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Vascular Morphogenesis in the Female Reproductive System pp 315–326Cite as

Birkhäuser

Early Placental Vascular Morphogenesis

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Part of the book series: Cardiovascular Molecular Morphogenesis ((CARDMM))

Abstract

Survival of the eutherian embryo/fetus depends on formation of a transient but vital organ, the placenta. This process, termed placentation, is the first test of the embryo’s differentiative and organogenesis capacity. It has two goals: attaching the conceptus to the uterus, and bringing the fetal and maternal circulations into close proximity to facilitate effective gas and nutrient/waste exchange. These functions require that fetal placental cells (trophoblasts) acquire an invasive phenotype. In mammals that form a hemochorial placenta (e.g., humans and mice), fetal trophoblasts come in direct contact with maternal blood. Thus, placentation also entails the unique requirement for close cooperation and direct cellular contact between two immunologically distinct organisms.

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References

  • Alexander, C. M., Hansell, E. J., Behrendtsen, O., Flannery, M. L., Kishnani, N. S., Hawkes, S. P., and Werb, Z. 1996. Expression and function of matrix metalloproteinases and their inhibitors at the maternal-embryonic boundary during mouse embryo implantation. Development 122:1723–1736.

    PubMed  CAS  Google Scholar 

  • Austgulen, R., Lien, E., Vince, G., and Redman, C. W. 1997. Increased maternal plasma levels of soluble adhesion molecules ICAM-1, VCAM-1, E-selectin in preeclampsia. Fur. J. Obstet. Gynecol. Reprod. Biol. 71:53–58.

    Article  CAS  Google Scholar 

  • Bass, K. E., Li, H., Hawkes, S. P., Howard, E., Bullen, E., Vu, T. K., McMaster, M.,Janatpour, M., and Fisher, S. J. 1997. Tissue inhibitor of metalloproteinase-3 expressionis upregulated during human cytotrophoblast invasion in vitro. Dey. Genet. 21:61–67.

    CAS  Google Scholar 

  • Berg, C. J., Atrash, H. K., Koonin, L. M., and Tucker, M. 1996. Pregnancy-related mortal-ity in the United States, 1987–1990. Obstet. Gynecol. 88:161–167.

    Article  PubMed  CAS  Google Scholar 

  • Birchmeier, C., Bladt, F., and Yamaai, T. 1997. The functions of HGF/SF and its receptor, the c-Met tyrosine kinase, in mammalian development. Ciba Found. Symp. 212:169–182.

    PubMed  CAS  Google Scholar 

  • Blankenship, T. N., and Enders, A. C. 1997a. Expression of platelet-endothelial cell adhesion molecule-1 PECAM by macaque trophoblast cells during invasion of the spiral arteries. Anat. Rec. 247:413–419.

    Article  CAS  Google Scholar 

  • Blankenship, T. N., and Enders, A. C. 1997b. Trophoblast cell-mediated modifications to uterine spiral arteries during early gestation in the macaque. Acta Anat. Basel 158:227–236.

    Article  CAS  Google Scholar 

  • Blankenship, T. N., Enders, A. C., and King, B. F. 1993. Trophoblastic invasion and the development of uteroplacental arteries in the macaque: immunohistochemical localization of cytokeratins, desmin, type IV collagen, laminin, and fibronectin. Cell Tissue Res. 272:227–236.

    Article  PubMed  CAS  Google Scholar 

  • Blankenship, T. N., and King, B. F. 1996. Macaque intra-arterial trophoblast and extravillous trophoblast of the cell columns and cytotrophoblastic shell express neural cell adhesion molecule NCAM. Anat. Rec. 245:525–531.

    Article  PubMed  CAS  Google Scholar 

  • Brosens, I. A., Robertson, W. B., and Dixon, H. G. 1972. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet. Gynecol. Annu. 1:177–191.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Cao, Y., Linden, P., Shima, D., Browne, F., and Folkman, J. 1996. In vivo angiogenic activity and hypoxia induction of heterodimers of placenta growth factor/vascular endothelial growth factor. J. Clin. Invest. 98:2507–2511.

    Article  PubMed  CAS  Google Scholar 

  • Charnock-Jones, D. S., Sharkey, A. M., Boocock, C. A., Ahmed, A., Plevin, R., Ferrara, N., and Smith, S. K. 1994. Vascular endothelial growth factor receptor localization and activation in human trophoblast and choriocarcinoma cells. Biol. Reprod. 51:524–530.

    Article  PubMed  CAS  Google Scholar 

  • Cheung, C. Y. 1997. Vascular endothelial growth factor: possible role in fetal development and placental function. J. Soc. Gynecol. Invest. 4:169–177.

    Article  CAS  Google Scholar 

  • Cross, J. C., Werb, Z., and Fisher, S. J. 1994. Implantation and the placenta: key pieces of the development puzzle. Science 266:1508–1518.

    Article  PubMed  CAS  Google Scholar 

  • Damsky, C. H., Fitzgerald, M. L., and Fisher, S. J. 1992. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Invest. 89:210–222.

    Article  PubMed  CAS  Google Scholar 

  • Damsky, C. H., Librach, C., Lim, K. H., Fitzgerald, M. L., McMaster, M. T., Janatpour, M., Zhou, Y., Logan, S. K., and Fisher, S. J. 1994. Integrin switching regulates normal trophoblast invasion. Development 120:3657–3666.

    PubMed  CAS  Google Scholar 

  • Davis, S., Aldrich, T. H., Jones, P. F., Acheson, A., Compton, D. L., Jain, V., Ryan, T. E., Bruno, J., Radziejewski, C., Maisonpierre, P. C., and Yancopoulos, G. D. 1996. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87:1161–1169.

    Article  PubMed  CAS  Google Scholar 

  • Dumont, D. J., Fong, G. H., Puri, M. C., Gradwohl, G., Alitalo, K., and Breitman, M. L. 1995. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev. Dyn. 203:80–92.

    Article  PubMed  CAS  Google Scholar 

  • Fisher, S. J., Cui, T. Y., Zhang, L., Hartman, L., Grahl, K., Zhang, G. Y., Tarpey, J., and Damsky, C. H. 1989. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J. Cell Biol. 109:891–902.

    Article  PubMed  CAS  Google Scholar 

  • Friesel, R. E., and Maciag, T. 1995. Molecular mechanisms of angiogenesis: fibroblast growth factor signal transduction. FASEB J. 9:919–925.

    PubMed  CAS  Google Scholar 

  • 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. 97:540–550.

    Article  PubMed  CAS  Google Scholar 

  • Genbacev, O., Zhou, Y., Ludlow, J. W., and Fisher, S. J. 1997. Regulation of human placental development by oxygen tension. Science 277:1669–1672.

    Article  PubMed  CAS  Google Scholar 

  • Guillemot, F., Nagy, A., Auerbach, A., Rossant, J., and Joyner, A. L. 1994. Essential role of Mash-2 in extraembryonic development. Nature 371:333–336.

    Article  PubMed  CAS  Google Scholar 

  • Gurtner, G. C., Davis, V., Li, H., McCoy, M. J., Sharpe, A., and Cybulsky, M. I. 1995. Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 9:1–14.

    Article  PubMed  CAS  Google Scholar 

  • Hamilton, W. J., and Boyd, J. D. 1966. Trophoblast in human utero-placental arteries. Nature 212:906–908.

    Article  Google Scholar 

  • Iruela-Arispe, M. L., and Dvorak, H. F. 1997. Angiogenesis: a dynamic balance of stimulators and inhibitors. Thromb. Haemost. 78:672–677.

    PubMed  CAS  Google Scholar 

  • Izumi, S., Slayden, O. D., Rubin, J. S., and Brenner, R. M. 1996. Keratinocyte growth factor and its receptor in the rhesus macaque placenta during the course of gestation. Placenta 17:123–135.

    Article  PubMed  CAS  Google Scholar 

  • Jaffe, R., Jauniaux, E., and Hustin, J. 1997. Maternal circulation in the first-trimester human placenta-myth or reality? Am. J. Obstet. Gynecol. 176:695–705.

    Article  PubMed  CAS  Google Scholar 

  • Kalousek, D. K., and Vekemans, M. 1996. Confined placental mosaicism. J. Med. Genet. 33:529–533.

    Article  PubMed  CAS  Google Scholar 

  • Konijnenberg, A., Stokkers, E. W., van der Post, J. A., Schaap, M. C., Boer, K., Bleker, O. P., and Sturk, A. 1997. Extensive platelet activation in preeclampsia compared with normal pregnancy: enhanced expression of cell adhesion molecules. Am. J. Obstet. Gynecol. 176:461–469.

    Article  PubMed  CAS  Google Scholar 

  • Kozak, K. R., Abbott, B., and Hankinson, O. 1997. ARNT-deficient mice and placental differentiation. Dev. Biol. 191:297–305.

    Article  PubMed  CAS  Google Scholar 

  • Krauss, T., Kuhn, W., Lakoma, C., and Augustin, H. G. 1997. Circulating endothelial cell adhesion molecules as diagnostic markers for the early identification of pregnant women at risk for development of preeclampsia. Am. J. Obstet. Gynecol. 177:443–449.

    Article  PubMed  CAS  Google Scholar 

  • Kwee, L., Baldwin, H. S., Shen, H. M., Stewart, C. L., Buck, C., Buck, C. A., and Labow, M. A. 1995. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule. Development 121:489–503.

    PubMed  CAS  Google Scholar 

  • Kyriakides, T. R., Zhu, Y. H., Smith, L. T., Bain, S. D., Yang, Z., Lin, M. T., Danielson, K. G., Iozzo, R. V., LaMarca, M., McKinney, C. E., Ginns, E. I., and Bornstein, P. 1998. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J. Cell Biol. 140:419–430.

    Article  PubMed  CAS  Google Scholar 

  • Levine, R. J., Hauth, J. C., Curet, L. B., Sibai, B. M., Catalano, P. M., Morris, C. D., DerSimonian, R., Esterlitz, J. R., Raymond, E. G., Bild, D. E., Clemens, J. D., and Cutler, J. A. 1997. Trial of calcium to prevent preeclampsia. N. Engl. J. Med. 337:69–76.

    Article  PubMed  CAS  Google Scholar 

  • Librach, C. L., Werb, Z., Fitzgerald, M. L., Chiu, K., Corwin, N. M., Esteves, R. A., Grobelny, D., Galardy, R., Damsky, C. H., and Fisher, S. J. 1991. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J. Cell Biol. 113:437–449.

    Article  PubMed  CAS  Google Scholar 

  • Lim, K. H., Zhou, Y., Janatpour, M., McMaster, M., Bass, K., Chun, S. H., and Fisher, S. J. 1997. Human cytotrophoblast differentiation/invasion is abnormal in preeclampsia. Am. J. Pathol. 151:1809–1818.

    PubMed  CAS  Google Scholar 

  • Lyall, F., Greer, I. A., Boswell, F., Macara, L. M., Walker, J. J., and Kingdom, J. C. 1994. The cell adhesion molecule, VCAM-1, is selectively elevated in serum in preeclampsia: does this indicate the mechanism of leucocyte activation? Br. J. Obstet. Gynaecol. 101:485–487.

    Article  PubMed  CAS  Google Scholar 

  • MacCalman, C. D., Furth, E. E., Omigbodun, A., Bronner, M., Coutifaris, C., and Strauss, J. F. R. 1996. Regulated expression of cadherin-11 in human epithelial cells: a role for cadherin-11 in trophoblast-endometrium interactions? Dev. Dyn. 206:201–211.

    Article  PubMed  CAS  Google Scholar 

  • Monkley, S. J., Delaney, S. J., Pennisi, D. J., Christiansen, J. H., and Wainwright, B. J. 1996. Targeted disruption of the Wnt2 gene results in placentation defects. Development 122:3343–3353.

    PubMed  CAS  Google Scholar 

  • Nakayama, H., Liu, Y., Stifani, S., and Cross, J. C. 1997. Developmental restriction of Mash-2 expression in trophoblast correlates with potential activation of the notch-2 pathway. Dev. Genet. 21:21–30.

    Article  PubMed  CAS  Google Scholar 

  • Navarro, P., Ruco, L., and Dejana, E. 1998. Differential localization of VE- and Ncadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J. Cell Biol. 140:1475–1484.

    Article  PubMed  CAS  Google Scholar 

  • Ness, R. B., and Roberts, J. M. 1996. Heterogeneous causes constituting the single syndrome of preeclampsia: a hypothesis and its implications. Am. J. Obstet. Gynecol. 175:1365–1370.

    Article  PubMed  CAS  Google Scholar 

  • O’Reilly, M. S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W. S., Flynn, E., Birkhead, J. R., Olsen, B. R., and Folkman, J. 1997. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 88:277–285.

    Article  PubMed  Google Scholar 

  • O’Reilly, M. S., Holmgren, L., Chen, C., and Folkman, J. 1996. Angiostatin induces and sustains dormancy of human primary tumors in mice. Nat. Med. 2:689–692.

    Article  PubMed  Google Scholar 

  • Proll, J., Blaschitz, A., Hartmann, M., Thalhamer, J., and Dohr, G. 1996. Human first-trimester placenta intra-arterial trophoblast cells express the neural cell adhesion molecule. Early Pregnancy 2:271–275.

    PubMed  CAS  Google Scholar 

  • Queenan, J. T., Jr., Kao, L. C., Arboleda, C. E., Ulloa-Aguirre, A., Golos, T. G., Cines, D. B., and Strauss, J. F. D. 1987. Regulation of urokinase-type plasminogen activator production by cultured human cytotrophoblasts. J. Biol. Chem. 262:10903–10906.

    PubMed  CAS  Google Scholar 

  • Ramsey, E. M., Houston, M. L., and Harris, J. W. 1976. Interactions of the trophoblast and maternal tissues in three closely related primate species. Am. J. Obstet. Gynecol. 124:647–652.

    PubMed  CAS  Google Scholar 

  • Redman, C. W. 1990. Platelets and the beginnings of preeclampsia. N. Engl. J. Med. 323:478–480.

    Article  PubMed  CAS  Google Scholar 

  • Rinkenberger, J. L., Cross, J. C., and Werb, Z. 1997. Molecular genetics of implantation in the mouse. Dev. Genet. 21:6–20.

    Article  PubMed  CAS  Google Scholar 

  • Risau, W. 1997. Mechanisms of angiogenesis. Nature 386:671–674.

    Article  PubMed  CAS  Google Scholar 

  • Robb, L., Li, R., Hartley, L., Nandurkar, H. H., Koentgen, F., and Begley, C. G. 1998. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat. Med. 4:303–308.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, J. M., and Redman, C. W. 1993. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet 341:1447–1451.

    Article  PubMed  CAS  Google Scholar 

  • Roberts, J. M., Taylor, R. N., Musci, T. J., Rodgers, G. M., Hubel, C. A., and McLaughlin, M. K. 1989. Preeclampsia: an endothelial cell disorder. Am. J. Obstet. Gynecol. 161:1200–1204.

    PubMed  CAS  Google Scholar 

  • Rodesch, E, Simon, P., Donner, C., and Jauniaux, E. 1992. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet. Gynecol. 80:283–285.

    PubMed  CAS  Google Scholar 

  • Senger, D. R., Claffey, K. P., Benes, J. E., Perruzzi, C. A., Sergiou, A. P., and Detmar, M. 1997. Angiogenesis promoted by vascular endothelial growth factor: regulation through alphalbetal and alpha2betal integrins. Proc. Natl. Acad. Sri. USA 94:13612–13617.

    Article  CAS  Google Scholar 

  • Shih, I. M., and Kurman, R. J. 1996. Expression of melanoma cell adhesion molecule in intermediate trophoblast. Lab. Invest. 75:377–388.

    PubMed  CAS  Google Scholar 

  • Shore, V. H., Wang, T. H., Wang, C. L., Torry, R. J., Caudle, M. R., and Torry, D. S. 1997. Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 18:657–665.

    Article  PubMed  CAS  Google Scholar 

  • Starkey, P. M., Sargent, I. L., and Redman, C. W. 1988. Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 65:129–134.

    PubMed  CAS  Google Scholar 

  • Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., Sato, T. N., and Yancopoulos, G. D. 1996. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171–1180.

    Article  PubMed  CAS  Google Scholar 

  • Taylor, R. N., Crombleholme, W. R., Friedman, S. A., Jones, L. A., Casal, D. C., and Roberts, J. M. 1991. High plasma cellular fibronectin levels correlate with biochemical and clinical features of preeclampsia but cannot be attributed to hypertension alone. Am. J. Obstet. Gynecol. 165:895–901.

    PubMed  CAS  Google Scholar 

  • Uehara, Y., Minowa, O., Mori, C., Shiota, K., Kuno, J., Noda, T., and Kitamura, N. 1995. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 6516:702–705.

    Article  Google Scholar 

  • Vicovac, L., Jones, C. J., and Aplin, J. D. 1995. Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta 16:41–56.

    Article  PubMed  CAS  Google Scholar 

  • Volpert, O. V., Lawler, J., and Bouck, N. P. 1998. A human fibrosarcoma inhibits systemic angiogenesis and the growth of experimental metastases via thrombospondin-1. Proc. Natl. Acad. Sci. USA 95:6343–6348.

    Article  PubMed  CAS  Google Scholar 

  • Vuorela, P., Hatva, E., Lymboussaki, A., Kaipainen, A., Joukov, V., Persico, M. G., Alitalo, K., and Halmesmeaki, E. 1997. Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol. Reprod. 56:489–494.

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto, H., Flannery, M. L., Kupriyanov, S., Pearce, J., McKercher, S. R., Henkel, G. W, Maki, R. A., Werb, Z., and Oshima, R. G. 1998. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12:1315–1326.

    Article  PubMed  CAS  Google Scholar 

  • Yancopoulos, G. D., Klagsbrun, M., and Folkman, J. 1998. Vasculogenesis, angiogenesis, and growth factors: ephrins enter the fray at the border. Cell 93:661–664.

    Article  PubMed  CAS  Google Scholar 

  • Yang, J. T., Rayburn, H., and Hynes, R. O. 1995. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121:549–560.

    PubMed  CAS  Google Scholar 

  • 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. 91:950–960.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, Y., Damsky, C. H., and Fisher, S. J. 1997a. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J. Clin. Invest. 99:2152–2164.

    Article  CAS  Google Scholar 

  • Zhou, Y., Fisher, S. J., Janatpour, M., Genbacev, O., Dejana, E., Wheelock, M., and Damsky, C. H. 1997b. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest. 99:2139–2151.

    Article  CAS  Google Scholar 

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Authors
  1. Caroline H. Damsky
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  2. Susan J. Fisher
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Editors and Affiliations

  1. Department of Vascular Biology and Angiogenesis Research, Tumor Biology Center, Freiburg, D-79106, Germany

    Hellmut G. Augustin

  2. Department of Obstetrics and Gynaecology, Monash Medical Centre, Victoria, 3168, Australia

    Peter A. W. Rogers

  3. Molecular Biology Institute, University of California, Los Angeles, CA, 90095-1570, USA

    M. Luisa Iruela-Arispe

  4. Department of Obstetrics and Gynaecology, Rosie Maternity Hospital, Cambridge, CB2 2SW, England

    Stephen K. Smith

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Damsky, C.H., Fisher, S.J. (2001). Early Placental Vascular Morphogenesis. In: Augustin, H.G., Rogers, P.A.W., Iruela-Arispe, M.L., Smith, S.K. (eds) Vascular Morphogenesis in the Female Reproductive System. Cardiovascular Molecular Morphogenesis. Birkhäuser, Boston, MA. https://doi.org/10.1007/978-1-4612-0213-4_17

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  • DOI: https://doi.org/10.1007/978-1-4612-0213-4_17

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