Trophoblast cell line resistance to NK lysis mainly involves an HLA class I-independent mechanism

Journal of Immunology

Volumn 162, Issue 10, 1999, Pages 5902-5909

  Avril, Tony ^a   Jarousseau, Annie Claude ^a   Watier, Herve ^a   Boucraut, Jose ^b   Le Bouteiller, Philippe ^c   Bardos, Pierre ^a   Thibault, Gilles ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c CHU PURPAN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 1; INTERLEUKIN 2;

ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; BLOOD PLACENTA BARRIER; CELL LINE; CYTOKINE RELEASE; CYTOLYSIS; CYTOTROPHOBLAST; DOWN REGULATION; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNITY; LYMPHOKINE ACTIVATED KILLER CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; SYNCYTIOTROPHOBLAST; TROPHOBLAST;

ANTIGENS, CD; ANTIGENS, CD94; CELL LINE; CITRIC ACID; CYTOTOXICITY, IMMUNOLOGIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HLA-C ANTIGENS; HUMANS; KILLER CELLS, LYMPHOKINE-ACTIVATED; KILLER CELLS, NATURAL; LECTINS, C-TYPE; MEMBRANE GLYCOPROTEINS; RECEPTORS, IMMUNOLOGIC; TROPHOBLASTS;

EID: 0033563274     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. King, A., C. Boocock, A. M. Sharkey, L. Gardner, A. Beretta, A. G. Siccardi, and Y. W. Loke. 1996. Evidence for the expression of HLA-C class I mRNA and protein by human first trimester trophoblasl. J. Immunol. 156:2068.
2. Parham, P. 1996. Immunology: keeping mother at bay. Curr. Biol. 6:638.
3. Gobin, S. J. P., L. Wilson, V. Keijsers, and P. J. VandenElsen. 1997. Antigen processing and presentation by human trophoblast-derived cell lines. J. Immunol. 158:3587.
4. Harel-Bellan, A., A. Quillet, C. Marchiol, R. DeMars, T. Tursz, and D. Fradelizi. 1986. Natural killer susceptibility of human cells may be regulated by genes in the HLA region on chromosome 6. Proc. Natl. Acad. Sci. USA 83:5688.
5. Storkus, W. J., D. N. Howell, R. D. Salter, J. R. Dawson, and P. Cresswell. 1987. NK susceptibility varies inversely with target cell class I HLA antigen expression. J. Immunol. 138:1657.
6. 2-microglobulin-transfected Daudi cells. J. Immunol. 141:17.
7. Storkus, W. J., J. Alexander, J. Alan Payne, J. R. Dawson, and P. Cresswell. 1989. Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc. Natl. Acad. Sci. USA 86:2361.
8. Shimizu, Y., and R. DeMars. 1989. Demonstration by class I gene transfer that reduced susceptibility of human cells to natural killer cell-mediated lysis is inversely correlated with HLA class I antigen expression. Eur. J. Immunol. 19:447.
9. Kovats, S., E. K. Main, C. Librach, M. Stubblebine, S. J. Fisher, and R. DeMars. 1990. A class I antigen, HLA-G, expressed in human trophoblasts. Science 248:220.
10. McMaster, M. T., C. L. Librach, Y. Zhou, K. H. Lim, M. J. Janatpour, R. DeMars, S. Kovats, C. Damsky, and S. J. Fisher. 1995. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J. Immunol. 154:3771.
11. Starkey, P. M., I. L. Sargent, and C. W. G. Redman. 1988. Cell populations in human early decidua: characterization and isolation of large granular lymphocytes by flow cytometry. Immunology 65:129.
12. Bulmer, J. N. 1989. Decidual cellular responses. Curr. Opin. Immunol. 1:1141.
13. King, A., S. V, Welling, L. Garner, and Y. W. Loke. 1989. Immunohistochemical characterization of the unusual large granular lymphocytes in human endometrium throughout the menstrual cycle. Hum. Immunol. 24:195.
14. King, A., and Y. W. Loke. 1991. On the nature and function of human uterine granular lymphocytes. Immunol. Today 12:432.
15. - decidual and peripheral blood leukocytes. J. Immunol. 152:4255.
16. Chumbley, G., A. King, K. Robertson, N. Holmes, and Y. W. Loke. 1994. Resistance of HLA-G and HLA-A2 transfectants to lysis by decidual NK cells. Cell. Immunol. 155:312.
17. Pazmany, L., O. Mandelboim, M. Valesgomez, D. M. Davis, H. T. Reyburn, and J. L. Strominger. 1996. Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science 274:792.
18. Münz, C., N. Holmes, A. King, Y. W. Loke, M. Colonna, H. Schild, and H. G. Rammensee. 1997. Human histocompatibility leukocyte antigen (HLA)-G molecules inhibit NKAT3 expressing natural killer cells. J. Exp. Med. 185:385.
19. Perez-Villar, J. J., I. Melero, F. Navarro, M. Carretero, T. Bellon, M. Llano, M. Colonna, D. E. Geraghty, and M. Lopez-Botet. 1997. The CD94/NKG2-A inhibitory receptor complex is involved in natural killer cell-mediated recognition of cells expressing HLA-G1. J. Immunol. 153:5736.
20. Pende, D., S. Sivori, L. Accame, L. Pareti, M. Falco, D. Geraghty, P. Le Bouteiller, L. Moretta, and A. Moretta. 1997. HLA-G recognition by human natural killer cells: involvement of CD94 both as inhibitory and as activating receptor complex. Eur. J. Immunol. 27:1875.
21. Söderstrom, K., B. Corliss, L. L. Lanier, and J. H. Phillips. 1997. CD94/NKG2 is the predominant inhibitory receptor involved in recognition for HLA-G by decidual and peripheral blood NK cells. J. Immunol. 159:1072.
22. 1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors? Proc. Natl. Acad. Sci. USA 94:5249.
23. Rouas-Freiss, N., R. M. B. Goncalves, C. Menier, J. Dausset, and E. D. Carosella. 1997. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl. Acad. Sci. USA 94:11520.
24. Lazetic, S., C. Chang, J. P. Houchins, L. L. Lanier, and J. H. Phillips. 1996. Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits. J. Immunol. 157: 4741.
25. Sivori, S., M. Vitale, C. Bottino, E. Marcenaro, L. Sanseverino, S. Parolini, L. Moretta, and A. Moretta. 1996. CD94 functions as a natural killer cell inhibitory receptor for different HLA class I alleles: identification of the inhibitory form of CD94 by the use of novel monoclonal antibodies. Eur. J. Immunol. 26:2487.
26. Carretero, M., C. Cantoni, T. Bellon, C. Bottino, R. Biassoni, A. Rodriguez, J. J. Perez-Villar, L. Moretta, A. Moretta, and M. Lopez-Botet. 1997. The CD94 and NKG2-A C-type lectins covalently assemble to form a NK cell inhibitory receptor for HLA class I molecules. Eur. J. Immunol. 27:563.
27. Brooks, A. G., P. E. Posch, C. J. Scorzelli, F. Borrego, and J. E. Coligan. 1997. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med 185:795.
28. Borrego, F., M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks. 1998. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 187:813.
29. Braud, V. M., D. S. J. Allan, C. A. O'Callaghan, K. Söderstrom, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, L. L. Lanier, and A. J. McMichael. 1998. HLA-E binds to natural killer cell receptors CD94/ NKG2A, B and C. Nature 391:795.
30. Lee, N., M. Llano, M. Carreto, 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.
31. Lanier, L. L. 1998. Follow the leader: NK cell receptors for classical and non-classical MHC class I. Cell 92:705.
32. King, A., and Y. W. Loke. 1993. Effect of IFN-γ and IFN-α on killing of human trophoblast by decidual LAK cells. J. Reprod. Immunol. 23:51.
33. Guillaudeux, T., A. M. Rodriguez, M. Girr, V. Mallet, S. A. Ellis, I. L. Sargent, R. Fauchet, E. Alsat, and P. Le Bouteiller. 1995. Methylation status and transcriptional expression of the MHC class I loci in human trophoblast cells from term placenta. J. Immunol. 154:3283.
34. Loke, Y. W., A. King, T. Burrows, L. Gardner, M. Bowen, S. Hiby, S. Howlett, N. Holmes, and D. Jacobs. 1997. Evaluation of trophoblast HLA-G antigen with a specific monoclonal antibody. Tissue Antigens 50:135.
35. King, A., and Y. W. Loke. 1990. Human trophoblast and JEG choriocarcinoma cells are sensitive to lysis by IL-2-stimulated decidual NK cells. Cell. Immunol. 129:435.
36. Ferry, B. L., I. L. Sargent, P. M. Starkey, and C. W. G. Redman. 1991. Cytotoxic activity against trophoblast and choriocarcinoma cells of large granular lymphocytes from human early pregnancy decidua. Cell. Immunol. 132:140.
37. Patillo, R. A., A. Ruckert, R. Hussa, R. Berstein, and E. Deles. 1971. The JAR cell line, continuous human multihormone production and controls. In Vitro 6:398.
38. Kohler, P. O., and W. E. Bridson. 1971. Isolation of hormone producing clonal lines of human choriocarcinoma. J. Clin. Endocrinol. Metab. 32:683.
39. Boucraut, J., T. Guillaudeux, M. Alizadeh, J. Boretto, G. Chimini, F. Malecaze, G. Semana, R. Fauchet, P. Pontarotti, and P. Le Bouteiller. 1993. HLA-E is the only class-I gene that escapes CpG methylation and is transcriptionally active in the trophoblast-derived human cell line JAR. Immunogenetics 38:117.
40. Boucraut, J., R. Hakem, A. Gauthier, R. Fauchet, and P. Le Bouteiller. 1991. Transfected trophoblast-derived human cells can express a single HLA class I allelic product. Tissue Antigens 37:84.
41. Sugawara, S., T. Abo, and K. Kumagai. 1987. A simple method to eliminate the antigenicity of surface class I MHC molecules from the membrane of viable cells by acid treatment at pH 3. J. Immunol. Methods 100:83.
42. Thibault, G., and P. Bardos. 1995. Compared TCR and CD3∈ expression on αβ and γδ T cells: evidence for the association of two TCR heterodimers with three CD3∈ chains in the TCR complex. J. Immunol. 154:3814.
43. Moretta, A., M. Vitale, S. Sivori, C. Bottino, L. Morelli, R. Augugliaro, M. Barbaresi, D. Pende, E. Ciccone, M. Lopez-Botet, and L. Moretta. 1994. Human natural killer cell receptors for HLA-dass I molecules: evidence that the Kp43 (CD94) molecule functions as receptor for HLA-B alleles. J. Exp. Med. 180:545.
44. Sernee, M. F., H. L. Ploegh, and D. J. Schust. 1998. Why certain antibodies cross-react with HLA-A and HLA-G: epitope mapping of two common MHC class I reagents. Mol. Immunol. 35:177.
45. Moretta, A., C. Bottino, M. Vitale, D. Pende, R. Biassoni, M. C. Mingari, and L. Moretta. 1996. Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 14:619.
46. + T lymphocytes. I. Inhibition of the lL-2-dependent proliferation by anti-Kp43 monoclonal antibody. J. Immunol. 144:3238.
47. Gorelik, E., Y. Gunji, and R. B. Herberman. 1988. H-2 antigen expression and sensitivity of BL6 melanoma cells to natural killer cell cytotoxicity. J. Immunol. 140:2096.
48. Dennert, G., C. Landon, E. M. Lord, D. W. Bahler, and J. G. Frelinger. 1988. Lysis of a lung carcinoma by poly I:C-induced natural killer cells is independent of the expression of class I histocompatibility antigens. J. Immunol. 140:2472.
49. Chervenak, R., and R. M. Wolcott. 1988. Target cell expression of MHC antigens is not (always) a turn-off signal to natural killer cells. J. Immunol. 140:3712.
50. b antigen expression has no effect on natural killer susceptibility and tumorigenicity of a murine hepatoma. J. Immunol. 141:4403.
51. Leiden, J. M., B. A. Karpinski, L. Gottschalk, and J. Kornbluth. 1989. Susceptibility to natural killer cell-mediated cytolysis is independent of the level of target cell class I HLA expression. J. Immunol. 142:2140.
52. Stam, N. J., W. M. Kast, A. C. Voordouw, L. B. Pastoors, F. A. VanderHoeven, C. F. Melief, and H. L. Ploegh. 1989. Lack of correlation between levels of MHC class I antigen and susceptibility to small cellular lung carcinoma (SCLC) by natural killer cells. J. Immunol. 142:4113.
53. Litwin, V., J. Gumperz, P. Parham, J. H. Phillips, and L. L. Lanier. 1993. Specificity of HLA class I antigen recognition by human NK clones: evidence for clonal heterogeneity, protection by self and non-self alleles, and influence of the target cell type. J. Exp. Med. 178:1321.
54. King, A., P. Kalra, and Y. W. Loke. 1990. Human trophoblast cell resistance to decidual NK lysis is due to lack of NK target structure. Cell. Immunol. 127:230.
55. Jarousseau, A. C., G. Thibault, P. Reverdiau, A. M. Rodriguez, M. Lacord, J. De Russe, H. Watier, D. Degenne, Y. Lebranchu, Y. Gruel, P. LeBouteiller, and P. Bardos. 1994. Adhesive properties of choriocarcinoma cells toward lymphocytes activated or not by interleukin-2. Cell. Immunol. 157:38.