Decidual NK cells alter in vitro first trimester extravillous cytotrophoblast migration: A role for IFN-γ

Journal of Immunology

Volumn 177, Issue 12, 2006, Pages 8522-8530

  Hu, Yuxiang ^a,b   Dutz, Jan P ^a,b   MacCalman, Colin D ^a,b   Yong, Paul ^a,b   Tan, Rusung ^a,b   Von Dadelszen, Peter ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GELATINASE A; GELATINASE B; NEUTRALIZING ANTIBODY; PLASMINOGEN ACTIVATOR INHIBITOR 1;

APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CHORION VILLUS; COCULTURE; CONTROLLED STUDY; CYTOTROPHOBLAST; DECIDUA; EXPLANT; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRAUTERINE GROWTH RETARDATION; NATURAL KILLER CELL; PLACENTA ACCRETA; PREECLAMPSIA; PRIORITY JOURNAL; SPONTANEOUS ABORTION;

EID: 33845438523     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.12.8522     Document Type: Article

References (46)

1. Khong, T. Y., F. De Wolf, W. B. Robertson, and I. Brosens. 1986. Inadequate maternal vascular response to placentation in pregnancies complicated by preeclampsia and by small-for-gestational age infants. Br. J. Obstet. Gynaecol. 93: 1049-1059.
2. Bulmer, J. N. 1992. Immune aspects of pathology of the placental bed contributing to pregnancy pathology. Baillieres Clin. Obstet. Gynaecol. 6: 461-488.
3. Parham, P. 2004. NK cells and trophoblasts: partners in pregnancy. J. Exp. Med. 200: 951-955.
4. Starkey, P. M., L. L. Sargent, and C. W. G. Redman. 1988. Cell populations in human early pregnancy decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 65: 129-134.
5. King, A., and Y. W. Loke. 1991. On the nature and function of human uterine granular lymphocytes. Immunol. Today 12: 432-435.
6. Meekins, J. W., R. Pijnenborg, M. Hanssens, I. R. McFadyen, and A. van Assche. 1994. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol. 101: 669-674.
7. Stallmach, T., G. Hebisch, P. Orban, and X. Lu. 1999. Aberrant positioning of trophoblast and lymphocytes in the feto-maternal interface with pre-eclampsia. Virchows Arch. 434: 207-211.
8. King, A., S. E. Hiby, L. Gardner, S. Joseph, I. M. Bowen, S. Verma, T. D. Burrows, and Y. W. Loke. 2000. Recognition of trophoblast HLA class I molecules by decidual NK cell receptors: a review. Placenta 21(Suppl. A): S81-S85.
9. King, A., D. S. Allan, M. Bowen, S. I. Powis, S. Joseph, S. Verma, S. E. Hiby, A. J. McMichael, Y. W. Loke, and V. M. Braud. 2000. HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur. J. Immunol. 30: 1623-1631.
10. Le Gal, F. A., B. Riteau, C. Sedlik, I. Khalil-Daher, C. Menier, I. Dausset, J. G. Guillet, E. D. Carosella, and N. Rouas-Freiss. 1999. HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes. Int. Immunol. 11: 1351-1356.
11. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. Lopez-Botet, and D. E. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95: 5199-5204.
12. Ashkar, A. A., G. P. Black, Q. Wei, H. He, L. Liang, J. R. Head, and B. A. Croy. 2003. Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J. Immunol. 171: 2937-2944.
13. Verma, S., S. E. Hiby, Y. W. Loke, and A. King. 2000. Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol. Reprod. 62: 959-968.
14. 4 in human trophoblast and its loss from extravillous cells. Placenta 14: 203-215.
15. Damsky, C. H., M. L. Fitzgerald, and S. J. Fisher. 1992. Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Invest. 89: 210-222.
16. 1. Biol. Reprod. 60: 828-838.
17. Bauer, S., J. Pollheimer, J. Hartmann, P. Husslein, J. D. Aplin, and M. Knofler. 2004. Tumor necrosis factor-α inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J. Clin. Endocrinol. Metab. 89: 812-822.
18. Caniggia, I., C. V. Taylor, J. W. K. Ritchie, S. J. Lye, and M. Letarte. 1997. Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 138: 4977-4988.
19. Bocher, W. O., S. Herzog-Hauff, J. Schlaak, K. H. Meyer zum Buschenfeld, and H. F. Lohr. 1999. Kinetics of hepatitis B surface antigen-specific immune responses in acute and chronic hepatitis B or after HBs vaccination: stimulation of the in vitro antibody response by interferon γ. Hepatology 29: 238-244.
20. Dallalio, G., M. North, and R. T. Means, Jr. 1996. Inhibition of marrow CFU-E colony formation from human immunodeficiency virus-infected patients by β- and γ-interferon. Am. J. Hematol. 53: 118-120.
21. Haddad, E. K., A. J. Duclos, E. Antecka, W. S. Lapp, and M. G. Baines. 1997. Role of interferon-γ in the priming of decidual macrophages for nitric oxide production and early pregnancy loss. Cell. Immunol. 181: 68-75.
22. Hunt, J. S., R. Atherton, and J. L. Pace. 1990. Differential responses of rat trophoblast cells and embryonic fibroblasts to cytokines that regulate proliferation and class I MHC antigen expression. J. Immunol. 145: 184-189.
23. Redline, R. W. 2000. Role of uterine natural killer cells and interferon γ in placental development. J. Exp. Med. 192: F1-F4.
24. + lymphoid cells in human first trimester pregnancy decidua as a source of novel transforming growth factor-β2-related immunosuppressive factors. Hum. Reprod. 9: 2270-2277.
25. Albertsson, P., K. M. Kim, L. E. Jonges, R. P. Kitson, P. J. Kuppen, B. R. Johansson, U. Nannmark, and R. H. Goldfarb. 2000. Matrix metalloproteinases of human NK cells. In Vivo 14: 269-276.
26. Vigano, P., B. Gaffuri, E. Somigliana, M. Infantino, M. Vignali, and A. M. Di Blasio. 2001. Interleukin-10 is produced by human uterine natural killer cells but does not affect their production of interferon-γ. Mol. Hum. Reprod. 7: 971-977.
27. Roth, I., and S. J. Fisher. 1999. IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion. Dev. Biol. 205: 194-204.
28. Irving, J. A., and P. K. Lala. 1995. Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-β, IGF-II, and IGFBP-1. Exp. Cell Res. 217: 419-427.
29. Karmakar, S., and C. Das. 2002. Regulation of trophoblast invasion by IL-1β and TGF-β1. Am. J. Reprod. Immunol. 48: 210-219.
30. Vivovac, L., C. J. Jones, and J. D. Aplin. 1995. Trophoblast differentiation during formation of anchoring villi in a model of the early human placenta in vitro. Placenta 16: 41-56.
31. 1. Biol. Reprod. 60: 828-838.
32. Lacey, H., T. Haigh, M. Westwood, and J. D. Aplin. 2002. Mesenchymally-derived insulin-like growth factor 1 provides a paracrine stimulus for trophoblast migration. BMC Dev. Biol. 2: 5-12.
33. Leach, R. E., B. Kilburn, J. Wang, Z. Liu, R. Romero, and D. R. Armant. 2004. Heparin-binding EGF-like growth factor regulates human extravillous cytotrophoblast development during conversion to the invasive phenotype. Dev. Biol. 266: 223-237.
34. Fink, L., W. Seeger, L. Ermert, J. Hanze, U. Stahl, F. Grimminger, W. Kummer, and R. M. Bohle. 1998. Real-time quantitative RT-PCR after laser-assisted cell picking. Nat. Med. 4: 1329-1333.
35. Hall, L. A., C. M. Krauthauser, R. S. Wexler, M. G. Hollingshead, A. M. Slee, and J. S. Kerr. 2000. The hollow fiber assay: continued characterization with novel approaches. Anticancer Res. 20: 903-911.
36. Kim, M. H., R. P. Kitson, P. Albertsson, U. Nannmark, P. H. Basse, P. J. Kuppen, M. E. Hokland, and R. H. Goldfarb. 2000. Secreted and membrane-associated matrix metalloproteinases of IL-2-activated NK cells and their inhibitors. J. Immunol. 164: 5883-5889.
37. Han, Y. P., Y. D. Nien, and W. L. Garner. 2002. Tumor necrosis factor-α-induced proteolytic activation of pro-matrix metalloproteinase-9 by human skin is controlled by down-regulating tissue inhibitor of metalloproteinase-1 and mediated by tissue-associated chymortypsin-like proteinase. J. Biol. Chem. 277: 27319-27327.
38. Tsuda, H., M. Sakai, T. Michimata, K. Tanebe, S. Hayakawa, and S. Saito. 2001. Characterization of NKT cells in human peripheral blood and decidual lymphocytes. Am. J. Reprod. Immunol. 45: 295-302.
39. Lidstrom, C., L. Matthiesen, G. Berg, S. Sharma, J. Ernerudh, and C. Ekerfelt. 2003. Cytokine secretion patterns of NK cells and macrophages in early human pregnancy decidua and blood: implications for suppressor macrophages in decidua. Am. J. Reprod. Immunol. 40: 444-452.
40. Croy, B. A., H. He, S. Esadeg, Q. Wei, D. McCartney, J. Zhang, A. Borzychowski, A. A. Ashkar, G. P. Black, S. S. Evans, et al. 2003. Uterine natural killer cells: insights into their cellular and molecular biology from mouse modelling. Reproduction 126: 149-160.
41. Lash, G. E., H. A. Otun, B. A. Innes, J. N. Bulmer, R. F. Searle, and S. C. Robson. 2005. Inhibition of trophoblast cell invasion by TGFB1, 2, and 3 is associated with a decrease in active proteases. Biol. Reprod. 74: 403-409.
42. Koopman, L. A., H. D. Kopcow, B. Rybalov, J. E. Boyson, J. S. Orange, F. Schatz, R. Masch, C. J. Lockwood, A. D. Schachter, P. J. Park, and J. L. Strominger. 2003. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J. Exp. Med. 198: 1201-1212.
43. Rouy, D., I. Ernens, C. Jeanty, and D. R. Wagner. 2005. Plasma storage at -80 degrees C does not protect matrix metalloproteinase-9 from degradation. Anal. Biochem. 338: 294-298.
44. Liu, J., C. Chakraborty, C. H. Graham, Y. P. Barbin, S. J. Dixon, and P. K. Lala. 2003. Noncatalytic domain of uPA stimulates human extravillous trophoblast migration by using phospholipase C, phosphatidylinositol 3-kinase and mitogen-activated protein kinase. Exp. Cell Res. 286: 138-151.
45. + dendritic cells. Am. J. Pathol. 157: 159-169.
46. Kammerer, U., A. O. Eggert, M. Kapp, A. D. McLellan, T. B. Geijtenbeek, J. Dietl, Y. van Kooyk, and E. Kampgen. 2003. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am. J. Pathol. 162: 887-896.