Decidual natural killer cell interactions with trophoblasts are impaired in pregnancies at increased risk of preeclampsia

American Journal of Pathology

Volumn 183, Issue 6, 2013, Pages 1853-1861

  Wallace, Alison E ^a   Host, Amanda J ^a   Whitley, Guy S ^a   Cartwright, Judith E ^a  

^a ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE;

ARTICLE; CELL INTERACTION; CELL MOTILITY; ENZYME PHOSPHORYLATION; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PREECLAMPSIA; PREGNANCY DISORDER; PRIORITY JOURNAL; RISK FACTOR; TROPHOBLAST; UTERINE ARTERY;

ADULT; CHEMOTAXIS; DECIDUA; FEMALE; HUMANS; KILLER CELLS, NATURAL; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3-KINASES; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RISK FACTORS; TROPHOBLASTS;

EID: 84888266400     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.08.023     Document Type: Article

References (45)

1. R. Pijnenborg, L. Vercruysse, and I. Brosens Deep placentation Best Pract Res Clin Obstet Gynaecol 25 2011 273 285
2. S.V. Ashton, G.S. Whitley, P.R. Dash, M. Wareing, I.P. Crocker, P.N. Baker, and J.E. Cartwright Uterine spiral artery remodeling involves endothelial apoptosis induced by extravillous trophoblasts through Fas/FasL interactions Arterioscler Thromb Vasc Biol 25 2005 102 108
3. R.J. Keogh, L.K. Harris, A. Freeman, P.N. Baker, J.D. Aplin, G.S. Whitley, and J.E. Cartwright Fetal-derived trophoblast use the apoptotic cytokine tumor necrosis factor-alpha-related apoptosis-inducing ligand to induce smooth muscle cell death Circ Res 100 2007 834 841
4. J.N. Bulmer, B.A. Innes, J. Levey, S.C. Robson, and G.E. Lash The role of vascular smooth muscle cell apoptosis and migration during uterine spiral artery remodeling in normal human pregnancy FASEB J 26 2012 2975 2985
5. A.E. Wallace, J.E. Cartwright, R. Begum, K. Laing, B. Thilaganathan, and G.S. Whitley Trophoblast-induced changes in C-x-C motif chemokine 10 expression contribute to vascular smooth muscle cell dedifferentiation during spiral artery remodeling Arterioscler Thromb Vasc Biol 33 2013 e93 e101
6. R. Pijnenborg, J. Anthony, D.A. Davey, A. Rees, A. Tiltman, L. Vercruysse, and A. van Assche Placental bed spiral arteries in the hypertensive disorders of pregnancy Br J Obstet Gynaecol 98 1991 648 655
7. I. Brosens, H.G. Dixon, and W.B. Robertson Fetal growth retardation and the arteries of the placental bed Br J Obstet Gynaecol 84 1977 656 663
8. S.D. Smith, C.E. Dunk, J.D. Aplin, L.K. Harris, and R.L. Jones Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy Am J Pathol 174 2009 1959 1971
9. H. El Costa, J. Tabiasco, A. Berrebi, O. Parant, M. Aguerre-Girr, M.P. Piccinni, and P. Le Bouteiller Effector functions of human decidual NK cells in healthy early pregnancy are dependent on the specific engagement of natural cytotoxicity receptors J Reprod Immunol 82 2009 142 147
10. J. Tabiasco, M. Rabot, M. Aguerre-Girr, H. El Costa, A. Berrebi, O. Parant, G. Laskarin, K. Juretic, A. Bensussan, D. Rukavina, and P. Le Bouteiller Human decidual NK cells: unique phenotype and functional properties - a review Placenta 27 Suppl A 2006 S34 S39
11. P. Le Bouteiller, J. Siewiera, Y. Casart, M. Aguerre-Girr, H. El Costa, A. Berrebi, J. Tabiasco, and N. Jabrane-Ferrat The human decidual NK-cell response to virus infection: what can we learn from circulating NK lymphocytes? J Reprod Immunol 88 2011 170 175
12. L.K. Harris IFPA Gabor Than Award lecture: transformation of the spiral arteries in human pregnancy: key events in the remodelling timeline Placenta 32 Suppl 2 2011 S154 S158
13. K. Naruse, G.E. Lash, B.A. Innes, H.A. Otun, R.F. Searle, S.C. Robson, and J.N. Bulmer Localization of matrix metalloproteinase (MMP)-2, MMP-9 and tissue inhibitors for MMPs (TIMPs) in uterine natural killer cells in early human pregnancy Hum Reprod 24 2009 553 561
14. R. Fraser, G.S. Whitley, A.P. Johnstone, A.J. Host, N.J. Sebire, B. Thilaganathan, and J.E. Cartwright Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance J Pathol 228 2012 322 332
15. J. Hanna, D. Goldman-Wohl, Y. Hamani, I. Avraham, C. Greenfield, S. Natanson-Yaron, D. Prus, L. Cohen-Daniel, T.I. Arnon, I. Manaster, R. Gazit, V. Yutkin, D. Benharroch, A. Porgador, E. Keshet, S. Yagel, and O. Mandelboim Decidual NK cells regulate key developmental processes at the human fetal-maternal interface Nat Med 12 2006 1065 1074
16. Y. Hu, J.P. Dutz, C.D. MacCalman, P. Yong, R. Tan, and P. von Dadelszen Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-gamma J Immunol 177 2006 8522 8530
17. N.J. Hannan, R.L. Jones, C.A. White, and L.A. Salamonsen The chemokines, CX3CL1, CCL14, and CCL4, promote human trophoblast migration at the feto-maternal interface Biol Reprod 74 2006 896 904
18. G.E. Lash, B. Schiessl, M. Kirkley, B.A. Innes, A. Cooper, R.F. Searle, S.C. Robson, and J.N. Bulmer Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy J Leukoc Biol 80 2006 572 580
19. S. Saito, K. Nishikawa, T. Morii, M. Enomoto, N. Narita, K. Motoyoshi, and M. Ichijo Cytokine production by CD16-CD56 bright natural killer cells in the human early pregnancy decidua Int Immunol 5 1993 559 563
20. M.J. Bilinski, J.G. Thorne, M.J. Oh, S. Leonard, C. Murrant, C. Tayade, and B.A. Croy Uterine NK cells in murine pregnancy Reprod Biomed Online 16 2008 218 226
21. S.E. Hiby, R. Apps, A.M. Sharkey, L.E. Farrell, L. Gardner, A. Mulder, F.H. Claas, J.J. Walker, C.W. Redman, L. Morgan, C. Tower, L. Regan, G.E. Moore, M. Carrington, and A. Moffett Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2 J Clin Invest 120 2010 4102 4110
22. S.E. Hiby, J.J. Walker, K.M. O'Shaughnessy, C.W. Redman, M. Carrington, J. Trowsdale, and A. Moffett Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success J Exp Med 200 2004 957 965
23. K. Melchiorre, K. Leslie, F. Prefumo, A. Bhide, and B. Thilaganathan First-trimester uterine artery Doppler indices in the prediction of small-for-gestational age pregnancy and intrauterine growth restriction Ultrasound Obstet Gynecol 33 2009 524 529
24. F. Prefumo, N.J. Sebire, and B. Thilaganathan Decreased endovascular trophoblast invasion in first trimester pregnancies with high-resistance uterine artery Doppler indices Hum Reprod 19 2004 206 209
25. K. Melchiorre, B. Wormald, K. Leslie, A. Bhide, and B. Thilaganathan First-trimester uterine artery Doppler indices in term and preterm pre-eclampsia Ultrasound Obstet Gynecol 32 2008 133 137
26. G.S. Whitley, P.R. Dash, L.J. Ayling, F. Prefumo, B. Thilaganathan, and J.E. Cartwright Increased apoptosis in first trimester extravillous trophoblasts from pregnancies at higher risk of developing preeclampsia Am J Pathol 170 2007 1903 1909
27. A.D. Kofinas, M. Penry, M. Swain, and C.G. Hatjis Effect of placental laterality on uterine artery resistance and development of preeclampsia and intrauterine growth retardation Am J Obstet Gynecol 161 1989 1536 1539
28. A.M. Martin, R. Bindra, P. Curcio, S. Cicero, and K.H. Nicolaides Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler at 11-14 weeks of gestation Ultrasound Obstet Gynecol 18 2001 583 586
29. J.E. Cartwright, D.P. Holden, and G.S. Whitley Hepatocyte growth factor regulates human trophoblast motility and invasion: a role for nitric oxide Br J Pharmacol 128 1999 181 189
30. I. Grant, J.E. Cartwright, B. Lumicisi, A.E. Wallace, and G.S. Whitley Caffeine inhibits EGF-stimulated trophoblast cell motility through the inhibition of mTORC2 and Akt Endocrinology 153 2012 4502 4510
31. J.L. James, P.R. Stone, and L.W. Chamley Cytotrophoblast differentiation in the first trimester of pregnancy: evidence for separate progenitors of extravillous trophoblasts and syncytiotrophoblast Reproduction 130 2005 95 103
32. J.L. James, P.R. Stone, and L.W. Chamley The regulation of trophoblast differentiation by oxygen in the first trimester of pregnancy Hum Reprod Update 12 2006 137 144
33. G.E. Lash, H.A. Otun, B.A. Innes, K. Percival, R.F. Searle, S.C. Robson, and J.N. Bulmer Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age Hum Reprod 25 2010 1137 1145
34. M. Jovanovic, and L. Vicovac Interleukin-6 stimulates cell migration, invasion and integrin expression in HTR-8/SVneo cell line Placenta 30 2009 320 328
35. H.L. LaMarca, P.R. Dash, K. Vishnuthevan, E. Harvey, D.E. Sullivan, C.A. Morris, and G.S. Whitley Epidermal growth factor-stimulated extravillous cytotrophoblast motility is mediated by the activation of PI3-K, Akt and both p38 and p42/44 mitogen-activated protein kinases Hum Reprod 23 2008 1733 1741
36. M. Knofler, and J. Pollheimer IFPA Award in Placentology lecture: molecular regulation of human trophoblast invasion Placenta 33 Suppl 2012 S55 S62
37. A. Trundley, and A. Moffett Human uterine leukocytes and pregnancy Tissue Antigens 63 2004 1 12
38. M. Jovanovic, I. Stefanoska, L. Radojcic, and L. Vicovac Interleukin-8 (CXCL8) stimulates trophoblast cell migration and invasion by increasing levels of matrix metalloproteinase (MMP)2 and MMP9 and integrins alpha5 and beta1 Reproduction 139 2010 789 798
39. F. Dominguez, S. Martinez, A. Quinonero, F. Loro, J.A. Horcajadas, A. Pellicer, and C. Simon CXCL10 and IL-6 induce chemotaxis in human trophoblast cell lines Mol Hum Reprod 14 2008 423 430
40. A.E. Wallace, R. Fraser, and J.E. Cartwright Extravillous trophoblast and decidual natural killer cells: a remodelling partnership Hum Reprod Update 18 2012 458 471
41. G.E. Lash, A.Y. Warren, S. Underwood, and P.N. Baker Vascular endothelial growth factor is a chemoattractant for trophoblast cells Placenta 24 2003 549 556
42. J.E. Cartwright, W.K. Tse, and G.S. Whitley Hepatocyte growth factor induced human trophoblast motility involves phosphatidylinositol-3-kinase, mitogen-activated protein kinase, and inducible nitric oxide synthase Exp Cell Res 279 2002 219 226
43. M. Cargnello, and P.P. Roux Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases Microbiol Mol Biol Rev 75 2011 50 83
44. H.A. Otun, G.E. Lash, B.A. Innes, J.N. Bulmer, K. Naruse, T. Hannon, R.F. Searle, and S.C. Robson Effect of tumour necrosis factor-alpha in combination with interferon-gamma on first trimester extravillous trophoblast invasion J Reprod Immunol 88 2011 1 11
45. G.E. Lash, H.A. Otun, B.A. Innes, M. Kirkley, L. De Oliveira, R.F. Searle, S.C. Robson, and J.N. Bulmer Interferon-gamma inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels FASEB J 20 2006 2512 2518