Placenta
Volume 29, Issue 10 , Pages 871-878 , October 2008

In Vitro and In Vivo Evidence for Lack of Endovascular Remodeling by Third Trimester Trophoblasts

  • S. Kalkunte

      Affiliations

    • Department of Pediatrics, Women and Infants Hospital, 101 Dudley Street, Providence, RI 02905, USA
  • ,
  • Z. Lai

      Affiliations

    • Department of Pediatrics, Women and Infants Hospital, 101 Dudley Street, Providence, RI 02905, USA
  • ,
  • N. Tewari

      Affiliations

    • Department of Pediatrics, Women and Infants Hospital, 101 Dudley Street, Providence, RI 02905, USA
  • ,
  • C. Chichester

      Affiliations

    • Department of Biomedical and Pharmaceutical Sciences, School of Pharmacy, University of Rhode Island, Kingston, RI, USA
  • ,
  • R. Romero

      Affiliations

    • Perinatology Research Branch, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH, DHHS, Bethesda, MD, USA
  • ,
  • J. Padbury

      Affiliations

    • Department of Pediatrics, Women and Infants Hospital, 101 Dudley Street, Providence, RI 02905, USA
  • ,
  • S. Sharma

      Affiliations

    • Department of Pediatrics, Women and Infants Hospital, 101 Dudley Street, Providence, RI 02905, USA
    • Corresponding Author InformationCorresponding author. Tel.: +401 274 1122x8004.

,Accepted 24 July 2008.

References 

  1. Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta. 2002;23:3–19
  2. Pijnenborg R, Bland JM, Robertson WB, Brosens I. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta. 1983;4:397–413
  3. Naicker T, Khedun SM, Moodley J, Pijnenborg R. Quantitative analysis of trophoblast invasion in preeclampsia. Acta Obstet Gynecol Scand. 2003;82:722–729
  4. Espinoza J, Romero R, Mee Kim Y, Kusanovic JP, Hassan S, Erez O, et al. Normal and abnormal transformation of the spiral arteries during pregnancy. J Perinat Med. 2006;34:447–458
  5. Kim YM, Bujold E, Chaiworapongsa T, Gomez R, Yoon BH, Thaler HT, et al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol. 2003;189:1063–1069
  6. Aplin J, Charlton S, Ayad S. An immunohistochemical study of human endometrial extracellular matrix during the menstrual cycle and first trimester of pregnancy. Cell Tissue Res. 1988;253:231–240
  7. Kham EP, Gardner L, Loke YW, King A. The role of trophoblasts in the physiological change in decidual spiral arteries. Hum Reprod. 1999;14:2131–2138
  8. Gilbert JS, Ryan MJ, LaMarca BB, Sedeek M, Murphy SR, Granger JP. Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction. Am J Physiol Heart Circ Physiol. 2008;294:541–550
  9. Hanna N, Hanna I, Hleb M, Wagner E, Dougherty J, Balkundi D, et al. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J Immunol. 2000;164:5721–5728
  10. Renaud SJ, Postovit LM, Macdonald-Goodfellow SK, McDonald GT, Caldwell JD, Graham CH. Activated macrophages inhibit human cytotrophoblast invasiveness in vitro. Biol Reprod. 2005;73:237–243
  11. Aldo PB, Krikun G, Visintin I, Lockwood C, Romero R, Mor G. A novel three-dimensional in vitro system to study trophoblast-endothelium cell interactions. Am J Reprod Immunol. 2007;58:98–110
  12. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at the human fetal–maternal interface. Nat Med. 2006;12:1065–1074
  13. Greenwood JD, Minhas K, di Santo JP, Makita M, Kiso Y, Croy BA. Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta. 2000;21:693–702
  14. Graham CH, Hawley TS, Hawley RG, MacDougall JR, Kerbel RS, Khoo N, et al. Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res. 1993;206:204–211
  15. Lewis MP, Clements M, Takeda S, Kirby PL, Seki H, Lonsdale LB, et al. Partial characterization of an immortalized human trophoblast cell-line, TCL-1, which possesses a CSF-1 autocrine loop. Placenta. 1996;17:137–146
  16. Fest S, Brachwitz N, Schumacher A, Zenclussen ML, Khan F, Wafula PO, et al. Supporting the hypothesis of pregnancy as a tumor: survivin is upregulated in normal pregnant mice and participates in human trophoblast proliferation. Am J Reprod Immunol. 2008;59:75–83
  17. Boguslawski G, McGlynn PW, Harvey KA, Kovala AT. SU1498, an inhibitor of vascular endothelial growth factor receptor 2, causes accumulation of phosphorylated ERK kinases and inhibits their activity in vivo and in vitro. J Biol Chem. 2004;279:5716–5724
  18. Bulla R, Villa A, Bossi F, Cassetti A, Radillo O, Spessotto P, et al. VE-cadherin is a critical molecule for trophoblast–endothelial cell interaction in decidual spiral arteries. Exp Cell Res. 2005;303:101–113
  19. Debnath J, Brugge JS. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer. 2005;5:675–688
  20. Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol. 2003;188:177–182
  21. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med. 2004;350:672–683
  22. Clark DE, Smith SK, He Y, Day KA, Licence DR, Corps AN, et al. A vascular endothelial growth factor antagonist is produced by the human placenta and released into the maternal circulation. Biol Reprod. 1998;59:1540–1548
  23. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med. 2006;12:642–649
  24. Lindheimer MD, Romero R. Emerging roles of antiangiogenic and angiogenic proteins in pathogenesis and prediction of preeclampsia. Hypertension. 2007;50:35–36
  25. Chung JY, Song Y, Wang Y, Magness RR, Zheng J. Differential expression of vascular endothelial growth factor (VEGF), endocrine gland derived-VEGF, and VEGF receptors in human placentas from normal and preeclamptic pregnancies. J Clin Endocrinol Metab. 2004;89:2484–2490
  26. Zhau Y, Fisher SJ, Janatpor M, Genbacev O, Dejana E, Wheelock M, et al. Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion. J Clin Invest. 1997;99:2139–2151
  27. Goldman-Who DS, Ariel I, Geenfield C, Hochner-Celnikier D, Cross J, Fisher S, et al. Lack of human leukocyte antigen-G expression in extravillous trophoblasts is associated with preeclampsia. Mol Hum Reprod. 2000;6:88–95
  28. Masatsugu Ueda M, Terai Y, Kumagai K, Ueki K, Yamaguchi H, Akise D, et al. Vascular endothelial growth factor C gene expression is closely related to invasion phenotype in gynecological tumor cells. Gynecol Oncol. 2001;82:162–166
  29. Zhou Y, Bellingard V, Feng KT, McMaster M, Fisher SJ. Human cytotrophoblasts promote endothelial survival and vascular remodeling through secretion of Ang2, PlGF, and VEGF-C. Dev Biol. 2003;263:114–125
  30. Hiratsuka S, Kataoka Y, Nakao K, Nakamura K, Morikawa S, Tanaka S, et al. Vascular endothelial growth factor A (VEGF-A) is involved in guidance of VEGF receptor-positive cells to the anterior portion of early embryos. Mol Cell Biol. 2005;25:355–363
  31. Yang S, Xin X, Zlot C, Ingle G, Fuh G, Li B, et al. Vascular endothelial cell growth factor-driven endothelial tube formation is mediated by vascular endothelial cell growth factor receptor-2, a kinase insert domain-containing receptor. Arterioscler Thromb Vasc Biol. 2001;21:1934–1940
  32. Zhou Y, McMaster M, Woo K, Janatpour M, Perry J, Karpanen T, et al. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome. Am J Pathol. 2002;160:1405–1423
  33. Karmakar S, Das C. Modulation of ezrin and E-cadherin expression by IL-1beta and TGF-beta1 in human trophoblasts. J Reprod Immunol. 2004;64:9–29
  34. D'Souza-Schorey C. Disassembling adherens junctions: breaking up is hard to do. Trends Cell Biol. 2005;15:19–26
  35. Rahnama F, Shafiei F, Gluckman PD, Mitchell MD, Lobie PE. Epigenetic regulation of human trophoblastic cell migration and invasion. Endocrinology. 2006;147:5275–5283

PII: S0143-4004(08)00221-X

doi: 10.1016/j.placenta.2008.07.009

Placenta
Volume 29, Issue 10 , Pages 871-878 , October 2008