Development of the utero-placental circulation: Purported mechanisms for cytotrophoblast invasion in normal pregnancy and pre-eclampsia

Pre-Eclampsia: Etiology and Clinical Practice

Volumn , Issue , 2007, Pages 20-36

  Lyall, Fiona ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84928293444     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9780511545634.003     Document Type: Chapter

References (124)

1. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. and Watson, J. (1994). Molecular Biology of the Cell. New York: Garland Publishing Inc.
2. Alexander, C. and Werb, Z. (1991). Extracellular matrix degradation. In Cell Biology of the Extracellular Matrix, ed. E. Hay. New York: Plenum Press, pp. 255–302.
3. Alsat, E., Wyplosz, P., Malassine, A., et al. (1996). Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast in vitro. J. Cell Physiol., 168, 346–53.
4. Aplin, J. D. (1993). Expression of integrin a6b4 in human trophoblast and its loss from extravillous cells. Placenta, 14, 203–15.
5. Aplin, J. D., Charlton, A. K. and Ayad, S. (1990). The role of matrix macromolecules in the invasion of decidua by trophoblast. Trophoblast Res., 4, 139–58.
6. Aplin, J. D., Haigh, T., Jones, C. J. P., Church, H. J. and Vicovac, L. J. (1999). Development of cytotrophoblast columns from explanted first trimester placental villi: role of fibronectin and integrin a5b1. Biol. Reprod., 60, 828–38.
7. Autio-Harmainen, H., Hurskainen, T., Niskasaari, K., Hoyhtya, M. and Tryggvason, K. (1992). Simultaneous expression of 70 kilodalton type IV collagenase and type IV collagen alpha 1 (IV) chain genes by cells of early human placenta and gestational endometrium.Lab. Invest., 67, 191–200.
8. Barber, A., Robson, S. C., Myatt, L., Bulmer, J. N. and Lyall, F. (2001). Hemeoxygenase expression in human placenta and placental bed: reduced expression of placenta endothelial HO-2 in preeclampsia and fetal growth restriction. FASEB J., 15, 1158–68.
9. Bass, K. E., Li, H. X., Hawkes, S. P., et al. (1997). Tissue inhibitor of metalloproteinase-3 expression is upregulated during human cytotrophoblast invasion in vitro.Dev. Genetics, 21, 61–7.
10. Bass, K. E., Morrish, D. W., Roth, I., et al. (1994). Human cytotrophoblast invasion is upregulated by epidermal growth factor. Evidence that paracrine factors modify this process. Dev. Biol., 164, 560–1.
11. Benyo, D. F., Miles, T. M. and Conrad, K. P. (1997). Hypoxia stimulates cytokine production by villous explants from the human placenta. J. Clin. Endo. Metabol., 82, 1582–8.
12. Birk, D. E., Silver, F. H. and Trelstad, R. L. (1991). Matrix assembly. In Cell Biology of Extracellular Matrix, ed. E. Hay. New York: Plenum Press, pp. 221–54.
13. Bischof, P., Friedli, E., Martell, 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, 1791–801.
14. Bischof, P., Haenggeli, L. and Campana, A. (1995a). Gelatinase and oncofetal fibronectin secretion is dependent on integrin expression on human cytotrophoblasts.Human Reprod., 10, 734–42.
15. Bischof, P., Haenggeli, L. and Campana, A. (1995b). Effect of leukemia inhibitory factor on human cytotrophoblast differentiation along the invasive pathway.Am. J. Reprod. Immunol., 34, 225–30.
16. Bjorn, S. F., Hastrup, N., Lund, L. R., Dano, K., Larsen, J. F. and Pyke, C. (1997). Co-ordinated expression of MMP-2 and its putative activator, MT1-MMP in human placentation.Mol. Hum. Reprod., 3, 713–23.
17. Brosens, I. A., Robertson, W. B. and Dixon, H. G. (1972). The role of the spiral arteries in the pathogenesis of pre-eclampsia. In Obstet Gyn Ann, ed. R. M. Wynn, vol. 4. New York: Appleton-Century-Crofts, pp. 177–91.
18. Bulmer, J. N., Morrison, L. and Johnson, P. M. (1988). Expression of the proliferation markers Ki67 and transferrin receptor by human trophoblast populations.J. Reprod. Immunol., 14, 291–302.
19. Burrows, T. D., King, A. and Loke, Y. W. (1994). Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells – implications for vascular invasion during implantation. Placenta, 15, 21–33.
20. Caniggia, I., Grisaru-Gravnosky, S., Kuliszewsky, M., Post, M. and Lye, S. J. (1999). Inhibition of TGFBb3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J. Clin. Invest., 103, 1641–50.
21. Caniggia, I., Mostachfi, H., Winter, J., et al. (2000a). Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGF-b3. J. Clin. Invest., 105, 577–87.
22. Caniggia, I., Winter, J., Lye, S. J. and Post, M. (2000b). Oxygen and placental development during the first trimester: implications for the pathophysiology of preeclampsia.Placenta, 21, S25–30.
23. Carter, W. G. P., Kaur, S. G., Gil, P. J. and Wayer, E. A. (1990). Distinct functions for a3b1 in focal adhesions and a6/b4 bullous pemphigoid antigen in a new stabilising anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J. Cell Biol., 111, 3141–54.
24. Castellucci, M., Classen-Linke, I., Munlhauser, J., Kaufmann, P., Zardi, L. and Chiquet-Ehrismann, R. (1991). The human placenta: a model for tenascin expression. ImmunoHistochem., 95, 449–58.
25. Chumbly, G., King, A., Robertson, K., Holmes, N. and Loke, Y. W. (1994). Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell Immunol., 155, 312–22.
26. Church, H. J., Richards, A. J. and Aplin, J. D. (1997). Laminins in decidua, placenta and choriocarcinoma cells. Trophoblast Res., 143–62.
27. Colbern, G. T., Chiang, M. H. and Main, E. K. (1994). Expression of the nonclassic histocompatibility antigen HLA-G by preeclamptic placenta. Am. J. Obstet. Gynecol., 170, 1244–50.
28. Coukos, G., Makrigiannakis, A., Amin, K., Albelda, S. M. and Coutifaris, C. (1998). Platelet endothelial cell adhesion molecule-1 is expressed by a subpopulation of human trophoblasts: a possible mechanism for trophoblast–endothelial interaction during haemochorial placentation. Mol. Hum. Reprod., 4, 357–67.
29. Coutifaris, C., Kao, L. C., Sehdev, H. M., et al. (1991). E-cadherin expression during the differentiation of human trophoblasts. Development, 113, 767–77.
30. Damsky, C. H., Fitzgerald, M. L. and Fisher, S. J. (1992). Distribution patterns of extracellular matrix components are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Invest., 89, 210–22.
31. Damsky, C. H., Librach, C., Lim, K.-H., et al. (1994). Integrin switching regulates normal trophoblast invasion.Development, 120, 3657–66.
32. DiFederico, E., Genbacev, O. and Fisher, F. J. (1999). Preeclampsia is associated with widespread apoptosis of placental cytotrophoblasts within the uterine wall.Am. J. Pathol., 155, 293–301.
33. Divers, M. J., Bulmer, J. N., Miller, D. and Lilford, R. J. (1995). Beta 1 integrins in third trimester human placentae: no differential expression in pathological pregnancy. Placenta, 16, 245–60.
34. Emmer, P. M., Joosten, I., Schut, M. H., Zusterzeel, P. L. M., Hendriks, J. C. M. and Steegers, E. A. P. (2004). Shift in expression of HLA-G mRNA spliceforms in pregnancies complicated by preeclampsia. J. Soc. Gyn. Invest., 11, 220–6.
35. Emonard, H. P., Christiane, Y., Smet, M., Grimaud, J. A. and Foidart, J. M. (1990). Type IV and interstitial collagenolytic activities in normal and malignant trophoblast cells are specifically regulated by the extracellular matrix. Invasion Metastasis, 10, 170–7.
36. Feinberg, R. F. and Kliman, H. J. (1993). Tropho-uteronectin (TUN): a unique oncofetal fibronectin deposited in the extracellular matrix of the tropho-uterine junction and regulated in vitro by cultured human trophoblast cells. Troph. Res., 7, 167–81.
37. Fernandez, P. L., Merino, M. J., Nogales, F. F., Charonis, A. S., Stetler Stevenson, W. G. and Liotta, L. (1992). Immunohistochemical profile of basement membrane proteins and 72-kilodalton type-IV collagenase in the implantation placental site – an integrated view.Lab. Invest., 66, 572–9.
38. Fisher, S. J., Cui, T. Y., Zhang, L., et al. (1989). Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J. Cell. Biol., 109, 891–902.
39. Genbacev, O., Joslin, R., Damsky, C. H., Polliotti, B. M. and Fisher, S. J. (1996). Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J. Clin. Invest., 97, 540–50.
40. Genbacev, O., Zhou, Y., Ludlow, J. W. and Fisher, S. J. (1997). Regulation of human placental development by oxygen tension. Science, 277, 1669–72.
41. Goldman-Wohl, D. S., Ariel, I., Greenfield, C., et al. (2000). Lack of human leucocyte antigen-G expression in extravillous trophoblast is associated with preeclampsia.Mol. Hum. Reprod., 6, 88–95.
42. Graham, C. H., Lysiak, J. J., McCrae, K. R. and Lala, P. K. (1992). Localization of transforming growth factor-B at the human fetal–maternal interface: role in trophoblast growth and differentiation. Biol. Reprod., 46, 561–72.
43. Hamai, Y., Fujii, T., Yamashita, T., et al. (1999). The expression of human leukocyte antigen-G on trophoblasts abolishes the growth-suppressing effect of interleukin-2 towards them. Am. J. Reprod. Immunol., 41, 153–8.
44. Hara, N., Fujii, T., Yamashita, T., Kozuma, S., Okai, T. and Taketani, Y. (1996). Altered expression of human leukocyte antigen (HLA-G) on extravillous trophoblasts in preeclampsia: immunohistological demonstration with Anti-HLA-G specific antibody ‘87G’ and anti-cytokeratin antibody ‘CAM5.2’. Am. J. Reprod. Immunol., 36, 349–538.
45. Hulboy, D. L., Rudolf, L. A. and Matrisisan, L. M. (1997). Matrix metalloproteases as mediators of reproductive function. Mol. Hum. Reprod., 3, 27–45.
46. Huppertz, B., Kertschanska, S., Frank, H. G., Gaus, G., Funayama, H. and Kaufmann, P. (1996). Extracellular matrix components of placental extravillous trophoblast: immunocytochemistry and ultrastructural distribution.Histochem. Cell Biol., 106, 291–301.
47. Huppertz, B., Kertschanska, S., Demir, A., Frank, H. G. and Kaufmann, P. I. (1998a). Immunohistochemistry of matrix metalloproteinases (MMP), their substrates and their inhibitors (TIMP) during trophoblast invasion in the human placenta. Cell Tiss. Res., 291, 133–48.
48. Huppertz, B. S., Kertschanska, S., Demir, A., Frank, H. G. and Kaufmann, P. (1998b). Production of membranetype matrix metalloproteinase-1 (MT-MMP-1) in early human placenta: a possible role in placental implantation.Cell Tiss. Res., 291, 133–48.
49. Hurskainen, T., Hoyhtya, M., Tuuttila, A., Oikarinen, and Autio-Harmainen, H. (1996). mRNA expressions of TIMP-1, -2 and -3 and 92-kD type IV collagenase in early human placenta studied by in situ hybridization.J. Histochem. Cytochem., 44, 1379–88.
50. Hustin, J. and Schapps, J. P. (1987). Echocardiographic and anatomic studies of the maternotrophoblastic border during the 1st trimester of pregnancy.Am. J. Obstet. Gynecol., 157, 62–168.
51. Irving, J. A. and Lala, P. K. (1995). Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGFb, IGF-II and IGFBP-1. Exp. Cell Res., 217, 419–27.
52. Janatpour, M. J., Utset, M. F., Cross, J. C., et al. (1999). A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation. Dev. Gen., 25, 146–57.
53. Kadyrov, M., Schmitz, C., Black, S., Kaufmann, P. and Huppertz, B. (2003). Pre-eclampsia and maternal anaemia display reduced apoptosis and opposite invasive phenotypes of extravillous trophoblast.Placenta, 24, 540–48.
54. Khong, T. Y., De Wolf, F., Robertson, W. B. and Brosens, I. (1986). Inadequate maternal vascular response to placentation in pregnancies complicated by preeclampsia and by small-for-gestational age infants.Br. J. Obstet. Gynaecol., 93, 1049–59.
55. King, B. F. and Blankenship, T. N. (1993). Expression of proliferating cell nuclear antigen (PCNA) in developing macaque placentas. Placenta, 14, A36.
56. King, B. F. and Blankenship, T. N. (1995). Neural cell adhesion molecule is present on macaque intra-arterial cytotrophoblast. Placenta, 16, A36.
57. King, A. and Loke, Y. W. (1988). Differential expression of blood-group-related carbohydrate antigens by trophoblast subpopulations. Placenta, 9, 513–21.
58. Kingdom, J. C. P. and Kaufmann, P. (1997). Oxygen and placental villous development: origins of fetal hypoxia.Placenta, 18, 613–21.
59. Kohnen, G., Kosanke, G., Korr, H. and Kaufmann, P. (1993). Comparison of various proliferation markers applied to human placental tissue. Placenta, 14, A38.
60. Korhonen, M., Ylanne, J., Laitnen, L., Cooper, H. N., Quaranta, V. and Virtanenen, I. (1991). Distribution of the a1–a6 integrin subunits in human developing and term placenta. Lab. Invest., 65, 347–56.
61. Kosanke, G. (1994). Proliferation, Wachstum und Differenzierung der Zottenba¨ume der menschlichen Placenta. Aachen: Verlag Shaker.
62. Kreis, T. and Vale, R. (1993). Guidebook to the Extracellular Matrix and Adhesion Proteins. Oxford: Oxford University Press.
63. Labarrere, C. and Faulk, W. P. (1995). Intercellular adhesion molecule-1 (ICAM-1) and HLA-DR antigens are expressed on endovascular cytotrophoblasts in abnormal pregnancies. Am. J. Reprod. Immunol., 33, 47–53.
64. Lala, P. K. and Graham, C. H. (1990). Mechanisms of trophoblast invasiveness and their control: the role of proteases and protease inhibitors. Cancer Metastasis Rev., 9, 369–79.
65. Lala, P. K. and Hamilton, G. S. (1996). Growth factors, proteases and protease inhibitors in the maternal–fetal dialogue. Placenta, 17, 545–55.
66. Larjava, H., Peltonen, J., Akiyama, S., Gralnik, H., Uitto, J. and Yamada, K. M. (1990). Novel functions for b1 integrins in keratinocyte cell–cell interactions. J. Cell Biol., 111, 803–185.
67. Leivo, I. P. L., Wahlström, T. and Engvall, E. (1989). Expression of merosin, a tissue specific basement membrane protein, in the intermediate trophoblast cells of choriocarcinoma and placenta. Lab. Invest., 60, 783–90.
68. Librach, C. L., Feigenbaum, S. L., Bass, K. E., et al. (1994). Interleukin-1 beta regulates human cytotrophoblast invasion in vitro. J. Biol. Chem., 269, 125–31.
69. Librach, C. L., Fisher, S. J., Fitgerald, M. L. and Damsky, C. H. (1991a). Cytotrophoblast–fibronectin and cytotrophoblast–laminin interactions have distinct roles in cytotrophoblast invasion. J. Cell Biol., 115, 6a.
70. Librach, C. L., Werb, Z., Fitzgerald, M. L., et al. (1991b). 92-kD type IV collagenase mediates invasion of human trophoblasts. J. Cell Biol., 113, 437–49.
71. Lim, K. H., Zhou, Y., Janatpour, M., et al. (1997). Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia. Am. J. Path., 151, 1809–18.
72. Lyall, F. (1998). Cell adhesion molecules: their role in pregnancy. Fetal Mat. Med. Rev., 10, 21–44.
73. Lyall, F. (2002). The human placental bed revisited.Placenta, 23, 555–62.
74. Lyall, F. (2003). Development of the uteroplacental circulation: the role of carbon monoxide and nitric oxide in trophoblast invasion and spiral artery transformation.Microscop. Res. Tech., 60, 402–11.
75. Lyall, F., Barber, A., Myatt, L., Bulmer, J. N. and Robson, S. C. (2000). Hemeoxygenase expression in human placenta and placental bed implies a role in regulation of trophoblast invasion and placental function. FASEB J., 14, 208–19.
76. Lyall, F., Bulmer, J. N., Duffie, E., Cousins, F., Theriault, E. A. and Robson, S. C. (2001a). Human trophoblast invasion and spiral artery transformation. The role of PECAM-1 in normal pregnancy, pre-eclampsia and fetal growth restriction. Am. J. Pathol., 158, 1713–21.
77. Lyall, F., Robson, S. C., Bulmer, J. N., Kelly, H. and Duffie, E. (1999). Human trophoblast invasion and spiral artery transformation: the role of nitric oxide.Am. J. Pathol., 154, 1105–14.
78. Lyall, F., Simpson, H., Robson, S. C., Bulmer, J. N. and Barber, A. (2001b). Transforming growth factor b expression in human placenta and placental bed in normal pregnancy, preeclampsia and fetal growth restriction. Am. J. Pathol., 159, 1827–38.
79. Lysiak, J. J., Hunt, J., Pringle, G. A. and Lala, P. K. (1995). Localization of transforming growth factor beta and its natural inhibitor decorin in the human placenta and decidua throughout gestation. Placenta, 16, 221–31.
80. MacCalman, C. D. and Chen, G. T. C. (1998). Type 2 cadherins in the human endometrium and placenta: their putative roles in human implantation and placentation.Am. J. Reprod. Immunol., 39, 96–107.
81. MacCalman, C. D., Omigbodum, A., Bronner, M. P. and Struass, J. F. (1995). Identification of the cadherins present in human placenta. J. Soc. Gynecol. Invest., 2, 146.
82. Maines, M. D. (1988). Heme oxygenase: function, multiplicity, regulatory mechanisms and clinical applications.FASEB J., 2, 2257–568.
83. Maines, M. D. (1993). Carbon monoxide: an emerging regulator of cGMP in the brain. Mol. Cell. Neurosci., 4, 389–97.
84. Maquoi, E., Polette, M., Nawrocki, B., et al. (1997). Expression of stromelysin-3 in the human placenta and placental bed. Placenta, 18, 277–85.
85. McMaster, M. T., Librach, C. L., Zhou, Y., et al. (1995). Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol., 154, 3771–8.
86. Meekins, J. W., Pijnenborg, R., Hanssens, M., McFadyen, I. R. and Van Assche, A. (1994). A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol., 101, 669–74.
87. Mould, P., Garratt, A. N., Askari, J. A., Akiyama, S. K. and Humphries, M. J. (1995). Identification of a novel anti-integrin monoclonal antibody that recognises a ligand-induced binding site epitope on the b1 subunit.FEBS Lett., 363, 118–22.
88. Moffett, A. and Loke, Y. W. (2004). The immunological paradox of pregnancy: a reappraisal. Placenta, 25, 1–8.
89. Mühlhauser, J., Crescimanno, C., Kaufmann, P., Höfler, H., Zaccheo, D. and Castellucci, M. (1993). Differentiation and proliferation patterns in human trophoblast revealed by c-erbB-2 oncogene product and EGR-R. J. Histochem. Cytochem., 41, 165–73.
90. Nanaev, A. K., Chwalisz, K., Frank, H. G., Kohnen, G., Hegele-Hartung, C. and Kaufmann, P. (1995). Physiological dilation of uteroplacental arteries in the guinea pig depends on nitric oxide synthase of extravillous trophoblast. Cell Tiss. Res., 282, 407–21.
91. Nawrocki, B., Polette, M., Marchand, V., et al. (1996). Membrane-type matrix metalloproteinase-1 expression at the site of human implantation. Placenta, 17, 565–72.
92. Nawrocki, B., Polette, M., Maquoi, E. and Birembaut, P. (1997). Expression of matrix metalloproteinases and their inhibitors during human placental development.Troph. Res., 10, 97–113.
93. O’Brien, M., Dausset, J., Carosella, E. D. and Moreau, P. (2000). Analysis of the role of HLA-G in preeclampsia.Hum. Immunol., 61, 1126–31.
94. Pepper, M. S. (1997). Transforming growth factor-beta: vasculogenesis and vessel wall integrity. Cytok. Growth Factor Rev., 8, 21–4.
95. Pijnenborg, R., Anthony, J., Davey, D. A., et al. (1991). Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br. J. Obstet. Gynaecol., 98, 648–55.
96. Pijnenborg, R., Bland, J. M., Robertson, W. B., Dixon, G. and Brosens I. (1981). The pattern of interstitial trophoblast invasion in early human pregnancy.Placenta, 2, 303–16.
97. Pijnenborg, R., Bland, J. M., Robertson, W. B. and Brosens, I. (1983). Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta, 4, 397–414.
98. Pijnenborg, R., Vercruysse, L., Verbist, L. and Van Assache, F. A. (1998). Interaction of interstitial trophoblast with placental bed capillaries and venules of normotensive and pre-eclamptic pregnancies. Placenta, 19, 569–75.
99. Polette, M., Nawrocki, B., Pintiaux, B., et al. (1994). Expression of gelatinases A and B and their tissue inhibitors by cells of early and term human placenta and gestational endometrium. Lab. Invest., 71, 838–46.
100. Rajakumar, A. and Conrad, K. P. (2000). Expression, ontogeny, and regulation of hypoxia-inducible transcription factors in the human placenta. Biol. Rep., 63, 559–69.
101. Rajakumar, A., Whitelock, K. A., Weissfeld, L. A., Daftary, A. R., Markovic, N. and Conrad, K. P. (2001a). Selective overexpression of the hypoxia-inducible transcription factor, HIF-2 alpha, in placentas from women with preeclampsia. Biol. Reprod., 64, 499–506.
102. Rajakumar, A., Whitelock, K. A., Weissfeld, L. A., Daftary, A. R., Markovic, N. and Conrad, K. P. (2001b). Erratum.Biol. Reprod., 64, 1019–20.
103. Robertson, W. B., Khong, T. Y., Brosens, I., De Wolf, F., Sheppard, B. L. and Bonnar, J. (1986). The placental bed biopsy: review from three European centres.Am. J. Obstet. Gynecol., 155, 401–12.
104. Rodesch, F., Simon, P., Donner, C. and Jauniaux, E. (1992). Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet. Gynecol., 80, 283–5.
105. Ruck, P., Marzusch, K., Krober, S., Horny, H.-P., Dietl, H. and Kaiserling, E. (1997). The distribution of tissue inhibitor of metalloproteinases-2 (TIMP-2) in decidua and trophoblast of early human pregnancy. Troph. Res., 10, 115–21.
106. Schaffer, L., Scheid, A., Spielmann, P., et al. (2003). Oxygen-regulated expression of TGF-beta 3, a growth factor involved in trophoblast differentiation. Placenta, 24, 941–50.
107. Selick, C. E., Horowitz, G. M., Gratch, M., Scott Jr, R. T., Navot, D. and Hofmann, G. E. (1994). Immunohistochemical localization of transforming growth factor-b in human implantation sites. J. Clin. Endocrinol. Metabol., 78, 592–6.
108. Semenza, G. L. (1998). Hypoxia-inducible factor-1 and the molecular physiology of oxygen homeostasis. J. Lab. Clin. Med., 131, 207–14.
109. Shi, W. L., Mognetti, B., Campana, A. and Bischof, P. (1995). Metalloproteinase secretion by endometrial leukocyte subsets. Am. J. Reprod. Immunol., 34, 299–310.
110. Simpson, H., Robson, S. C., Bulmer, J. N., Barber, A. and Lyall, F. (2002). Transforming growth factor b expression in human placenta and placental bed during early pregnancy. Placenta, 23, 44–58.
111. Taylor, C. M., Stevens, H., Anthony, F. W. and Wheeler, T. (1997). Influence of hypoxia on vascular endothelial growth factor and chorionic gonadotrophin production in trophoblast derived cell lines; JEG, Jar and BeWo.Placenta, 18, 451–8.
112. Thompson, C. B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science, 267, 1456–62.
113. Verma, A., Hirsch, D. J., Glatt, C. E., Ronnett, G. V. and Snyder, S. H. (1993). Carbon monoxide: a putative neural messenger. Science, 259, 381.
114. Vettraino, I. M., Roby, J., Tolley, T. and Parks, W. C. (1996). Collagenase-1, stromelysin-1 and matrilysin are expressed within the placenta during multiple stages of human pregnancy. Placenta, 17, 557–63.
115. Vicovac, L. and Aplin, J. (1996). Epithelial–mesenchymal transition during trophoblast differentiation. Acta Anat., 156, 202–16.
116. Vicovac, L., Jones, C. S. and Aplin, J. D. (1995). Trophoblast differentiation during formation of anchoring in a model of the early human placenta in vitro. Placenta, 16, 41–56.
117. Vuckovic, M., Genbacev, O. and Kumar, S. (1992). Immunolocalization of transforming growth factor beta in 1st and 3rd trimester human placenta. Pathobiology, 60, 149–50.
118. Winterhager, E., von Ostau, C., Grümmer, R., Kaufmann, P. and Fisher, S. J. (1996). Connexin and E-Cadherin Expression wa¨hrend der Differenzierung des humanen Trophoblasten. Ann. Anat., 178, 41.
119. Zakhary, R., Gaine, S. P., Dinerman, J. L., Ruat, M., Flavahan, N. A. and Snyder, S. H. (1996). Hemeoxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc. Natl Acad. Sci. USA, 93, 795–8.
120. Zhou, Y., Damsky, C. H., Chiu, K., Roberts, J. M. and Fisher, S. J. (1993). Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts. J. Clin. Invest., 91, 950–60.
121. Zhou, Y., Damsky, C. H. and Fisher, S. J. (1997b). Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype.J. Clin. Invest., 99, 2152–64.
122. Zhou, Y., Fisher, S. J., Janatpour, M., Genbacev, O., Dejana, E. and Wheelock, M. (1997a). Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion?J. Clin. Invest., 99, 2139–51.
123. Zhou, Y., Genbacev, O., Damsky, C. H. and Fisher, S. J. (1998). Oxygen regulates human cytotrophoblast differentiation and invasion: implications for endovascular invasion in normal pregnancy and in pre-eclampsia. J. Reprod. Immunol., 39, 197–213.
124. Zygmunt, M., Boving, B., Wienhard, J., et al. (1997). Expression of cell adhesion molecules in the extravillous trophoblast is altered in IUGR. Am. J. Reprod. Immunol., 38, 295–301.