Role of HLA-G in innate immunity through direct activation of NF-κB in natural killer cells

Molecular Immunology

Volumn 45, Issue 2, 2008, Pages 419-427

  Guillard, Christine ^a   Zidi, Inès ^a   Marcou, Céline ^a   Menier, Catherine ^a   Carosella, Edgardo D ^a   Moreau, Philippe ^a  

^a Inst Univ d'Hématologie   (France)

Author keywords

HLA G; Natural killer cells; NF B; Signal transduction

Indexed keywords

HLA G ANTIGEN; HLA G1 ANTIGEN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; INNATE IMMUNITY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 34548354826     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.06.160     Document Type: Article

References (50)

1. Allan D.S.J., Colonna M., Lanier L.L., Churakova T.D., Abrams J.S., Ellis S.A., McMichael A.J., and Braud V.M. Tetrameric complexes of human histocompatibility leukocyte antigen (HLA)-G bind to peripheral blood myelomonocytic cells. J. Exp. Med. 189 (1999) 1149-1156
2. Birbach A., Gold P., Binder B.R., Hofer E., de Martin R., and Schmid J.A. Signaling molecules of the NF-kappa B pathway shuttle constitutively between cytoplasm and nucleus. J. Biol. Chem. 277 (2002) 10842-10851
3. Blery M., Olcese L., and Vivier E. Early signaling via inhibitory and activating NK receptors. Hum. Immunol. 61 (2000) 51-64
4. Bonizzi G., and Karin M. The two NF-[kappa]B activation pathways and their role in innate and adaptive immunity. Trends Immunol. 25 (2004) 280-288
5. Bottero V., Imbert V., Frelin C., Formento J.L., and Peyron J.F. Monitoring NF-kappa B transactivation potential via real-time PCR quantification of I kappa B-alpha gene expression. Mol. Diagn. 7 (2003) 187-194
6. Carosella E.D., Moreau P., Aractingi S., and Rouas-Freiss N. HLA-G: a shield against inflammatory aggression. Trends Immunol. 22 (2001) 553-555
7. Carosella E.D., Moreau P., Le Maoult J., Le Discorde M., Dausset J., and Rouas-Freiss N. HLA-G molecules: from maternal-fetal tolerance to tissue acceptance. Adv. Immunol. 81 (2003) 199-252
8. Caumartin J., Favier B., Daouya M., Guillard C., Moreau P., Carosella E.D., and LeMaoult J. Trogocytosis-based generation of suppressive NK cells. EMBO J. (2007) 1423-1433
9. Chapman T.L., Heikema A.P., and Bjorkman P.J. The inhibitory receptor LIR-1 uses a common binding interaction to recognize class I MHC molecules and the viral homolog UL18. Immunity 11 (1999) 603-613
10. Chen Z.J. Ubiquitin signalling in the NF-kB pathway. Nat. Cell Biol. 7 (2005) 758
11. Chiao P., Miyamoto S., and Verma I. Autoregulation of I{kappa}B{alpha} activity. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 28-32
12. Colonna M., Navarro F., Bellon T., Llano M., Garcia P., Samaridis J., Angman L., Cella M., and Lopez-Botet M. A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186 (1997) 1809-1818
13. Colonna M., Samaridis J., Cella M., Angman L., Allen R., O'Callaghan C.A., Dunbar R.S., Ogg G., Cerundolo V., and Rolink A. Cutting edge: human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J. Immunol. 160 (1998) 3096-3100
14. Cosman D., Fanger N., Borges L., Kubin M., Chin W., Peterson L., and Hsu M.L. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7 (1997) 273-282
15. Creput C., Durrbach A., Menier C., Guettier C., Samuel D., Dausset J., Charpentier B., Carosella E.D., and Rouas-Freiss N. Human leukocyte antigen-G (HLA-G) expression in biliary epithelial cells is associated with allograft acceptance in liver-kidney transplantation. J. Hepatol. 39 (2003) 587-594
16. Faure M., and Long E.O. KIR2DL4 (CD158d), an NK cell-activating receptor with inhibitory potential. J. Immunol. 168 (2002) 6208-6214
17. Guillard C., Chretien S., Pelus A.-S., Porteu F., Muller O., Mayeux P., and Duprez V. Activation of the mitogen-activated protein kinases Erk1/2 by erythropoietin receptor via a Gi protein beta gamma-subunit-initiated pathway. J. Biol. Chem. 278 (2003) 11050-11056
18. Hayden M.S., and Ghosh S. Signaling to NF-{kappa}B. Genes Dev. 18 (2004) 2195-2224
19. Hof P., Pluskey S., Dhe-Paganon S., Eck M.J., and Shoelson S.E. Crystal structure of the tyrosine phosphatase SHP-2. Cell 92 (1998) 441-450
20. Kanai T., Fujii T., Unno N., Yamashita T., Hyodo H., Miki A., Hamai Y., Kozuma S., and 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. 45 (2001) 94-99
21. Kanai T., Fujii T., Kozuma S., Yamashita T., Miki A., Kikuchi A., and Taketani Y. Soluble HLA-G influences the release of cytokines from allogeneic peripheral blood mononuclear cells in culture. Mol. Hum. Reprod. 7 (2001) 195-200
22. Karin M. The beginning of the end: Ikappa B kinase (IKK) and NF-kappa B activation. J. Biol. Chem. 274 (1999) 27339-27342
23. Kelley J., Walter L., and Trowsdale J. Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet. 1 (2005) 129-139
24. Lefebvre S., Berrih-Aknin S., Adrian F., Moreau P., Poea S., Gourand L., Dausset J., Carosella E.D., and Paul P. A specific interferon (IFN)-stimulated response element of the distal HLA-G promoter binds IFN-regulatory factor 1 and mediates enhancement of this nonclassical class I gene by IFN-beta. J. Biol. Chem. 276 (2001) 6133-6139
25. Lila N., Amrein C., Guillemain R., Chevalier P., Latremouille C., Fabiani J.-N., Dausset J., Carosella E.D., and Carpentier A. Human leukocyte antigen-G expression after heart transplantation is associated with a reduced incidence of rejection. Circulation 105 (2002) 1949-1954
26. Lila N., Carpentier A., Amrein C., Khalil-Daher I., Dausset J., and Carosella E.D. Implication of HLA-G molecule in heart-graft acceptance. Lancet 355 (2000) 2138
27. Menier C., Saez B., Horejsi V., Martinozzi S., Krawice-Radanne I., Bruel S., Le Danff C., Reboul M., Hilgert I., and Rabreau M. Characterization of monoclonal antibodies recognizing HLA-G or HLA-E: new tools to analyze the expression of nonclassical HLA class I molecules. Hum. Immunol. 64 (2003) 315-326
28. Moreau P., Adrian-Cabestre F., Menier C., Guiard V., Gourand L., Dausset J., Carosella E.D., and Paul P. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int. Immunol. 11 (1999) 803-811
29. Moretta L., and Moretta A. Killer immunoglobulin-like receptors. Curr. Opin. Immunol. 16 (2004) 626-633
30. Navarro F., Llano M., Bellón T., Colonna M., Geraghty D.E., and López-Botet M. The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur. J. Immunol. 29 (1999) 277-283
31. Neznanov N., Neznanova L., Kondratov R.V., O'Rourke D.M., Ullrich A., and Gudkov A.V. The ability of protein tyrosine phosphatase SHP-1 to suppress NFkappaB can be inhibited by dominant negative mutant of SIRPalpha. DNA Cell. Biol. 23 (2004) 175-182
32. Paul P., Rouas-Freiss N., Khalil-Daher I., Moreau P., Riteau B., Le Gal F.A., Avril M.F., Dausset J., Guillet J.G., and Carosella E.D. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 4510-4515
33. Paul P., Rouas-Freiss N., Moreau P., Cabestre F.A., Menier C., Khalil-Daher I., Pangault C., Onno M., Fauchet R., and Martinez-Laso J. HLA-G, E, -F preworkshop: tools and protocols for analysis of non-classical class I genes transcription and protein expression. Hum. Immunol. 61 (2000) 1177-1195
34. Ponte M., Cantoni C., Biassoni R., Tradori-Cappai A., Bentivoglio G., Vitale C., Bertone S., Moretta A., Moretta L., and Mingari M.C. Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 5674-5679
35. Qu C.-K. Role of the SHP-2 tyrosine phosphatase in cytokine-induced signaling and cellular response. Biochim. Biophys. Acta Mol. Cell. Res. 1592 (2002) 297-301
36. Rajagopalan S., Bryceson Y.T., Kuppusamy S.P., Geraghty D.E., van der Meer A., Joosten I., and Long E.O. Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol. 4 (2006) e9
37. Rajagopalan S., and Long E.O. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J. Exp. Med. 189 (1999) 1093-1100
38. Rieger L., Hofmeister V., Probe C., Dietl J., Weiss E.H., Steck T., and 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. 8 (2002) 255-261
39. Riteau B., Menier C., Khalil-Daher I., Martinozzi S., Pla M., Dausset J., Carosella E.D., and Rouas-Freiss N. HLA-G1 co-expression boosts the HLA class I-mediated NK lysis inhibition. Int. Immunol. 13 (2001) 193-201
40. Robertson M.J., Cochran K.J., Cameron C., Le J.M., Tantravahi R., and Ritz J. Characterization of a cell line, NKL, derived from a aggressive human natural killer cell leukemia. Exp. Hematol. 24 (1996) 406
41. Rouas-Freiss N., Goncalves R.M.-B., Menier C., Dausset J., and Carosella E.D. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 11520-11525
42. Rouas-Freiss N., Marchal R.E., Kirszenbaum M., Dausset J., and Carosella E.D. The alpha 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. U.S.A. 94 (1997) 5249-5254
43. Rouas-Freiss N., Menier M.P., Edgardo C., and Carosella D. HLA-G in cancer: a way to turn off the immune system. Semin. Cancer Biol. 13 (2003) 325-336
44. Tosi M.F. Innate immune responses to infection. J. Allergy Clin. Immunol. 116 (2005) 241-249
45. van der Meer A., Lukassen H.G., van Lierop M.J., Wijnands F., Mosselman S., Braat D.D., and Joosten I. Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells. Mol. Hum. Reprod. 10 (2004) 189-195
46. Yamamoto Y., and Gaynor R.B. I[kappa]B kinases: key regulators of the NF-[kappa]B pathway. Trends Biochem. Sci. 29 (2004) 72-79
47. Yang Y., Chu W., Geraghty D.E., and Hunt J.S. Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J. Immunol. 156 (1996) 4224-4231
48. Yao A.Y., Tang H.Y., Wang Y., Feng M.F., and Zhou R.L. Inhibition of the activating signals in NK92 cells by recombinant GST-sHLA-G1a chain. Cell. Res. 14 (2004) 155-160
49. You M., Flick L.M., Yu D., and Feng G.-S. Modulation of the nuclear factor {kappa}B pathway by Shp-2 tyrosine phosphatase in mediating the induction of interleukin (IL)-6 by IL-1 or tumor necrosis factor. J. Exp. Med. 193 (2001) 101-110
50. Zhou J., Zhang J., Lichtenheld M.G., and Meadows G.G. A role for NF-{kappa}B activation in perforin expression of NK cells upon IL-2 receptor signaling. J. Immunol. 169 (2002) 1319-1325