Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance

Abstract

During human pregnancy, natural killer (NK) cells accumulate in the maternal decidua, but their specific roles remain to be determined. Decidual NK (dNK) cells are present during trophoblast invasion and uterine spiral artery remodelling. These events are crucial for successful placentation and the provision of an adequate blood supply to the developing fetus. Remodelling of spiral arteries is impaired in the dangerous pregnancy complication pre‐eclampsia. We studied dNK cells isolated from pregnancies at 9–14 weeks' gestation, screened by uterine artery Doppler ultrasound to determine resistance indices which relate to the extent of spiral artery remodelling. dNK cells were able to promote the invasive behaviour of fetal trophoblast cells, partly through HGF. Cells isolated from pregnancies with higher resistance indices were less able to do this and secreted fewer pro‐invasive factors. dNK cells from pregnancies with normal resistance indices could induce apoptotic changes in vascular smooth muscle and endothelial cells in vitro , events of importance in vessel remodelling, partly through Fas signalling. dNK cells isolated from high resistance index pregnancies failed to induce vascular apoptosis and secreted fewer pro‐apoptotic factors. We have modelled the cellular interactions at the maternal‐fetal interface and provide the first demonstration of a functional role for dNK cells in influencing vascular cells. A potential mechanism contributing to impaired vessel remodelling in pregnancies with a higher uterine artery resistance is presented. These findings may be informative in determining the cellular interactions contributing to the pathology of pregnancy disorders where remodelling is impaired, such as pre‐eclampsia. Copyright © 2012 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.

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References 46

1. 1.

   Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta. 2006;27:939-958.

   Not in our library10.1016/j.placenta.2005.12.006

2. 2.

   Tabiasco J, Rabot M, Aguerre-Girr M, et al. Human decidual NK cells: unique phenotype and functional properties—a review. Placenta. 2006;27(Suppl A):S34-S39.

   Not in our library10.1016/j.placenta.2006.01.009

3. 3.

   Moffett-King A. Natural killer cells and pregnancy. Nature Rev Immunol. 2002;2:656-663.

   Not in our library10.1038/nri886

4. 4.

   Hanna J, Goldman-Wohl D, Hamani Y, et al. Decidual NK cells regulate key developmental processes at the human fetal–maternal interface. Nature Med. 2006;12:1065-1074.

   Not in our library10.1038/nm1452

5. 5.

   Craven CM, Morgan T, Ward K. Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta. 1998;19:241-252.

   Not in our library10.1016/s0143-4004(98)90055-8

6. 6.

   Pijnenborg R, Bland JM, Robertson WB, et al. Uteroplacental arterial changes related to interstitial trophoblast migration in early human pregnancy. Placenta. 1983;4:397-413.

   Not in our library10.1016/s0143-4004(83)80043-5

7. 7.

   Kam EP, Gardner L, Loke YW, et al. The role of trophoblast in the physiological change in decidual spiral arteries. Hum Reprod. 1999;14:2131-2138.

   Not in our library10.1093/humrep/14.8.2131

8. 8.

   Ashton SV, Whitley GS, Dash PR, et al. Uterine spiral artery remodeling involves endothelial apoptosis induced by extravillous trophoblasts through Fas/FasL interactions. Arterioscler Thromb Vasc Biol. 2005;25:102-108.

   Not in our library10.1161/01.atv.0000148547.70187.89

9. 9.

   Harris LK, Keogh RJ, Wareing M, et al. Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a fas ligand-dependent mechanism. Am J Pathol. 2006;169:1863-1874.

   Not in our library10.2353/ajpath.2006.060265

10. 10.

    Red-Horse K, Rivera J, Schanz A, et al. Cytotrophoblast induction of arterial apoptosis and lymphangiogenesis in an in vivo model of human placentation. J Clin Invest. 2006;116:2643-2652.

    Not in our library10.1172/jci27306

11. 11.

    Keogh RJ, Harris LK, Freeman A, et al. Fetal-derived trophoblast use the apoptotic cytokine tumor necrosis factor-alpha-related apoptosis-inducing ligand to induce smooth muscle cell death. Circ Res. 2007;100:834-841.

    Not in our library10.1161/01.res.0000261352.81736.37

12. 12.

    James JL, Whitley GS, Cartwright JE. Shear stress and spiral artery remodelling: the effects of low shear stress on trophoblast-induced endothelial cell apoptosis. Cardiovasc Res. 2011;90:130-139.

    Not in our library10.1093/cvr/cvq396

13. 13.

    Smith SD, Dunk CE, Aplin JD, et al. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am J Pathol. 2009;174:1959-1971.

    Not in our library10.2353/ajpath.2009.080995

14. 14.

    Hazan AD, Smith SD, Jones RL, et al. Vascular–leukocyte interactions. Mechanisms of human decidual spiral artery remodeling in vitro. Am J Pathol. 2010;177:1017-1030.

    Not in our library10.2353/ajpath.2010.091105

15. 15.

    Croy BA, He H, Esadeg S, et al. Uterine natural killer cells: insights into their cellular and molecular biology from mouse modelling. Reproduction. 2003;126:149-160.

    Not in our library10.1530/rep.0.1260149

16. 16.

    Chakraborty D, Rumi MA, Konno T, et al. Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc Natl Acad Sci U S A. 2011;108:16295-16300.

    Not in our library10.1073/pnas.1109478108

17. 17.

    Meekins JW, Pijnenborg R, Hanssens M, et al. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol. 1994;101:669-674.

    Not in our library10.1111/j.1471-0528.1994.tb13182.x

18. 18.

    Pijnenborg R, Anthony J, Davey DA, et al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol. 1991;98:648-655.

    Not in our library10.1111/j.1471-0528.1991.tb13450.x

19. 19.

    Brosens I, Dixon HG, Robertson WB. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol. 1977;84:656-663.

    Not in our library10.1111/j.1471-0528.1977.tb12676.x

20. 20.

    Hiby SE, Apps R, Sharkey AM, et al. Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J Clin Invest. 2010;120:4102-4110.

    Not in our library10.1172/jci43998

21. 21.

    Hiby SE, Walker JJ, O'Shaughnessy KM, et al. Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med. 2004;200:957-965.

    Not in our library10.1084/jem.20041214

22. 22.

    Prefumo F, Sebire NJ, Thilaganathan B. Decreased endovascular trophoblast invasion in first trimester pregnancies with high-resistance uterine artery Doppler indices. Hum Reprod. 2004;19:206-209.

    Not in our library10.1093/humrep/deh037

23. 23.

    Melchiorre K, Wormald B, Leslie K, et al. First-trimester uterine artery Doppler indices in term and preterm pre-eclampsia. Ultrasound Obstet Gynecol. 2008;32:133-137.

    Not in our library10.1002/uog.5400

24. 24.

    Poon LC, Staboulidou I, Maiz N, et al. Hypertensive disorders in pregnancy: screening by uterine artery Doppler at 11–13 weeks. Ultrasound Obstet Gynecol. 2009;34:142-148.

    Not in our library10.1002/uog.6452

25. 25.

    Trundley A, Gardner L, Northfield J, et al. Methods for isolation of cells from the human fetal–maternal interface. Methods Mol Med. 2006;122:109-122.

    Not in our library10.1385/1-59259-989-3:109

26. 26.

    Choy MY, Whitley G, Manyonda IT. Efficient, rapid and reliable establishment of human trophoblast cell lines using poly-l-ornithine. Early Pregnancy: Biol Med. 2000;2:124-143.

    Not in our library

27. 27.

    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.

    Not in our library10.1038/sj.bjp.0702757

28. 28.

    Burrows TD, King A, Loke YW. Expression of adhesion molecules by endovascular trophoblast and decidual endothelial cells: implications for vascular invasion during implantation. Placenta. 1994;15:21-33.

    Not in our library10.1016/s0143-4004(05)80233-4

29. 29.

    Genbacev O, DiFederico E, McMaster M, et al. Invasive cytotrophoblast apoptosis in pre-eclampsia. Hum Reprod. 1999;14:59-66.

    Not in our library10.1093/humrep/14.suppl_2.59

30. 30.

    Quenby S, Farquharson R. Uterine natural killer cells, implantation failure and recurrent miscarriage. Reprod Biomed Online. 2006;13:24-28.

    Not in our library10.1016/s1472-6483(10)62012-3

31. 31.

    Williams PJ, Bulmer JN, Searle RF, et al. Altered decidual leucocyte populations in the placental bed in pre-eclampsia and foetal growth restriction: a comparison with late normal pregnancy. Reproduction. 2009;138:177-184.

    Not in our library10.1530/rep-09-0007

32. 32.

    Trundley A, Moffett A. Human uterine leukocytes and pregnancy. Tissue Antigens. 2004;63:1-12.

    Not in our library10.1111/j.1399-0039.2004.00170.x

33. 33.

    Lash GE, Otun HA, Innes BA, et al. Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Hum Reprod. 2010;25:1137-1145.

    Not in our library10.1093/humrep/deq050

34. 34.

    De Oliveira LG, Lash GE, Murray-Dunning C, et al. Role of interleukin 8 in uterine natural killer cell regulation of extravillous trophoblast cell invasion. Placenta. 2010;31:595-601.

    Not in our library10.1016/j.placenta.2010.04.012

35. 35.

    Hu Y, Dutz JP, MacCalman CD, et al. Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: a role for IFN-gamma. J Immunol. 2006;177:8522-8530.

    Not in our library10.4049/jimmunol.177.12.8522

36. 36.

    Liu J, Chakraborty C, Graham CH, et al. Noncatalytic domain of uPA stimulates human extravillous trophoblast migration by using phospholipase C, phosphatidylinositol 3-kinase and mitogen-activated protein kinase. Exp Cell Res. 2003;286:138-151.

    Not in our library10.1016/s0014-4827(03)00089-2

37. 37.

    Huang Y, Zhu XY, Du MR, et al. Chemokine CXCL16, a scavenger receptor, induces proliferation and invasion of first-trimester human trophoblast cells in an autocrine manner. Hum Reprod. 2006;21:1083-1091.

    Not in our library10.1093/humrep/dei436

38. 38.

    Leach RE, Kilburn B, Wang J, et al. Heparin-binding EGF-like growth factor regulates human extravillous cytotrophoblast development during conversion to the invasive phenotype. Dev Biol. 2004;266:223-237.

    Not in our library10.1016/j.ydbio.2003.09.026

39. 39.

    Uehara Y, Minowa O, Mori C, et al. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature. 1995;373:702-705.

    Not in our library10.1038/373702a0

40. 40.

    Furugori K, Kurauchi O, Itakura A, et al. Levels of hepatocyte growth factor and its messenger ribonucleic acid in uncomplicated pregnancies and those complicated by preeclampsia. J Clin Endocrinol Metab. 1997;82:2726-2730.

    Not in our library10.1210/jcem.82.8.4176

Cited by papers we hold 4

• Pathogenesis of Preeclampsia and Therapeutic Approaches Targeting the Placenta · 2020
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• Dynamic Function and Composition Changes of Immune Cells During Normal and Pathological Pregnancy at the Maternal-Fetal Interface · 2019
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• Preeclampsia: The Relationship between Uterine Artery Blood Flow and Trophoblast Function · 2019
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• Uterine Natural Killer Cells: Functional Distinctions and Influence on Pregnancy in Humans and Mice · 2017
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