Placenta
Volume 30, Issue 5 , Pages 398-404 , May 2009

The Urokinase Plasminogen Activator (uPA) System in Uterine Natural Killer Cells in the Placental Bed During Early Pregnancy

  • K. Naruse

      Affiliations

    • Institute of Cellular Medicine, Newcastle University, UK
    • These authors contributed equally to the manuscript.
  • ,
  • G.E. Lash

      Affiliations

    • Institute of Cellular Medicine, Newcastle University, UK
    • These authors contributed equally to the manuscript.
    • Corresponding Author InformationCorrespondence to: Dr Gendie E. Lash, Institute of Cellular Medicine, 3rd Floor, William Leech Building, Newcastle University, Newcastle upon Tyne NE2 4HH, UK. Tel.: +44 191 222 8578; fax: +44 191 222 5066.
  • ,
  • J.N. Bulmer

      Affiliations

    • Institute of Cellular Medicine, Newcastle University, UK
  • ,
  • B.A. Innes

      Affiliations

    • Institute of Cellular Medicine, Newcastle University, UK
  • ,
  • H.A. Otun

      Affiliations

    • Institute of Cellular Medicine, Newcastle University, UK
  • ,
  • R.F. Searle

      Affiliations

    • School of Medical Education Development, Newcastle University, UK
  • ,
  • S.C. Robson

      Affiliations

    • Institute of Cellular Medicine, Newcastle University, UK

,Accepted 11 February 2009.

References 

  1. Preissner KT, Kanse SM, May AE. Urokinase receptor: a molecular organizer in cellular communication. Curr Opin Cell Biol. 2000;12:621–628
  2. Vassalli JD, Sappino AP, Belin D. The plasminogen activator/plasmin system. J Clin Invest. 1991;88:1067–1072
  3. Kanse SM, Kost C, Wilhelm OG, Andreasen PA, Preissner KT. The urokinase receptor is a major vitronectin-binding protein on endothelial cells. Exp Cell Res. 1996;224:344–353
  4. Bischof P, Irminger-Finger I. The human cytotrophoblastic cell, a mononuclear chameleon. Int J Biochem Cell Biol. 2005;37:1–16
  5. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta. 2006;27:939–958
  6. 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
  7. Lala PK, Chakraborty C. Factors regulating trophoblast migration and invasiveness: possible derangements contributing to pre-eclampsia and fetal injury. Placenta. 2003;24:575–587
  8. 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
  9. 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
  10. Al-Atrash G, Shetty S, Idell S, Xue Y, Kitson RP, Halady PKS, et al. IL-2-mediated upregulation of uPA and uPAR in natural killer cells. Biochem Biophys Res Com. 2002;292:184–189
  11. Saito S, Nishikawa K, Morii T, Enomoto M, Narita N, Motooshi K, et al. Cytokine production by CD16–CD56bright natural killer cells in the human early pregnancy decidua. Int Immunol. 1993;5:559–563
  12. Bulmer JN, Morrison L, Longfellow M, Ritson A, Pace D. Granulated lymphocytes in human endometrium: histochemical and immunohistochemical studies. Hum Reprod. 1991;6:791–798
  13. Bulmer JN, Lash GE. Human uterine natural killer cells: a reappraisal. Mol Immunol. 2005;42:511–521
  14. Lash GE, Schiessl B, Kirkley M, Innes BA, Cooper A, Searle RF, et al. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J Leukoc Biol. 2006;80:572–580
  15. Robson SC, Simpson H, Ball E, Lyall F, Bulmer JN. Punch biopsy in human placental bed. Am J Obstet Gynecol. 2002;187:1349–1355
  16. Sappino AP, Madani R, Huarte J, Belin D, Kiss JZ, Wohlwend A, et al. Extracellular proteolysis in the adult murine brain. J Clin Invest. 1993;92:679–685
  17. Adams EJ, Green JA, Clark AH, Youngson JH. Comparison of different scoring systems for immunohistochemical staining. J Clin Pathol. 1999;52:75–77
  18. Vassiliadou N, Bulmer JN. Functional studies of human decidua in spontaneous early pregnancy loss: effect of soluble factors and purified CD56+ lymphocytes on killing of natural killer- and lymphokine-activated killer-sensitive targets. Biol Reprod. 1998;58:982–987
  19. Graham CH, McCrae KR. Altered expression of gelatinase and surface-associated plasminogen activator activity by trophoblast cells isolated from placentas of preeclamptic patients. Am J Obstet Gynecol. 1996;175:555–562
  20. Al-Atrash G, Kitson RP, Sue Y, Mazar AP, Kim MH, Goldfarb RH. uPA and uPAR contribute to NK cell invasion through the extracellular matrix. Anticancer Res. 2001;21:1697–1704
  21. Gellert GC, Goldfarb RH, Kitson RP. Physical association of uPAR with the alphaV integrin on the surface of human NK cells. Biochem Biophys Res Commun. 2004;315:1025–1032
  22. Lash GE, Otun HA, Innes BA, Kirkley M, De Oliveira L, Searle RF, et al. Interferon-γ inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels. FASEB J. 2006;20:2512–2518
  23. Multhaupt HA, Mazar A, Cines DB, Warhol MJ, McCrae KR. Expression of urokinase receptors by human trophoblast. A histochemical and ultrastructural analysis. Lab Invest. 1994;71:392–400
  24. Floridon C, Niesen O, Holund B, Sunde L, Westergaard JG, Thomsen SG, et al. Localization and significance of urokinase plasminogen activator and its receptor in placental tissue from intrauterine, ectopic and molar pregnancies. Placenta. 1999;20:711–721
  25. Hu ZY, Liu YX, Liu K, Byrne S, Ny T, Feng Q, et al. Expression of tissue type and urokinase type plasminogen activators as well as plasminogen activator inhibitor type-1 and type-2 in human and rhesus monkey placenta. J Anat. 1999;194:183–185
  26. Tsatas D, Baker MS, Rice GE. Tissue-specific expression of the relaxed conformation of plasminogen activator inhibitor-2 and low-density lipoprotein receptor-related protein in human term gestational tissues. J Histochem Cytochem. 1997;45:1593–1602
  27. Plaisier M, Koolwijk P, Willems F, Helmerhorst FM, van Hinsbergh VWM. Pericellular-acting proteases in human first trimester decidua. Mol Hum Reprod. 2008;14:41–51
  28. Ueyama M, Kasatori N, Urayama T, Maemura T, Yao Y, Shiraishi T, et al. Quantitative evaluation of the influence of ovarian steroids on plasminogen activators and inhibitors in human endometrial cells and trophoblasts. Thromb Res. 2002;108:235–244
  29. Bruse C, Guan Y, Carlberg M, Carlstrom K, Bergqvist A. Basal release of urokinase plasminogen activator, plasminogen activator inhibitor-1, and soluble plasminogen activator receptor from separated and cultured endometriotic and endometrial stromal and epithelial cells. Fertil Steril. 2005;83:1155–1160
  30. Anteby EY, Greenfield C, Natanson-Yaron S, Goldman-Wohl D, Hamani Y, Khudyak V, et al. Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod. 2004;10:229–235
  31. Lash GE, Otun HA, Percival K, Innes BA, Bulmer JN, Searle RF, et al. Uterine natural killer cell regulation of trophoblast invasion. Reprod Sci. 2007;14:258A
  32. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cell regulate key developmental processes at the human fetal–maternal interface. Nat Med. 2006;12:1065–1074
  33. Hu Y, Dutz JP, MacCalman CD, Yong P, Tan R, von Dadelszen P. Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-gamma. J Immunol. 2006;177:8522–8530
  34. Craven CM, Morgan T, Ward K. Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta. 1998;19:241–252
  35. Kam EP, Gardner L, Loke YW, King A. The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod. 1999;14:2131–2138
  36. Naruse K, Lash GE, Innes BA, Otun HA, Oliveira LG, Searle RF, et al. Uterine natural killer cells disrupt vascular smooth muscle structure in vitro: A role in spiral artery remodeling?. Placenta. 2007;28:A22

PII: S0143-4004(09)00058-7

doi: 10.1016/j.placenta.2009.02.002

Placenta
Volume 30, Issue 5 , Pages 398-404 , May 2009