Interaction between uterine natural killer cells and extravillous trophoblast cells: Effect on cytokine and angiogenic growth factor production

Human Reproduction

Volumn 26, Issue 9, 2011, Pages 2289-2295

  Lash, Gendie E ^a   Naruse, Katsuhiko ^a   Robson, Andrew ^a   Innes, Barbara A ^a   Searle, Roger F ^a   Robson, Stephen C ^a   Bulmer, Judith N ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

angiogenic growth factors; co culture; cytokines; EVT; pregnancy; uNK cell; villous cytotrophoblast

Indexed keywords

ANGIOGENIC FACTOR; ANGIOPOIETIN 1; ANGIOPOIETIN 2; CYTOKINE; FIBROBLAST GROWTH FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; PLACENTAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN A; VASCULOTROPIN C;

ARTICLE; CELL CONTACT; CELL INTERACTION; CELL TYPE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOTROPHOBLAST; ENZYME LINKED IMMUNOSORBENT ASSAY; EX VIVO STUDY; EXTRAVILLOUS TROPHOBLAST; FEMALE; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; NATURAL KILLER CELL; TROPHOBLAST; UTERINE NATURAL KILLER;

EID: 80051943555     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/der198     Document Type: Article

References (29)

1. Apps R, Murphy SP, Fernando R, Gardner L, Ahad T, Moffett A. Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies. Immunology 2009;127:26-39.
2. Bilban M, Tauber S, Haslinger P, Pollheimer J, Saleh L, Pehamberger H, Wagner O, Knöfler M. Trophoblast invasion: assessment of cellular models using gene expression signatures. Placenta 2010; 31:989-996.
3. Bischof P, Irminger-Finger I. The human cytotrophoblastic cell, a mononuclear chameleon. Int J Biochem Cell Biol 2005;37:1-16. (Pubitemid 39286016)
4. Bulmer JN, Lash GE. Human uterine natural killer cells: a reappraisal. Mol Immunol 2005;42:511-521. (Pubitemid 39655962)
5. Distler JH, Hirth A, Kurowska-Stolarska M, Gay RE, Gay S, Distler O. Angiogenic and angiostatic factors in the molecular control of angiogenesis. Q J Nucl Med 2003;47:149-161. (Pubitemid 37279152)
6. Engert S, Rieger L, Kapp M, Becker JC, Dietl J, Kammerer U. Profiling chemokines, cytokines and growth factors in human early pregnancy decidua by protein array. Am J Reprod Immunol 2007; 58:129-137. (Pubitemid 47097379)
7. Gude NM, Roberts CT, Kalionis B, King RG. Growth and function of the normal human placenta. Thromb Res 2004;114:397-407. (Pubitemid 39422572)
8. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I et al. Decidual NK cells regulate key developmental processes at human fetal-maternal interface. Nat Med 2006;12:1065-1074. (Pubitemid 44353388)
9. 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. (Pubitemid 44893814)
10. Jokhi PP, King A, Loke YW. Cytokine production and cytokine receptor expression by cells of the human first trimester placental-uterine interface. Cytokine 1997;9:126-137. (Pubitemid 27116888)
11. Kanai T, Fujii T, Unno N, Yamashita T, Hyodo H, Miki A, Hamai Y, Kozuma S, Taketani Y. Human leukocyte antigen-G-expressing cells differently modulate the release of cytokines from mononuclear cells present in the decidua versus peripheral blood. Am J Reprod Immunol 2001;45:94-99. (Pubitemid 32111904)
12. Kharfi A, Giguere Y, Sapin V, Masse J, Dastugue B, Forest JC. Trophoblastic remodeling in normal and preeclamptic pregnancies: implication of cytokines. Clin Biochem 2003;36:323-331. (Pubitemid 36776800)
13. Lala PK, Chakraborty C. Factors regulating trophoblast migration and invasiveness: possible derangements contributing to pre-eclampsia and fetal injury. Placenta 2003;24:575-587. (Pubitemid 37203312)
14. Lash GE, Schiessl B, Kirkley M, Innes BA, Cooper A, Searle RF, Robson SC, Bulmer JN. Expression of angiogenic growth factors by uterine natural killer cells during early pregnancy. J Leukoc Biol 2006; 80:572-580. (Pubitemid 44835791)
15. Lash GE, Otun HA, Innes BA, Percival K, Searle RF, Robson SC, Bulmer JN. Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age. Hum Reprod 2010a; 25:1137-1145.
16. Lash GE, Robson SC, Bulmer JN. Review: functional role of uterine natural killer (uNK) cells in human early pregnancy decidua. Placenta 2010b; 31:S87-S92.
17. Lash GE, Naruse K, Innes BA, Robson SC, Searle RF, Bulmer JN. Secretion of angiogenic growth factors by villous cytotrophoblast and extravillous trophoblast in early human pregnancy. Placenta 2010c; 31:545-548.
18. Li XF, Charnock-Jones DS, Zhang E, Hiby S, Malik S, Day K, Licence D, Bowen JM, Gardner L, King A et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 2001;86:1823-1834. (Pubitemid 32374944)
19. Naruse K, Innes BA, Bulmer JN, Robson SC, Searle RF, Lash GE. Secretion of cytokines by extravillous trophoblast, cytotrophoblast and uterine natural killer cells in the first trimester of human pregnancy. J Reprod Immunol 2010;86:148-150.
20. Ntrivalas E, Kwak-Kim J, Beaman K, Mantouvalos H, Gilman-Sachs A. An in vitro coculture model to study cytokine profiles of natural killer cells during maternal immune cell-trophoblast interactions. J Soc Gynecol Investig 2006;13:196-202.
21. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006;27:939-958. (Pubitemid 44204033)
22. Rieger L, Kammerer U, Hofmann J, Sutterlin M, Dietl J. Choriocarcinoma cells modulate the cytokine production of decidual large granular lymphocytes in coculture. Am J Reprod Immunol 2001;46:137-143. (Pubitemid 32691196)
23. Rieger L, Hofmeister V, Probe C, Dietl J, Weiss EH, Steck T, Kammerer U. Th1-and Th2-like cytokine production by first-trimester decidual large granular lymphocytes is influenced by HLA-G and HLA-E. Mol Hum Reprod 2002;8:255-261. (Pubitemid 34196352)
24. Saito S, Nishikawa K, Morii T, Enomoto M, Narita N, Motooshi K, Ichijo M. Cytokine production by CD162CD56bright natural killer cells in the human early pregnancy decidua. Int Immunol 1993;5:559-563. (Pubitemid 23162525)
25. Smith SD, Dunk CE, Aplin JD, Harris LK, Jones RL. Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy. Am J Pathol 2009;174:1959-1971.
26. Tarrade A, Kuen RL, Malassine A, Tricottet A, Blain P, Vidaud M, Evain-Brion D. Characterization of human villous and extravillous trophoblasts isolated from first trimester placenta. Lab Invest 2001;81:1199-1211. (Pubitemid 32911969)
27. Van der Meer A, Lukassen HGM, van Lierop MJC, Wijnands F, Mosselman S, Braat DDM, Joosten I. Membrane-bound HLA-G activates proliferation and interferon-g production by uterine natural killer cells. Mol Hum Reprod 2004;10:189-195. (Pubitemid 38456021)
28. Van der Meer A, Lukassen HG, van Cranenbroek B, Weiss EH, Braat DD, van Lierop MJ, Joosten I. Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells. Mol Hum Reprod 2007;13:123-133. (Pubitemid 46152599)
29. 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. (Pubitemid 28144987)