Placenta
Volume 28, Issue 5 , Pages 390-398 , May 2007

Effect of Low Oxygen Concentrations on Trophoblast-Like Cell Line Invasion

  • G.E. Lash

      Affiliations

    • School of Surgical and Reproductive Sciences, 3rd Floor, William Leech Building, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK
    • Corresponding Author InformationCorresponding author. Tel.: +44 191 222 5213; fax: +44 191 222 5066.
  • ,
  • J. Hornbuckle

      Affiliations

    • School of Surgical and Reproductive Sciences, 3rd Floor, William Leech Building, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK
  • ,
  • A. Brunt

      Affiliations

    • School of Surgical and Reproductive Sciences, 3rd Floor, William Leech Building, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK
  • ,
  • M. Kirkley

      Affiliations

    • School of Surgical and Reproductive Sciences, 3rd Floor, William Leech Building, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK
  • ,
  • R.F. Searle

      Affiliations

    • Medical Education Development, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK
  • ,
  • S.C. Robson

      Affiliations

    • School of Surgical and Reproductive Sciences, 3rd Floor, William Leech Building, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK
  • ,
  • J.N. Bulmer

      Affiliations

    • Clinical and Laboratory Sciences, University of Newcastle upon Tyne, Newcastle upon Tyne NE2 4HH, UK

,Accepted 1 June 2006.

References 

  1. 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
  2. Brosens I, Robertson WB, Dixon HG. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol. 1967;93:569–579
  3. Pijnenborg R, Dixon G, Robertson WB, Brosens I. Trophoblastic invasion of human decidua from 8 to 18weeks of pregnancy. Placenta. 1980;1:3–19
  4. Khong TY, Lane EB, Robertson WB. An immunocytochemical study of fetal cells at the maternal-placental interface using monoclonal antibodies to keratins, vimentin and desmin. Cell Tissue Res. 1986;246:189–195
  5. Pijnenborg R. Implantation and immunology: maternal inflammatory and immune cellular responses to implantation and trophoblast invasion. Reprod Biomed Online. 2002;4:14–17
  6. Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest. 1996;97:540–550
  7. Bauer S, Pollheimer J, Hartmann J, Husslein P, Aplin JD, Knofler M. Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J Clin Endocrinol Metab. 2004;89:812–822
  8. Lash GE, Otun HA, Innes BA, Bulmer JN, Searle RF, Robson SC. Inhibition of trophoblast cell invasion by TGFB1, 2, and 3 is associated with a decrease in active proteases. Biol Reprod. 2005;73:374–381
  9. Zygmunt M, Hahn D, Munstedt K, Bischof P, Lang U. Invasion of cytotrophoblastic JEG-3 cells is stimulated by hCG in vitro. Placenta. 1998;19:587–593
  10. Mandl M, Haas J, Bischof P, Nohammer G, Desoye G. Serum-dependent effects of IGF-I and insulin on proliferation and invasion of human first trimester trophoblast cell models. Histochem Cell Biol. 2002;117:391–399
  11. Cartwright JE, Holden DP, Whitley GS. Hepatocyte growth factor regulates human trophoblast motility and invasion: a role for nitric oxide. Br J Pharmacol. 1999;128:181–189
  12. Lash GE, Cartwright JE, Whitley GS, Trew AJ, Baker PN. The effects of angiogenic growth factors on extravillous trophoblast invasion and motility. Placenta. 1999;20:661–667
  13. Fitzpatrick TE, Lash GE, Yanaihara A, Charnock-Jones DS, Macdonald-Goodfellow SK, Graham CH. Inhibition of breast carcinoma and trophoblast cell invasiveness by vascular endothelial growth factor. Exp Cell Res. 2003;283:247–255
  14. Frank HG, Genbacev O, Blaschitz A, Chen CP, Clarson L, Evain-Brion D, et al. Cell culture models of human trophoblast—primary culture of trophoblast—a workshop report. Placenta. 2000;21:S120–S122
  15. King A, Thomas L, Bischof P. Cell culture models of trophoblast II: trophoblast cell lines—a workshop report. Placenta. 2000;21:S113–S119
  16. Genbacev O, Miller RK. Post-implantation differentiation and proliferation of cytotrophoblast cells: in vitro models—a review. Placenta. 2000;21:S45–S49
  17. Frank HG, Morrish DW, Potgens A, Genbacev O, Kumpel B, Caniggia I. Cell culture models of human trophoblast: primary culture of trophoblast—a workshop report. Placenta. 2001;22:S107–S109
  18. Shiverick KT, King A, Frank H, Whitley GS, Cartwright JE, Schneider H. Cell culture models of human trophoblast II: trophoblast cell lines—a workshop report. Placenta. 2001;22:S104–S106
  19. Morrish DW, Whitley GS, Cartwright JE, Graham CH, Caniggia I. In vitro models to study trophoblast function and dysfunction—a workshop report. Placenta. 2002;23:S114–S118
  20. Lash GE, Otun HA, Innes BA, Bulmer JN, Searle RF, Robson SC. Low oxygen concentrations inhibit trophoblast cell invasion from early gestation placental explants via alterations in levels of the urokinase plasminogen activator system. Biol Reprod. 2006;74:403–409
  21. Graham CH, Fitzpatrick TE, McCrae KR. Hypoxia stimulates urokinase receptor expression through a heme protein-dependent pathway. Blood. 1998;91:3300–3307
  22. Fitzpatrick TE, Graham CH. Stimulation of plasminogen activator inhibitor-1 expression in immortalized human trophoblast cells cultured under low levels of oxygen. Exp Cell Res. 1998;245:155–162
  23. Graham CH. Effect of transforming growth factor-beta on the plasminogen activator system in cultured first trimester human cytotrophoblasts. Placenta. 1997;18:137–143
  24. Tse WK, Whitley GS, Cartwright JE. Transforming growth factor-beta1 regulates hepatocyte growth factor-induced trophoblast motility and invasion. Placenta. 2002;23:699–705
  25. Graham CH, Connelly I, MacDougall JR, Kerbel RS, Stetler-Stevenson WG, Lala PK. Resistance of malignant trophoblast cells to both the anti-proliferative and anti-invasive effects of transforming growth factor-beta. Exp Cell Res. 1994;214:93–99
  26. 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
  27. Choy MY, St Whitley G, Manyonda IT. Efficient, rapid and reliable establishment of human trophoblast cell lines using poly-l-ornithine. Early Pregnancy. 2000;4:124–143
  28. Kohler PO, Bridson WE. Isolation of hormone-producing clonal lines of human choriocarcinoma. J Clin Endocrinol Metab. 1971;32:683–687
  29. Pattillo RA, Hussa RO, Garancis JC. Glycogen metabolism in human hormone-producing trophoblastic cells in continuous culture. I. Regulation of glycogen metabolism by glucose. In Vitro. 1971;7:59–67
  30. Kadyrov M, Kaufmann P, Huppertz B. Expression of a cytokeratin 18 neo-epitope is a specific marker for trophoblast apoptosis in human placenta. Placenta. 2001;22:44–48
  31. Aplin JD. Adhesion molecules in implantation. Rev Reprod. 1997;2:84–93
  32. Kilburn BA, Wang J, Duniec-Dmuchowski ZM, Leach RE, Romero R, Armant DR. Extracellular matrix composition and hypoxia regulate the expression of HLA-G and integrins in a human trophoblast cell line. Biol Reprod. 2000;62:739–747
  33. Hall DE, Reichardt LF, Crowley E, Holley B, Moezzi H, Sonnenberg A, et al. The alpha 1/beta 1 and alpha 6/beta 1 integrin heterodimers mediate cell attachment to distinct sites on laminin. J Cell Biol. 1990;110:2175–2184
  34. Manyonda IT, Whitley GS, Cartwright JE. Trophoblast cell lines: a response to the Workshop Report by King et al. Placenta. 2001;22:262–263
  35. Canning MT, Postovit LM, Clarke SH, Graham CH. Oxygen-mediated regulation of gelatinase and tissue inhibitor of metalloproteinases-1 expression by invasive cells. Exp Cell Res. 2001;267:88–94
  36. Karmakar S, Dhar R, Das C. Inhibition of cytotrophoblastic (JEG-3) cell invasion by interleukin 12 involves an interferon gamma-mediated pathway. J Biol Chem. 2004;279:55297–55307
  37. Lash GE, Tayler CM, Trew AJ, Cooper S, Anthony FW, Wheeler T, et al. Vascular endothelial growth factor and placental growth factor release in cultured trophoblast cells under different oxygen tensions. Growth Factors. 2002;20:189–196
  38. Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest. 2000;105:577–587

PII: S0143-4004(06)00134-2

doi: 10.1016/j.placenta.2006.06.001

Placenta
Volume 28, Issue 5 , Pages 390-398 , May 2007