Theriogenology
Volume 73, Issue 6 , Pages 817-827 , 1 April 2010

How to study placental vascular development?

  • F. Herr

      Affiliations

    • Department of Obstetrics and Gynecology, University of Greifswald, Greifswald, Germany
  • ,
  • N. Baal

      Affiliations

    • Department of Obstetrics and Gynecology, University of Giessen, Giessen, Germany
  • ,
  • R. Widmer-Teske

      Affiliations

    • Department of Obstetrics and Gynecology, University of Greifswald, Greifswald, Germany
  • ,
  • T. McKinnon

      Affiliations

    • Department of Obstetrics and Gynecology, University of Giessen, Giessen, Germany
  • ,
  • M. Zygmunt

      Affiliations

    • Department of Obstetrics and Gynecology, University of Greifswald, Greifswald, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 3834 866500; fax: +49 3834 866501.

Received 28 July 2009 ,Accepted 29 October 2009.

References 

  1. Barker DJ. Fetal growth and adult disease. Br J Obstet Gynaecol. 1992;99:275–276
  2. Valladares E, Peña R, Ellsberg M, Persson LA, Högberg U. Neuroendocrine response to violence during pregnancy—impact on duration of pregnancy and fetal growth. Acta Obstet Gynecol Scand. 2009;88:818–823
  3. Reynolds LP, Killilea SD, Redmer DA. Angiogenesis in the female reproductive system. FASEB J. 1992;6:886–892
  4. Zygmunt M, Herr F, Münstedt K, Lang U, Liang OD. Angiogenesis and vasculogenesis in pregnancy. Eur J Obstet Gynecol Reprod Biol. 2003;110(Suppl 1):10–18
  5. Ilancheran S, Moodley Y, Manuelpillai U. Human fetal membranes: a source of stem cells for tissue regeneration and repair?. Placenta. 2009;30:2–10
  6. Kaufmann P, Black S, Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod. 2003;69:1–7
  7. Demir R, Kayisli UA, Cayli S, Huppertz B. Sequential steps during vasculogenesis and angiogenesis in the very early human placenta. Placenta. 2006;27:535–539
  8. Kingdom J, Huppertz B, Seaward G, Kaufmann P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol. 2000;92:35–43
  9. Anson-Cartwright L, Dawson K, Holmyard D, Fisher SJ, Lazzarini RA, Cross JC. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet. 2000;25:311–314
  10. Kaufmann P, Mayhew TM, Charnock-Jones DS. Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta. 2004;25:114–126
  11. Demir R, Kaufmann P, Castellucci M, Erbengi T, Kotowski A. Fetal vasculogenesis and angiogenesis in human placental villi. Acta Anat (Basel). 1989;136:190–203
  12. Downs KM, Gifford S, Blahnik M, Gardner RL. Vascularization in the murine allantois occurs by vasculogenesis without accompanying erythropoiesis. Development. 1998;125:4507–4520
  13. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653–660
  14. Kacemi A, Vervelle C, Uzan S, Challier JC. Immunostaining of vascular, perivascular cells and stromal components in human placental villi. Cell Mol Biol (Noisy-le-grand). 1999;45:101–113
  15. Charnock-Jones DS, Kaufmann P, Mayhew TM. Aspects of human fetoplacental vasculogenesis and angiogenesis. I. Molecular regulation. Placenta. 2004;25:103–113
  16. Demir R, Kayisli UA, Seval Y, Celik-Ozenci C, Korgun ET, Demir-Weusten AY, et al. Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta. 2004;25:560–572
  17. Seval Y, Korgun ET, Demir R. Hofbauer cells in early human placenta: possible implications in vasculogenesis and angiogenesis. Placenta. 2007;28:841–845
  18. Zygmunt M, Herr F, Keller-Schoenwetter S, Kunzi-Rapp K, Münstedt K, Rao CV, et al. Characterization of human chorionic gonadotropin as a novel angiogenic factor. J Clin Endocrinol Metab. 2002;87:5290–5296
  19. Herr F, Liang OD, Herrero J, Lang U, Preissner KT, Han VK, et al. Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy. J Clin Endocrinol Metab. 2003;88:4811–4817
  20. Liang OD, Korff T, Eckhardt J, Rifaat J, Baal N, Herr F, et al. Oncodevelopmental alpha-fetoprotein acts as a selective proangiogenic factor on endothelial cell from the fetomaternal unit. J Clin Endocrinol Metab. 2004;89:1415–1422
  21. Jauniaux E, Watson A, Ozturk O, Quick D, Burton G. In-vivo measurement of intrauterine gases and acid-base values early in human pregnancy. Hum Reprod. 1999;14:2901–2904
  22. Takizawa T, Eguchi H, Namimatsu S, Jeschke U, Fuchs R, Robinson JM. Histochemistry for placenta research: theory and application. J Nippon Med Sch. 2007;74:268–273
  23. Nuovo G. The utility of immunohistochemistry and in situ hybridization in placental pathology. Arch Pathol Lab Med. 2006;130:979–983
  24. Castellucci M, Kaufmann P. A three-dimensional study of the normal human placental villous core: II. Stromal architecture. Placenta. 1982;3:269–286
  25. Mayhew TM. Stereology and the placenta: where's the point? – a review. Placenta. 2006;27(Suppl A):17–25
  26. Mayhew TM. Quantifying immunogold localization patterns on electron microscopic thin sections of placenta: recent developments. Placenta. 2009;30:565–570
  27. Langheinrich AC, Wienhard J, Vormann S, Hau B, Bohle RM, Zygmunt M. Analysis of the fetal placental vascular tree by X-ray micro-computed tomography. Placenta. 2004;25:95–100
  28. Langheinrich AC, Vorman S, Seidenstücker J, Kampschulte M, Bohle RM, Wienhard J, et al. Quantitative 3D micro-CT imaging of the human feto-placental vasculature in intrauterine growth restriction. Placenta. 2008;29:937–941
  29. Bergmann A, Zygmunt M, Clapp JF. Running throughout pregnancy: effect on placental villous vascular volume and cell proliferation. Placenta. 2004;25:694–698
  30. Kadyrov M, Kosanke G, Kingdom J, Kaufmann P. Increased fetoplacental angiogenesis during first trimester in anaemic women. Lancet. 1998;352:1747–1749
  31. Todros T, Sciarrone A, Piccoli E, Guiot C, Kaufmann P, Kingdom J. Umbilical Doppler waveforms and placental villous angiogenesis in pregnancies complicated by fetal growth restriction. Obstet Gynecol. 1999;93:499–503
  32. Kingdom JC, Burrell SJ, Kaufmann P. Pathology and clinical implications of abnormal umbilical artery Doppler waveforms. Ultrasound Obstet Gynecol. 1997;9:271–286
  33. Mayhew TM. Fetoplacental angiogenesis during gestation is biphasic, longitudinal and occurs by proliferation and remodelling of vascular endothelial cells. Placenta. 2002;23:742–750
  34. Mayhew TM, Charnock-Jones DS, Kaufmann P. Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies. Placenta. 2004;25:127–139
  35. Bárcena A, Kapidzic M, Muench MO, Gormley M, Scott MA, Weier JF, et al. The human placenta is a hematopoietic organ during the embryonic and fetal periods of development. Dev Biol. 2009;327:24–33
  36. Carter AM. Animal models of human placentation—a review. Placenta. 2007;(Suppl A):41–47
  37. Miglino MA, Ambrósio CE, dos Santos Martins D, Wenceslau CV, Pfarrer C, Leiser R. The carnivore pregnancy: the development of the embryo and fetal membranes. Theriogenology. 2006;66:1699–1702
  38. Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta. 2002;23:3–19
  39. Cox B, Kotlyar M, Evangelou AI, Ignatchenko V, Ignatchenko A, Whiteley K, et al. Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol. 2009;279:1–15
  40. Carlström M, Wentzel P, Skøtt O, Persson AE, Eriksson UJ. Angiogenesis inhibition causes hypertension and placental dysfunction in a rat model of preeclampsia. J Hypertens. 2009;27:829–837
  41. Leiser R, Kaufmann P. Placental structure: in a comparative aspect. Exp Clin Endocrinol. 1994;102:122–134
  42. Zeiler M, Leiser R, Johnson GA, Tinneberg HR, Pfarrer C. Development of an in vitro model for bovine placentation: a comparison of the in vivo and in vitro expression of integrins and components of extracellular matrix in bovine placental cells. Cells Tissues Organs. 2007;186:229–242
  43. Baal N, Reisinger K, Jahr H, Bohle RM, Liang O, Münstedt K, et al. Expression of transcription factor Oct-4 and other embryonic genes in CD133 positive cells from human umbilical cord blood. Thromb Haemost. 2004;92:767–775
  44. Cohen M, Bischof P. Coculture of decidua and trophoblast to study proliferation and invasion. Methods Mol Biol. 2009;550:63–72
  45. Wang R, Clark R, Bautch VL. Embryonic stem cell-derived cystic embryoid bodies form vascular channels: an in vitro model of blood vessel development. Development. 1992;114:303–316
  46. Hirashima M, Kataoka H, Nishikawa S, Matsuyoshi N, Nishikawa S. Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood. 1999;93:1253–1263
  47. Miller RK, Genbacev O, Turner MA, Aplin JD, Caniggia I, Huppertz B. Human placental explants in culture: approaches and assessments. Placenta. 2005;26:439–448
  48. Campbell S, Park JH, Rowe J, Seeho SK, Morris JM, Gallery ED. Chorionic villus sampling as a source of trophoblasts. Placenta. 2007;28:1118–1122
  49. Pauly RR, Passaniti A, Crow M, Kinsella JL, Papadopoulos N, Monticone R, et al. Experimental models that mimic the differentiation and dedifferentiation of vascular cells. Circulation. 1992;86(Suppl III):68–73
  50. Barnés CM, Huang S, Kaipainen A, Sanoudou D, Chen EJ, Eichler GS, et al. Evidence by molecular profiling for a placental origin of infantile hemangioma. Proc Natl Acad Sci U S A. 2005;102:19097–19102
  51. Librach CL, Werb Z, Fitzgerald ML, Chiu K, Corwin NM, Esteves RA, et al. 92-kD type IV collagenase mediates invasion of human cytotrophoblasts. J Cell Biol. 1991;113:437–449
  52. Delia D, Lampugnani MG, Resnati M, Dejana E, Aiello A, Fontanella E, et al. CD34 expression is regulated reciprocally with adhesion molecules in vascular endothelial cells in vitro. Blood. 1993;81:1001–1008
  53. Bates RC, Buret A, van Helden DF, Horton MA, Burns GF. Apoptosis induced by inhibition of intercellular contact. J Cell Biol. 1994;125:403–415
  54. Mueller-Klieser W. Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am J Physiol. 1997;273:1109–1123
  55. Korff T, Augustin HG. Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J Cell Biol. 1998;143:1341–1352
  56. Füller T, Korff T, Kilian A, Dandekar G, Augustin HG. Forward EphB4 signaling in endothelial cells controls cellular repulsion and segregation from ephrinB2 positive cells. J Cell Sci. 2003;116:2461–2470
  57. Baal N, Widmer-Teske R, McKinnon T, Preissner KT, Zygmunt MT. In vitro spheroid model of placental vasculogenesis: does it work? Lab Invest. 2009;89:152–163
  58. Korff T, Krauss T, Augustin HG. Three-dimensional spheroidal culture of cytotrophoblast cells mimics the phenotype and differentiation of cytotrophoblasts from normal and preeclamptic pregnancies. Exp Cell Res. 2004;297:415–423

PII: S0093-691X(09)00496-8

doi: 10.1016/j.theriogenology.2009.11.003

Theriogenology
Volume 73, Issue 6 , Pages 817-827 , 1 April 2010