Decidual natural killer cell receptor expression is altered in pregnancies with impaired vascular remodeling and a higher risk of pre-eclampsia

Journal of Leukocyte Biology

Volumn 97, Issue 1, 2015, Pages 79-86

  Wallace, Alison E ^a   Whitley, Guy S ^a   Thilaganathan, Baskaran ^b   Cartwright, Judith E ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^b ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

Chemokine; LILRB1 KIR; Trophoblast

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA C ANTIGEN; HLA G ANTIGEN; NATURAL KILLER CELL RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL FUNCTION; CELL ISOLATION; COCULTURE; CONTROLLED STUDY; DECIDUA; DOPPLER ECHOCARDIOGRAPHY; FEMALE; FIRST TRIMESTER PREGNANCY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; RISK ASSESSMENT; TROPHOBLAST; UTERINE ARTERY; VASCULAR REMODELING; CYTOLOGY; DOPPLER FLOWMETRY; ECHOGRAPHY; IMMUNOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK FACTOR;

DECIDUA; FEMALE; FLOW CYTOMETRY; HUMANS; PRE-ECLAMPSIA; PREGNANCY; RECEPTORS, NATURAL KILLER CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RISK FACTORS; ULTRASONOGRAPHY, DOPPLER; UTERINE ARTERY; VASCULAR REMODELING;

EID: 84925286448     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.2A0614-282R     Document Type: Article

References (45)

1. Koopman, L. A., Kopcow, H. D., Rybalov, B., Boyson, J. E., Orange, J. S., Schatz, F., Masch, R., Lockwood, C. J., Schachter, A. D., Park, P. J., Strominger, J. L. (2003) Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198, 1201-1212.
2. Hanna, J., Goldman-Wohl, D., Hamani, Y., Avraham, I., Greenfield, C., Natanson-Yaron. S., Prus, D., Cohen-Daniel, L., Arnon, T. I., Manaster, I., Gazil, R., Yutkin, V., Benharroch, D., Porgador, A., Keshel, E., Yagel, S., Mandelboim, O. (2006) Decidual NK cells regulate key- developmental processes at the human fetal-maternal interface. Nat. Med. 12, 1065-1074.
3. Wallace, A. E., Fraser, R., Cartwright, J. E. (2012) Extra villous trophoblast and decidual natural killer cells: a remodelling partnership. Hum. Repord. Update 18, 458-471.
4. Hiby, S. E., Apps, R., Sharkey, A. M., Farrell, L. E., Gardner, L., Mulder, A., Claas, F. H., Walker, J. J., Redman, C. W., Morgan, L., Tower, G, Regan, L., Moore, G. E., Carrington, M., Moffett, A. (2010) Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2. J. Clin. Invest. 120, 4102-4110.
5. Hiby, S. E., Walker, J. J., O'Shaughnessy, K. M., Redman, C. W., Carrington M., Trowsdale J., Moffett, A. (2004) Combinations of maternal KIR and fetal HLA-C genes influence the- risk of preeclampsia and reproductive success. J. Exp. Med. 200, 957-965.
6. Hiby, S. E., Regan L., Lo, W., Farrell, I., Carrington, M., Moffett, A. (2008) Association of maternal killer-cell immunoglobulin-like receptors and parental HI A-C genotypes with recurrent miscarriage. Hum. Reprod. 23, 972-976.
7. Wallace, A. E., Host, A. J., Whitley, G. S., Cartwright,J. E. (2013) Decidual natural killer cell interactions with trophoblasts are impaired in pregnancies at increased risk of preeclampsia. Am. J. Pathol. 183, 1853-1861.
8. Cartwright, J. E., Fraser, R., Leslie, K., Wallace, A. E., James J. L. (2010) Remodelling at the maternal-fetal interface: relevance to human pregnancy disorders. Reproduction 140, 803-813.
9. Ashton, S. V., Whiüey, G. S., Dash, P. R., Wareing, M., Crocker, I. P., Baker, P. N., Cartwright, J. E. (2005) Uterine spiral artery remodeling involves endothelial apoptosis induced by extravillous trophoblasts through Fas/FasL interactions. Arterioscler. Thromb. Vase. Biol. 25, 102-108.
10. Harris, L. K., Keogh, R. J., Wareing, M., Baker, P. N., Cartwright, J. E., Aplin, J. D., Whitley, G. S. (2006) Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a Fas ligand-dependent mechanism. Am. J. Pathol. 169, 1863-1874.
11. Wallace, A. E., Cartwright, J. E., Begum, R., Laing, K., Thilaganathan, B., Whiüey, G. S. (2013) Trophoblast-induced changes in Gx-C motif chemokine 10 expression contribute to vascular smooth muscle cell dedifferentiation during spiral artery remodeling. Artetioscler. Thromb. Vase. Biol. 33, e93-e101.
12. Zhou, Y., Fisher, S.J.,Janatpour, M., Genbacev, O., Dejana, E., Wheeloek, M., Damsky, C. H. (1997) Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest. 99, 2139-2151.
13. Chazara, O., Xiong, S., Moffett, A. (2011) Maternal KIR and fetal HIA-C: a fine balance. J. Leukoc. Biol 90, 703-716.
14. Male, V., Sharkey, A., Masters, L., Kennedy, P. R., Farrell, I. E., Moffett, A. (2011) The effect of pregnancy on the uterine NKcell KIR repertoire. Eur. J. Immunol. 41, 3017-3027.
15. El Costa, H., Tabiasco, J., Bcrrebi, A., Parant, O., Aguerrc-Girr, M., Piccinni, M. P., Le Bouteiller, P. (2009) Effector functions of human decidual NK cells in healthy early pregnancy are dependent on the specific engagement of natural cytotoxicity receptors. J. Reprod. Immunol. 81, 142-147.
16. Brosens, I., Dixon, H. G., Robertson, W. B. (1977) Fetal growth retardation and the arteries of the placental bed. Br. J. Obstet. Gynaecol. 84, 656-663.
17. Brosens, I. A., Robertson, W. B., Dixon, H. G. (1972) The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet. Gynecol. Annu. 1, 177-191.
18. Melchiorre, K., Wormald, B., Leslie, K., Bhide, A., Thilaganathan, B. (2007) First-trimester uterine artery Doppler indices in term and preterm pre-eclampsia. Ultrasound Obstet. Gynecol. 32, 133-137.
19. Prefumo, F., Sebire, N. J., Thilaganathan, B. (2004) Decreased endovascular trophoblast invasion in first trimester pregnancies with high-resistance uterine artery Doppler indices. Hum. Reprod. 19, 206-209.
20. Fraser, R., Whitley, G. S., Johnstone, A. P., Host, A. J., Sebire, N. J., Thilaganathan, B., Cartwright, J. E. (2012) Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J. Pathol. 228, 322-332.
21. Whitley, G. S., Dash, P. R., Ayling, L. J., Prefumo, F., Thilaganathan B., Cartwright, J. E. (2007) Increased apoptosis in first trimester extravillous trophoblasts from pregnancies at higher risk of developing preeclampsia. Am. J. Pathol. 170, 1903-1909.
22. Morandi, F., Ferretti, E., Castriconi, R., Dondero, A., Petretto, A., Bottino, C., Pistoia, V. (2011) Soluble H1A-G dampens CD94/NKG2A expression and function and differentially modulates chemotaxis and cytokine and chemokine secretion in CD56brighl and CD56dim NK cells. Blood 118, 5840-5850.
23. McCormick, J., Whitley, G. S., Le Bouteiller, P., Cartwright, J. E. (2009) Soluble HI A-G regulates motility and invasion of the trophoblast-derived cell line SGHPL-4. Hum. Reprod. 24, 1339-1345.
24. El Costa, H., Casemayou, A., Aguerre-Girr, M., Rabot, M., Berrebi, A., Parant, O., Clouet-Delannoy, M., Lombardelli, L., Jabrane-Ferrat, N., Rukavina, D., Bensussan, A., Piccinni M. P., Le Bouteiller, P., Tabiasco, J. (2007) Critical and differential roles of NKp46- and NKpSO-activating receptors expressed by uterine NK cells in early pregnancy. J. Immunol. 181, 3009-3017.
25. Le Bouteiller, P., Tabiasco, J., Polgar, B., Kozma, N., Giustiniani, D., Siewiera, J., Berrebi, A., Aguere-Giir, M., Bensussan, A., Jabrane-Ferrat, N. (2011) CD 160: a unique activating NK cell receptor. Immunol. Lett. 138, 98-96.
26. Marlin, R., Duriez, M., Bcrkane, N., de Truchis, C., Madec, Y., Rey-Cuille, M. A., Cummings, J. S., Cannou, C., Quillay, H., Barrć-Sinoussi, F., Nugeyre, M. T., Menu, E., et al. (2012) Dynamic shift from CD85j/ILT-2 to NKG2D NK receptor expression pattern on human decidual NK during the first trimester of pregnancy. PLoS ONE 7, e30017.
27. Sharkey, A. M., Gardner, L., Hiby, S., Farrell, L., Apps, R., Masters, L., Goodridge J., Lathbury, L., Stewart, C. A., Venma, S., Moffett, A. (2008) Killer Ig-like receptor expression in uterine NK cells is biased toward recognidon of HIA-C and alters witli gestational age. J. Immunol 181, 39-46.
28. Lash, G. E., Otun, H. A., Innes, B. A., Percival, K., Searle, R. F., Robson, S. C., Buhner, J. N. (2010) Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Hum. Reprod. 25,1137-1145.
29. Naruse, K, Innes, B. A., Bulmer J. N., Robson, S. C., Searle, R. F., Lash, F. E. (2010) Secretion of cytokines by villous cytotrophoblast and extravillous trophoblast in the first trimester of human pregnancy. J. Reprod. Immunol. 86, 148-150.
30. Moffctt-King, A. (2002) Natural killer cells and pregnancy. Nat. Rev. Immunol. 2, 656-663.
31. Manaster, I., Mizrahi, S., Goldman-Wohl, D., Sela, H. Y., Stern-Ginossar, N., Lankry, D., Gruda, R., Hurwitz, A., Bdolah, Y., Haimov-Kochman, R., Yagel, S., Mandelboim, O. (2008) Endometrial NK cells arc special immature cells that await pregnancy. J. Immunol. 181, 1869-1876.
32. Vacca, P., Pietra, G., Falco, M., Romeo, E., Bottino, C., Bellora, F., Prefumo, F., Fulcheri, E., Venturini, P. L., Costa, M., Moretta, A., Moretta, L., Mingari, M. C. (2006) Analysis of natural killer cells isolated from human decidua: Evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-ccll function. Blood 108, 4078-4085.
33. Vacca, P., Gantoni, C., Prato, C., Fulcheri, E., Moretta, A., Moretta, L., Mingari, M. C. (2008) Regulatory role of NKp44, NKp46, DNAM-1 and NKG2D receptors in the interaction between NK cells and trophoblast cells. Evidence for divergent functional profiles of decidual versus peripheral NK cells. Int. Immunol. 20, 1395-1405.
34. Siewiera, J., El Costa, H., Tabiasco, J., Berrebi, A., Cartron, G., Le Bouteiller, P., Jabrane-Ferrat, N. (2013) Human cytomegalovirus infection elicits new decidual natural killer cell effector functions. PLoS Pathog. 9, e1003257.
35. Xiong, S., Sharkey, A. M., Kennedy, P. R., Gardner, L., Farrell, L. E., Chazara, O., Bauer, J., Hiby, S. E., Golucci, F., Moffett, A. (2013) Maternal uterine NK cell-activating receptor KIR2DS1 enhances placentation. J. Clin. Invest 123, 4264-4272.
36. Shiroishi, M., Tsumoto, K, Amano, K, Shirakihara, Y., Colonna M Braud, V. M., Allan, D. S., Makadzange, A., Rowland-Jones, S., Willcox B., Jones, E. Y., van der Merwe, P. A., Kumagai, I., Maenaka, K. (2003) Human inhibitory receptors Ig-like transcript 2 (ILT2) and II.T4 compete with CD8 for MHC class I binding and bind preferentially t HLA-G. Proc. Natl. Acad. Sci. USA 100, 8856-8861.
37. Apps, R., Gardner, I., Sharkey, A. M., Holmes, N., Moffett, A. (2007) A homodimeric complex of HLA-G on normal trophoblast cells modulat antigen-presenting cells via LILRB1. Eur. J. Immunol. 37, 1924-1937
38. Favier, B., Lemaoult, J., Lesport, E., Carosella, E. D. (2010) II.T2/HLA-G interaction impairs NK-cell functions through the inhibition of the lat ' but not the early events of the NK-cell activating synapse. FASEB J. 24, 689-699.
39. Heidenreich, S., Zu Eulenburg, C., Hildebrandt, Y., Stübig, T., Sierich G., Badbaran, A., Eiermann, T. H., Binder, T. M., Kröger, N. (2012) Impact of the NK cell receptor LIR-1 (ILT-2/CD85j/LILRBl) on cytotoxicity against multiple myeloma. Clin. Dev. Immunol. 2012, 652130
40. Li, C., Houser, B. L., Nicotra, M. L., Strominger, J. L. (2009) HLA-G homodimer-induced cytokine secretion through HIA-G receptors on human decidual macrophages and natural killer cells. Proc Natl Acad. Sci. USA 106, 5767-5772.
41. Apps, R., Sharkey, A., Gardner, L., Male, V., Kennedy, P., Masters I., Farrell, L., Jones, D., Thomas, R., Moffett, A. (2011) Ex vivo functional responses to HIA-G differ between blood and decidual NK cells Mol. Hum. Reprod. 17, 577-586.
42. Otun, H. A., Lash, G. E., Innes, B. A., Bulmer J. N., Naruse, K. Hann, T., Searle, R. F., Robson, S. C. (2011) Effect of tumour necrosis factor-α in combination with interferon-γ on first trimester extravillous trophoblast invasion. J. Reprod. Immunol. 88, 1-11.
43. Huber, A. V., Saleh, L., Bauer, S., Husslein, P., Knöfler, M. (2006) TNFalpha-mediated induction of PAI-1 restricts invasion of HTR-8/ SVneo trophoblast cells. Placenta 27, 127-136.
44. Xu, B., Nakhla, S., Makris, A., Hennessy, A. (2011) TNF-α inhibits trophoblast integration into endothelial cellular networks Placenta 32, 241-246.
45. Kopcow, H. D., Allan, D. S., Chen, X., Rybalov, B., Andzelm, M. M., Ge, B., Strominger, J. L. (2005) Human decidual NK cells form immature activating synapses and are not cytotoxic. Proc. Natl. Acad. Sci USA 102, 15563-15568.