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

from Part I - Basic science

Published online by Cambridge University Press:  03 September 2009

By
Fiona Lyall
Edited by
Fiona Lyall  and
Michael Belfort
Fiona Lyall
Affiliation:
University of Glasgow
Michael Belfort
Affiliation:
University of Utah
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Summary

Introduction: the placental bed

The placental bed underlies the fetal placenta and includes the decidua basalis and the underlying myometrium containing the uterine spiral arteries. In order to establish human hemochorial placentation and to provide a progressive increase in blood supply to the growing fetus, the placental bed spiral arteries must undergo considerable alterations. These physiological modifications are thought to be brought about by the interaction of invasive cytotrophoblast with the spiral artery vessel wall. Failure of spiral artery transformation is thought to play an important role in the sequence of events which gives rise to pre-eclampsia. The mechanisms that control human trophoblast invasion in normal, let alone abnormal pregnancy, are still poorly understood. This is partly due to difficulties in obtaining “true” placental bed biopsies.

Much of the information on the early physiological changes within the placental bed comes from unique studies on intact hysterectomy specimens (Pijnenborg et al., 1981) Details of trophoblast invasion during late pregnancy and in pregnancies complicated by pre-eclampsia and fetal growth restriction is principally derived from the study of placental bed biopsies taken at the time of Cesarean section. Placental bed biopsies may not be representative of the whole placental bed. To help circumvent this problem, multiple biopsies combined with large numbers of cases should help to provide a more representative picture. The entire blood vessel will not be present in a single biopsy, thus limiting our interpretation of what is happening along its full length.

Type
Chapter
Information
Pre-eclampsia
Etiology and Clinical Practice
 , pp. 20 - 36
Publisher: Cambridge University Press
Print publication year: 2007

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References

Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. and Watson, J. (1994). Molecular Biology of the Cell. New York: Garland Publishing Inc.Google Scholar
Alexander, C. and Werb, Z. (1991). Extracellular matrix degradation. In Cell Biology of the Extracellular Matrix, ed. Hay, E. New York: Plenum Press, pp. 255–302.CrossRefGoogle Scholar
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, 346–53.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Aplin, J. D. (1993). Expression of integrin α6β4 in human trophoblast and its loss from extravillous cells. Placenta, 14, 203–15.CrossRefGoogle ScholarPubMed
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.Google Scholar
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 α5β1. Biol. Reprod., 60, 828–38.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
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, 61–7.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
Birk, D. E., Silver, F. H. and Trelstad, R. L. (1991). Matrix assembly. In Cell Biology of Extracellular Matrix, ed. Hay, E.. New York: Plenum Press, pp. 221–54.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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. Wynn, R. M., vol. 4. New York: Appleton-Century-Crofts, pp. 177–91.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Caniggia, I., Grisaru-Gravnosky, S., Kuliszewsky, M., Post, M. and Lye, S. J. (1999). Inhibition of TGFBβ3restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies. J. Clin. Invest., 103, 1641–50.CrossRefGoogle ScholarPubMed
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-β3. J. Clin. Invest., 105, 577–87.CrossRefGoogle Scholar
Caniggia, I., Winter, J., Lye, S. J. and Post, M. (2000b). Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta, 21, S25–30.CrossRefGoogle Scholar
Carter, W. G. P., Kaur, S. G., Gil, P. J. and Wayer, E. A. (1990). Distinct functions for α3β1 in focal adhesions and α6/β4 bullous pemphigoid antigen in a new stabilising anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J. Cell Biol., 111, 3141–54.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.CrossRefGoogle Scholar
Church, H. J., Richards, A. J. and Aplin, J. D. (1997). Laminins in decidua, placenta and choriocarcinoma cells. Trophoblast Res., 143–62.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Coutifaris, C., Kao, L. C., Sehdev, H. M., et al. (1991). E-cadherin expression during the differentiation of human trophoblasts. Development, 113, 767–77.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Damsky, C. H., Librach, C., Lim, K.-H., et al. (1994). Integrin switching regulates normal trophoblast invasion. Development, 120, 3657–66.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
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.Google Scholar
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Genbacev, O., Zhou, Y., Ludlow, J. W. and Fisher, S. J. (1997). Regulation of human placental development by oxygen tension. Science, 277, 1669–72.CrossRefGoogle ScholarPubMed
Goldman-Wohl, D. S., Ariel, I., Greenfield, C., et al. (2000). Lack of human leucocyte antigen-G expression in extravillous trophoblast is associated with pre-eclampsia. Mol. Hum. Reprod., 6, 88–95.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Hulboy, D. L., Rudolf, L. A. and Matrisisan, L. M. (1997). Matrix metalloproteases as mediators of reproductive function. Mol. Hum. Reprod., 3, 27–45.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Huppertz, B. S., Kertschanska, S., Demir, A., Frank, H. G. and Kaufmann, P. (1998b). Production of membrane-type matrix metalloproteinase-1 (MT-MMP-1) in early human placenta: a possible role in placental implantation. Cell Tiss. Res., 291, 133–48.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Irving, J. A. and Lala, P. K. (1995). Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGFβ, IGF-II and IGFBP-1. Exp. Cell Res., 217, 419–27.CrossRefGoogle ScholarPubMed
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, 146–57.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Khong, T. Y., Wolf, F., Robertson, W. B. and Brosens, I. (1986). Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br. J. Obstet. Gynaecol., 93, 1049–59.CrossRefGoogle ScholarPubMed
King, B. F. and Blankenship, T. N. (1993). Expression of proliferating cell nuclear antigen (PCNA) in developing macaque placentas. Placenta, 14, A36.CrossRefGoogle Scholar
King, B. F. and Blankenship, T. N. (1995). Neural cell adhesion molecule is present on macaque intra-arterial cytotrophoblast. Placenta, 16, A36.Google Scholar
King, A. and Loke, Y. W. (1988). Differential expression of blood-group-related carbohydrate antigens by trophoblast subpopulations. Placenta, 9, 513–21.CrossRefGoogle ScholarPubMed
Kingdom, J. C. P. and Kaufmann, P. (1997). Oxygen and placental villous development: origins of fetal hypoxia. Placenta, 18, 613–21.CrossRefGoogle ScholarPubMed
Kohnen, G., Kosanke, G., Korr, H. and Kaufmann, P. (1993). Comparison of various proliferation markers applied to human placental tissue. Placenta, 14, A38.Google Scholar
Korhonen, M., Ylanne, J., Laitnen, L., Cooper, H. N., Quaranta, V. and Virtanenen, I. (1991). Distribution of the α1–α6 integrin subunits in human developing and term placenta. Lab. Invest., 65, 347–56.Google Scholar
Kosanke, G. (1994). Proliferation, Wachstum und Differenzierung der Zottenbäume der menschlichen Placenta. Aachen: Verlag Shaker.Google Scholar
Kreis, T. and Vale, R. (1993). Guidebook to the Extracellular Matrix and Adhesion Proteins. Oxford: Oxford University Press.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Lala, P. K. and Hamilton, G. S. (1996). Growth factors, proteases and protease inhibitors in the maternal–fetal dialogue. Placenta, 17, 545–55.CrossRefGoogle ScholarPubMed
Larjava, H., Peltonen, J., Akiyama, S., Gralnik, H., Uitto, J. and Yamada, K. M. (1990). Novel functions for β1 integrins in keratinocyte cell–cell interactions. J. Cell Biol., 111, 803–185.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
Lyall, F. (1998). Cell adhesion molecules: their role in pregnancy. Fetal Mat. Med. Rev., 10, 21–44.CrossRefGoogle Scholar
Lyall, F. (2002). The human placental bed revisited. Placenta, 23, 555–62.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Lyall, F., Simpson, H., Robson, S. C., Bulmer, J. N. and Barber, A. (2001b). Transforming growth factor β expression in human placenta and placental bed in normal pregnancy, preeclampsia and fetal growth restriction. Am. J. Pathol., 159, 1827–38.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Maines, M. D. (1988). Heme oxygenase: function, multiplicity, regulatory mechanisms and clinical applications. FASEB J., 2, 2257–568.CrossRefGoogle ScholarPubMed
Maines, M. D. (1993). Carbon monoxide: an emerging regulator of cGMP in the brain. Mol. Cell. Neurosci., 4, 389–97.CrossRefGoogle Scholar
Maquoi, E., Polette, M., Nawrocki, B., et al. (1997). Expression of stromelysin-3 in the human placenta and placental bed. Placenta, 18, 277–85.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Meekins, J. W., Pijnenborg, R., Hanssens, M., McFadyen, I. R. and 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.CrossRefGoogle ScholarPubMed
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 β1 subunit. FEBS Lett., 363, 118–22.CrossRefGoogle Scholar
Moffett, A. and Loke, Y. W. (2004). The immunological paradox of pregnancy: a reappraisal. Placenta, 25, 1–8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Pepper, M. S. (1997). Transforming growth factor-beta: vasculogenesis and vessel wall integrity. Cytok. Growth Factor Rev., 8, 21–4.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Pijnenborg, R., Vercruysse, L., Verbist, L. and Assache, F. A. (1998). Interaction of interstitial trophoblast with placental bed capillaries and venules of normotensive and pre-eclamptic pregnancies. Placenta, 19, 569–75.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Rajakumar, A., Whitelock, K. A., Weissfeld, L. A., Daftary, A. R., Markovic, N. and Conrad, K. P. (2001b). Erratum. Biol. Reprod., 64, 1019–20.Google Scholar
Robertson, W. B., Khong, T. Y., Brosens, I., 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.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Selick, C. E., Horowitz, G. M., Gratch, M., Scott, R. T. Jr, Navot, D. and Hofmann, G. E. (1994). Immunohistochemical localization of transforming growth factor-β in human implantation sites. J. Clin. Endocrinol. Metabol., 78, 592–6.Google ScholarPubMed
Semenza, G. L. (1998). Hypoxia-inducible factor-1 and the molecular physiology of oxygen homeostasis. J. Lab. Clin. Med., 131, 207–14.CrossRefGoogle ScholarPubMed
Shi, W. L., Mognetti, B., Campana, A. and Bischof, P. (1995). Metalloproteinase secretion by endometrial leukocyte subsets. Am. J. Reprod. Immunol., 34, 299–310.CrossRefGoogle ScholarPubMed
Simpson, H., Robson, S. C., Bulmer, J. N., Barber, A. and Lyall, F. (2002). Transforming growth factor β expression in human placenta and placental bed during early pregnancy. Placenta, 23, 44–58.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Thompson, C. B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science, 267, 1456–62.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Vicovac, L. and Aplin, J. (1996). Epithelial–mesenchymal transition during trophoblast differentiation. Acta Anat., 156, 202–16.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Winterhager, E., Ostau, C., Grümmer, R., Kaufmann, P. and Fisher, S. J. (1996). Connexin and E-Cadherin Expression während der Differenzierung des humanen Trophoblasten. Ann. Anat., 178, 41.Google Scholar
Zakhary, R., Gaine, S. P., Dinerman, J. L., Ruat, M., Flavahan, N. A. and Snyder, S. H. (1996). Heme-oxygenase 2: endothelial and neuronal localization and role in endothelium-dependent relaxation. Proc. Natl Acad. Sci. USA, 93, 795–8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed

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