey, ML, Hassell, JR, Star, VL, Cannon, FB, Laurie, GW, Martin, GR. Basement membrane complexes with biological activity. Biochemistry 1986; 25: 312–8.CrossRefGoogle ScholarPubMed
46 Kliman, HJ, Coutifaris, C, Feinberg, RF, Strauss, JF III, Haimowitz, JE. Implantation in vitro models utilizing human tissues. In: Yoshinag, K ed. Blastocyst implantation. Boston: Adams, 1989: 83–91.Google Scholar
47 Yagel, 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.Google Scholar
48 Librach, 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
49 Queenan, JT, Kao, L-C, Arboleda, et al. Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J Biol Chem 1987; 262: 10903–903.CrossRefGoogle ScholarPubMed
50 Jensen, HE, Poulsen, OM, Hau, J. Localization of plasmin on the surface of the human trophoblast. Biomed Biochim Acta 1989; 48: 437–40.Google Scholar
51 Bischof, P, Friedli, E, Martelli, M, Campana, A. Expression of extracellular matrix-degrading metalloproteinases by cultured human cytotrophoblast cells: effects of cell adhestion and immunopurification. Am J Obstet Gynecol 1991; 165: 1791–801.Google Scholar
52 Herz, J, Clouthier, DE, Hammer, RE. LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 1992; 71: 411–21.Google Scholar
53 Fernandez, PL, Merino, MJ, Nogales, FF, Charonis, AS, Stetler-Stevenson, W, Liott, L. Immunohistochemical profile of basement membrane proteins and 72 kilodalton type IV collagenase in the implantation placental site. An integrated view. Lab Invest 1992; 66: 572–79.Google Scholar
54 Lala, PK, Graham, CH. Mechanisms of trophoblast invasiveness and their control: the role of proteases and protease inhibitors. Cancer Metastasis Rev 1990; 9: 369–79.Google Scholar
55 Strickland, S, Reich, E, Sherman, MI. Plasminogen activator in early embryogenesis: enzyme production by trophoblast and parietal endoderm. Cell 1976; 9: 231–40.Google Scholar
56 Sherman, MI, Strickland, S, Reich, E. Differentiation of early mouse embryonic and teratocarcinoma cells in vitro: plasminogen activator production. Canc Res 1976; 36: 4208–16.Google Scholar
57 Axelrod, HR. Altered trophoblast functions in implantation-defective mouse embryos. Dev Biol 1985; 108: 185–90.Google Scholar
58 Martin, O, Arias, F. Plasminogen activator production by trophoblast cells in vitro: effect of steroid hormones and protein synthesis inhibitors. J Obstet Gynecol 1982; 142: 402–409.Google Scholar
59 Zini, JM, Murray, SC, Graham, CH et al. Characterization of urokinase receptor expression by human placental trophoblasts. Blood 1992; 79: 2917–29.Google Scholar
60 Cajot, JF, Schleuning, WD, Medcalf, RL et al. Mouse L cells expressing human prourokinase-type plasminogen activator: effects on extracellular matrix degradation and invasion. J Cell Biol 1989; 109: 915–25.Google Scholar
61 Ellis, V, Pyke, C, Eriksen, J, Solberg, H, Dano, K. The urokinase receptor: involvement in cell surface proteolysis and cancer invasion. Ann N Y Acad Sci 1992; 667: 13–31.Google Scholar
62 Estreicher, A, Mullhauser, J, Carpentier, J-L, Orci, L, Vassalli, J-D. The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J Cell Biol 1990; 111: 783–92.Google Scholar
63 Hall, SW, Humphries, JE, Gonias, SL. Inhibition of cell surface receptor-bound plasmin by α2-antiplasmin and α2-macroglobulin. J Biol Chem 1991; 266: 12329–36.Google Scholar
64 Plow, EF, Felez, J, Miles, LA. Cellular regulation of fibrinolysis. Thromb Hemost 1991; 66: 32–36.Google Scholar
65 Strickland, DK, Ashcom, JD, Williams, S, Burgess, WH, Migliorini, M, Argraves, WS. Sequence identity between the α2 macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem 1990; 265: 17401–404.Google Scholar
66 Williams, SE, Ashcom, JD, Argraves, WS, Strickland, DK. A novel mechanism for controlling the activity of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J Biol Chem 1992; 267: 9035–40.Google Scholar
67 Loskutoff, DJ, Ny, T, Sawdey, M, Lawrence, D. Fibrinolytic system of cultured endothelial cells: regulation by plasminogen activator inhibitor. J Cell Biochem 1980; 32: 273.CrossRefGoogle Scholar
68 Wun, TC, Reich, E. An inhibitor of plasminogen activation from human placenta. Purification and characterization. J Biol Chem 1987; 262: 3646–53.Google Scholar
69 Kruithof, EKO, Tran-Thang, C, Gudinchet, A et al. Fibrinolysis in pregnancy: a study of plasminogen activator inhibitors. Blood 1987; 69: 460.Google Scholar
70 Ye, RD, Wun, TC, Sadler, JE. cDNA cloning and expression in Escherichia coli of a plasminogen activator inhibitor from human placenta. J Biol Chem 1987; 262: 3718–25.Google Scholar
71 DeBoer, K, Lecander, I, ten Cate, JW, Borm, JJJ, Treffers, PE. Placental-type plasminogen activator inhibitor in pre-eclampsia. Am J Obstet Gynecol 1968; 158: 518.Google Scholar
72 Gore, M, Eldon, S, Trofatter, KF, Soong, S-J, Pizzo, SV. Pregnancy-induced changes in the fibrinolytic balance: evidence for defective release of tissue plasminogen activator and increased levels of the fast-acting tissue plasminogen activator inhibitor. Am J Obstet Gynecol 1987; 156: 674.Google Scholar
73 Feinberg, RF, Strauss JF3, Wun, T-C, Kliman, HJ. Plasminogen activators (PAs) and plasminogen activator inhibitors (PAIs) in human trophoblasts: markers of trophoblast invasion (Abstract). Proc Soc Gyn Invest 1989; 36: 487.Google Scholar
74 Feinberg, RF, Kao, LC, Wang, C-L, Bui, L, Kliman, HJ, Strauss JF3. Plasminogen activator inhibitor (PAI) expression in normal and malignant human trophoblasts: regulation by 8-bromo-camp and phorbol esters (Abstract). Proc Soc Gyn Invest 1990; 37: 329.Google Scholar
75 Sappino, AP, Huarte, J, Belin, D, Vassalli, JD. Plasminogen activators in tissue remodeling and invasion: mRNA localization in mouse ovaries and implanting embryos. J Cell Biol 1989; 109: 2471–79.Google Scholar
76 Multhaupt, HAB, Mazar, A, Cines, DB, Warhol, MJ, McCrae, KR. Expression of urokinase receptors by human trophoblast: a histochemical and ultrastructural analysis. Lab Invest 1994 (in press).Google Scholar
77 Mignatti, P, Robbins, E, Rifkin, DB. Tumor invasion through the human amniotic membrane: requirement for a proteinase cascade. Cell 1986; 47: 487–98.Google Scholar
78 Reich, R, Thompson, EW, Iwamoto, Y et al. Effects of inhibitors of plasminogen activator, serine proteinases, and collagenase IV on the invasion of basement membranes by metastatic cells. Cancer Res 1988; 48: 3307–12.Google ScholarPubMed
79 Gavrilovic, J, Murphy, G. The role of plasminogen in cell-mediated collagen degradation. Cell Biol Int Rep 1989; 13: 367–75.Google Scholar
80 Shi, QJ, Lei, ZM, Rao, CV, Lin, J. Novel role of human chorionic gonadotropin in differentiation of human cytorophoblasts. Endocrinology 1993; 132: 1387–95.Google Scholar
81 Milwidsky, A, Finci, YZ, Yagel, S, Mayer, M. Gonadotropin-mediated inhibition of proteolytic enzymes produced by human trophoblast in culture. J Clin Endocrinol Metab 71: 1101–105.Google Scholar
82 Lysiak, JJ, McCrae, KR, Lala, PK. Localization of transforming growth factor-beta at the human fetal-maternal interface: role in trophoblast growth and differentiation. Biol Reprod 1992; 46: 561–72.Google Scholar
83 Stewart, CL. A cytokine regulating embryo implantation. Ann N Y Acad Sci 1994 (in press).Google Scholar
84 Damsky, 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.Google Scholar
85 Graham, CH, Lala, PK. Mechanism of control of trophoblast invasion in situ. J Cell Physiol 1991; 148: 228–34.Google Scholar
86 Emonard, 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
87 Paranjpe, M, Engel, L, Youg, N, Liotta, LA. Activation of human breast carcinoma collagenase through plasminogen activator. Life Sci 1980; 26: 1223–31.CrossRefGoogle ScholarPubMed
88 O'Grady, RL, Upfold, LI, Stephens, RW. Rat mammary carcinoma cells secrete active collagenase and activate latent enzyme in the stroma via plasminogen activator. Int J Cancer 1981; 28: 509–15.Google Scholar
89 Salo, T, Liotta, LA, Keski-Oja, J, Turpeenniemi-Hujanen, T, Tryggvason, K. Secretion of basement membrane collagen degrading enzyme and plasminogen activator by transformed cells - role in metastasis. Int J Cancer 1982; 30: 669–73.CrossRefGoogle ScholarPubMed
90 Keski-Oja, J, Lohi, J, Tuuttila, A, Tryggvason, K, Vartio, T. Proteolytic processing of the 72,000-Da type IV collagenase by urokinase plasminogen activator. Exp Cell Res 1992; 202: 471–76.Google Scholar
91 Liotta, LA, Murano, G, Katz, DA, Gordon, RK, Chiang, PK, Schiffmann, E. Tumor cell autocrine motility factor. Proc Natl Acad Sci USA 1986; 83: 3302–306.Google Scholar
92 Terranova, VP, DiFlorio, R, Hujanen, ES et al. Laminin promotes rabbit neutrophil motility and attachment. J Clin Invest 1986; 77: 1180–86.CrossRefGoogle ScholarPubMed
93 Kao, LC, Caltabiano, S, Wu, S, Strauss JF3, 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.Google Scholar
94 Armant, DR. Cell interactions with laminin and its proteolytic fragments during outgrowth of mouse primary trophoblast cells. Biol Reprod 1991; 45: 664–72.Google Scholar
95 Romagnano, L, Babiarz, B. Mechanisms of murine trophoblast interaction with laminin. Biol Reprod 1993; 49: 374–80.CrossRefGoogle ScholarPubMed
96 Loke, YW, Gardner, L, Burland, K, King, A. Laminin in human trophoblast-decidua interaction. Hum Reprod 1989; 4: 457–63.CrossRefGoogle ScholarPubMed
97 Loke, YW, Gardner, L, Grabowska, A. Isolation of human extravillous trophoblast cells by attachment to laminin-coated magnetic beads. Placenta 1989; 10: 407–15.Google Scholar
98 Aplin, JD. Expression of integrin alpha 6 beta 4 in human trophoblast and its loss from extravillous cells. Placenta 1993; 14: 2744–53.Google Scholar
99 Burrows, TD, King, A, Loke, YW. Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin. Hum Reprod 1993; 8: 475–84.Google Scholar
100 Zhou, Y, Damsky, CH, Chiu, K, Roberts, JM, Fisher, SJ. Pre-eclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J Clin Invest 1993; 91: 950–60.Google Scholar
101 Yagel, S, Kerbel, R, Lala, P, Eldar, GT, Dennis, JW. Basement membrane invasion by first trimester human trophoblast: requirement for branched complex-type Asn-linked oligosaccharides. Clin Exp Metastasis 1990; 8: 305–17.Google Scholar
102 Pöllänen, J, Saksela, O, Salonen, E-M, Andreasen, P, Nielsen, L, Dano, K, Vaheri, A. Distinct localizations of urokinase-type plasminogen activator and its Type 1 inhibitor under cultured human fibroblasts and sarcoma cells. J Cell Biol 1987; 104: 1085–96.Google Scholar
103 Ingber, DE, Folkman, J. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol 1989; 109: 317–30.Google Scholar
104 Ingber, D. Integrins as mechanochemical transducers. Curr Opin Cell Biol 1991; 3: 841–48.Google Scholar
105 Autio, HH, Sandberg, M, Pihlajaniemi, T, Vuorio, E. Synthesis of laminin and type IV collagen by trophoblastic cells and fibroblastic stromal cells in the early human placenta. Lab Invest 1991; 64: 483–91.Google Scholar
106 OShea, KS, Liu, LH, Kinnunen, LH, Dixit, VM. Role of the extracellular matrix protein thrombospondin in the early development of the mouse embryo. J Cell Biol 1990; 111: 2713–23.CrossRefGoogle ScholarPubMed
107 Feinberg, RF, Kliman, HJ, Wang, CL. Transforming growth factor beta (TGFβ) stimulates tropho-uteronectin (TUN) synthesis in vitro: implications for trophoblast implantation in vivo. J Clin Endocrinol Metab 1994; 78: 1241–48.Google Scholar
108 Nachtigall, MJ, Kliman, HJ, Feinberg, RF, Meaddough, EL, Arici, A. Potential role of leukemia inhibitory factor (LIF) in human implantation (Abstract). Proc Soc Gyn Invest 1994; 41: 96.Google Scholar
109 Strickland, S, Richards, WG. Invasion of the trophoblasts. Cell 1992; 71: 355–57.Google Scholar
110 Vuckovic, M, Genbacev, O, Kumar, S. Immunohistrochemical localisation of transforming growth factor-beta in first and third trimester human placenta. Pathobiology 1992; 60: 149–51.Google Scholar
111 Hofmann, GE, Drews, MR, Scott, RTJ, Navot, D, Heller, D, Deligdisch, L. Epidermal growth factor and its receptor in human implantation trophoblast: immunohistochemical evidence for autocrine/paracrine function. J Clin Endocrinol Metab 1992; 74: 981–88.Google Scholar
112 Filla, MS, Zhang, CX, Kaul, KL. A potential transforming growth factor alpha/epidermal growth factor receptor autocrine circuit in placental cytotrophoblasts. Cell Growth Differ 4: 387–93.Google Scholar
113 Laiho, M, Keski-Oja, J. Growth factors in the regulation of pericellular proteolysis: a review. Cancer Res 1989; 49: 2533–53.Google Scholar
114 Smith, MA. Pre-eclampsia. Prim Care 1993; 20: 655–64.Google Scholar
115 Khong, TY, Sawyer, IH, Heryet, AR. An immunohistolic study of endothelialization of uteroplacental vessels in human pregnancy-evidence that endothelium is focally disrupted by trophoblast in pre-eclampsia. Am J Obstet Gynecol 1992; 167: 751–56.Google Scholar
116 Roberts, JM, Taylor, RN, Musci, TJ, Rodgers, GM, Hubel, CA, Mclaughlin, MK. Pre-eclampsia - An Endothelial Cell Disorder. Am J Obstet Gynecol 1989; 161: 1200–204.Google Scholar
117 Chua, S, Wilkins, T, Sargent, I, Redman, C. Trophoblast deportation in pre-eclamptic pregnancy. Br J Obstet Gynaecol 1991; 98: 973–79.Google Scholar
118 Bishop, PW, Malam, JE, Morris, JA, Fox, H. Accelerated expression of Ca antigen by placental villous trophoblast in pre-eclampsia. Placenta 1990; 11: 487–92.Google Scholar
119 Zeeman, GG, Dekker, GA, van, GHP, Kraayenbrink, AA. Endothelial function in normal and pre-eclamptic pregnancy: a hypothesis. Eur J Obstet Gynecol Reprod Biol 1988; 43: 113–22.Google Scholar
120 Toppozada, MK. Role of prostaglandins in pre-eclampsia. Acta Obstet Gynecol Scand 1990; 69: 375–77.CrossRefGoogle ScholarPubMed
121 Hsu, CD, Iriye, B, Johnson, TR, Witter, FR, Hong, SF, Chan, DW. Elevated circulating thrombomodulin in severe pre-eclampsia. Am J Obstet Gynecol 1993; 169: 148–49.Google Scholar
122 Fay, RA. Uric acid in pregnancy and pre-eclampsia: an alternative hypothesis. Aust N Z J Obstet Gynaecol 1990: 30: 141–42.Google Scholar
123 Purcell, WM. Human placental mast cells: a role in pre-eclampsia? Med Hypotheses 1992; 39: 281–83.Google Scholar
124 Zeeman, GG, Dekker, GA. Pathogenesis of pre-eclampsia: a hypothesis. Clin Obstet Gynecol 1992; 35: 317–37.Google Scholar
125 Krege, JH, Katz, VL. A proposed relationship between vasopressinase altered vasopressin and pre-eclampsia. Med Hypotheses 1990; 31: 283–87.Google Scholar
126 Tuohy, JF, James, DK. Pre-eclampsia and trisomy 13. Br J Obstet Gynaecol 1992; 99: 891–94.CrossRefGoogle ScholarPubMed
127 Feinberg, RF, Kliman, HJ, Cohen, AW. Preeclampsia, trisomy 13, and the placental bed. Obstet Gynecol 1991; 78: 505–508.Google Scholar
128 Arkwright, PD, Radernacher, TW, Dwek, RA, Redman, CW. Pre-eclampsia is associated with an increase in trophoblast glycogen synthase activity, similar to that found in hydatidiform moles. J Clin Invest 1993; 91: 2744–53.CrossRefGoogle ScholarPubMed
129 Christiane, Y, Aghayan, M, Emonard, H, Lallemand, A, Mahieu, P, Foidart, JM. Galactose alpha 1–3 galactose and anti-aloha galactose antibody in normal and pathological pregnancies. Placenta 1992; 13: 475–87.CrossRefGoogle ScholarPubMed
130 Young, RH, Kurman, RJ, Scully, RE. Proliferations and tumors of intermediate trophoblast of the placental site. Semin Diagn Pathol 1988; 5: 223–37.Google Scholar
131 Kurman, RJ. Pathology of trophoblast. Monogr Pathol 1991; 33: 195–227.Google Scholar
132 Sasagawa, M, Sasaki, T, Yasuda, M et al. Morphological and immunohistochemical study on specimens of trophoblastic diseases in which the presence of a villous formation could not be established. Nippon Sanka Fujinka Gakkai Zasshi 1988; 40: 761–68.Google Scholar
133 Kliman, HJ. Placental hormones. Infertil Reprod Med Clin North Am 1994 (in press).Google Scholar