Nitric oxide produces HLA-G nitration and induces metalloprotease-dependent shedding creating a tolerogenic milieu

Immunology

Volumn 126, Issue 3, 2009, Pages 436-445

  Díaz Lagares, Angel ^a   Alegre, Estibaliz ^a   LeMaoult, Joel ^b   Carosella, Edgardo D ^b   González, Álvaro ^a  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

Human leucocyte antigen G; Immunosuppression; Monocytes; Nitration; Nitric oxide

Indexed keywords

3 NITROTYROSINE; CELL PROTEIN; HLA G ANTIGEN; METALLOPROTEINASE; NITRIC OXIDE; NITRITE; PEROXYNITRITE; TYROSINE;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ARTICLE; BIOLOGICAL ACTIVITY; BIOSYNTHESIS; CELL CULTURE; CELL LINE; CELL SURFACE; CULTURE MEDIUM; CYTOTOXICITY; CYTOTOXICITY TEST; DONOR; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE REPRESSION; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; NATURAL KILLER CELL; NITRATION; NITROGEN AVAILABILITY; NITROGEN UTILIZATION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CYTOTOXICITY, IMMUNOLOGIC; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA ANTIGENS; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; MATRIX METALLOPROTEINASES; MOLSIDOMINE; NITRIC OXIDE; NITRIC OXIDE DONORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA PROCESSING, POST-TRANSCRIPTIONAL; TRIAZENES; TUMOR CELLS, CULTURED;

EID: 59449106816     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2008.02911.x     Document Type: Article

References (48)

1. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007 87 : 315 424.
2. Berchner-Pfannschmidt U, Yamac H, Trinidad B, Fandrey J. Nitric oxide modulates oxygen sensing by hypoxia-inducible factor 1-dependent induction of prolyl hydroxylase 2. J Biol Chem 2007 282 : 1788 96.
3. Connelly L, Palacios-Callender M, Ameixa C, Moncada S, Hobbs AJ. Biphasic regulation of NF-κB activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 2001 166 : 3873 81.
4. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 2003 305 : 776 83.
5. Wei XQ, Charles IG, Smith A et al. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 1995 375 : 408 11.
6. Chang RH, Feng MH, Liu WH, Lai MZ. Nitric oxide increased interleukin-4 expression in T lymphocytes. Immunology 1997 90 : 364 9.
7. Fernandez-Ruiz V, Gonzalez A, Lopez-Moratalla N. Effect of nitric oxide in the differentiation of human monocytes to dendritic cells. Immunol Lett 2004 93 : 87 95.
8. Roozendaal R, Vellenga E, de Jong MA, Traanberg KF, Postma DS, de Monchy JGR, Kauffman HF. Resistance of activated human Th2 cells to NO-induced apoptosis is mediated by γ-glutamyltranspeptidase. Int Immunol 2001 13 : 519 28.
9. Hviid TVF. HLA-G in human reproduction: aspects of genetics, function and pregnancy complications. Hum Reprod Update 2005 12 : 209 32.
10. Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ, DeMars R. A class I antigen, HLA-G, expressed in human trophoblasts. Science 1990 248 : 220 3.
11. Alegre E, Diaz-Lagares A, LeMaoult J, Lopez-Moratalla N, Carosella ED, Gonzalez A. Maternal antigen presenting cells are a source of plasmatic HLA-G during pregnancy: longitudinal study during pregnancy. Hum Immunol 2007 68 : 661 7.
12. Lopez AS, Alegre E, LeMaoult J, Carosella E, Gonzalez A. Regulatory role of tryptophan degradation pathway in HLA-G expression by human monocyte-derived dendritic cells. Mol Immunol 2006 43 : 2151 60.
13. Paul P, Rouas-Freiss N, Khalil-Daher I et al. HLA-G expression in melanoma: a way for tumor cells to escape from immunosurveillance. Proc Natl Acad Sci USA 1998 95 : 4510 5.
14. Kirszenbaum M, Moreau P, Gluckman E, Dausset J, Carosella E. An alternatively spliced form of HLA-G mRNA in human trophoblasts and evidence for the presence of HLA-G transcript in adult lymphocytes. Proc Natl Acad Sci USA 1994 91 : 4209 13.
15. Moreau P, Carosella E, Teyssier M, Prost S, Gluckman E, Dausset J, Kirszenbaum M. Soluble HLA-G molecule an alternatively spliced HLA-G mRNA form candidate to encode it in peripheral blood mononuclear cells and human trophoblasts. Hum Immunol 1995 43 : 231 6.
16. Colonna M, Samaridis J, Cella M et al. Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J Immunol 1998 160 : 3096 100.
17. Riteau B, Rouas-Freiss N, Menier C, Paul P, Dausset J, Carosella ED. HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J Immunol 2001 166 : 5018 26.
18. Riteau B, Menier C, Khalil-Daher I, Sedlik C, Dausset J, Rouas-Freiss N, Carosella ED. HLA-G inhibits the allogeneic proliferative response. J Reprod Immunol 1999 43 : 203 11.
19. 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 61.
20. Park GM, Lee S, Park B, Kim E, Shin J, Cho K, Ahn K. Soluble HLA-G generated by proteolytic shedding inhibits NK-mediated cell lysis. Biochem Biophys Res Commun 2004 313 : 606 11.
21. Zidi I, Guillard C, Marcou C, Krawice-Radanne I, Sangrouber D, Rouas-Freiss N, Carosella ED, Moreau P. Increase in HLA-G1 proteolytic shedding by tumor cells: a regulatory pathway controlled by NF-kappaB inducers. Cell Mol Life Sci 2006 63 : 2669 81.
22. Solier C, Aguerre-Girr M, Lenfant F, Campan A, Berrebi A, Rebmann V, Grosse-Wilde H, Le Bouteiller P. Secretion of pro-apoptotic intron 4-retaining soluble HLA-G1 by human villous trophoblast. Eur J Immunol 2002 32 : 3576 86.
23. Zarlingo TJ, Eis AL, Brockman DE, Kossenjans W, Myatt L. Comparative localization of endothelial and inducible nitric oxide synthase isoforms in haemochorial and epitheliochorial placentae. Placenta 1997 18 : 511 20.
24. Torres MI, Lopez-Casado MA, Luque J, Pena J, Rios A. New advances in coeliac disease: serum and intestinal expression of HLA-G. Int Immunol 2006 28 : 713 8.
25. Wiendl H, Feger U, Schreiner B et al. Expression of the immune-tolerogenic major histocompatibility molecule HLA-G in multiple sclerosis: implications for CNS immunity. Brain 2005 128 : 2689 704.
26. Lozano JM, Gonzalez R, Kindelan JM, Rouas-Freiss N, Caballos R, Dausset J, Carosella ED, Pena J. Monocytes and T lymphocytes in HIV-1-positive patients express HLA-G molecule. Aids 2002 16 : 347 51.
27. Donaghy L, Gros F, Amiot L, Mary C, Maillard A, Guiguen C, Gangneux J-P. Elevated levels of soluble non-classical major histocompatibility class I molecule human leucocyte antigen (HLA)-G in the blood of HIV-infected patients with or without visceral leishmaniasis. Clin Exp Immunol 2007 147 : 236 40.
28. De Stefano D, Maiuri M, Iovine B, Ialenti A, Bevilacqua M, Carnuccio R. The role of NF-κB, IRF-1, and STAT-1α transcription factors in the iNOS gene induction by gliadin and IFN-γ in RAW 264.7 macrophages. J Mol Med 2006 84 : 65 74.
29. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Natl Acad Sci U S A 2005 102 : 9936 41.
30. Weinberg J, Misukonis M, Shami P et al. Human mononuclear phagocyte inducible nitric oxide synthase (iNOS): analysis of iNOS mRNA, iNOS protein, biopterin, and nitric oxide production by blood monocytes and peritoneal macrophages. Blood 1995 86 : 1184 95.
31. Lopez AS, Alegre E, Diaz A, Mugueta C, Gonzalez A. Bimodal effect of nitric oxide in the enzymatic activity of indoleamine 2,3-dioxygenase in human monocytic cells. Immunol Lett 2006 106 : 163 71.
32. Rouas-Freiss N, Marchal RE, Kirszenbaum M, Dausset J, Carosella ED. 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 1997 94 : 5249 54.
33. Le Rond S, Gonzalez A, Gonzalez ASL, Carosella ED, Rouas-Freiss N. Indoleamine 2,3 dioxygenase and human leucocyte antigen-G inhibit the T-cell alloproliferative response through two independent pathways. Immunology 2005 116 : 297 307.
34. Bahri R, Hirsch F, Josse A et al. Soluble HLA-G inhibits cell cycle progression in human alloreactive T lymphocytes. J Immunol 2006 176 : 1331 9.
35. Clements CS, Kjer-Nielsen L, Kostenko L et al. Crystal structure of HLA-G: a nonclassical MHC class I molecule expressed at the fetal-maternal interface. Proc Natl Acad Sci U S A 2005 102 : 3360 5.
36. Rebmann V, LeMaoult J, Rouas-Freiss N, Carosella ED, Grosse-Wilde H. Quantification and identification of soluble HLA-G isoforms. Tissue Antigens 2007 69 : 143 9.
37. Menier C, Riteau B, Carosella ED, Rouas-Freiss N. MICA triggering signal for NK cell tumor lysis is counteracted by HLA-G1-mediated inhibitory signal. Int J Cancer 2002 100 : 63 70.
38. Jung T, Engels M, Klotz L-O, Kroncke K-D, Grune T. Nitrotyrosine and protein carbonyls are equally distributed in HT22 cells after nitrosative stress. Free Radic Biol Med 2007 42 : 773 86.
39. Death AK, Nakhla S, McGrath KCY, Martell S, Yue DK, Jessup W, Celermajer DS. Nitroglycerin upregulates matrix metalloproteinase expression by human macrophages. J Am Coll Cardiol 2002 39 : 1943 50.
40. Novaro V, Colman-Lerner A, Ortega FV et al. Regulation of metalloproteinases by nitric oxide in human trophoblast cells in culture. Reprod Fertil Dev 2001 13 : 411 20.
41. Webster NL, Crowe SM. Matrix metalloproteinases, their production by monocytes and macrophages and their potential role in HIV-related diseases. J Leukoc Biol 2006 80 : 1052 66.
42. Hooper D, Ohnishi S, Kean R, Numagami Y, Dietzschold B, Koprowski H. Local nitric oxide production in viral and autoimmune diseases of the central nervous system. Proc Natl Acad Sci U S A 1995 92 : 5312 6.
43. Rouas-Freiss N, Moreau P, Ferrone S, Carosella ED. HLA-G proteins in cancer: do they provide tumor cells with an escape mechanism? Cancer Res 2005 65 : 10139 44.
44. Myatt L, Rosenfield RB, Eis AL, Brockman DE, Greer I, Lyall F. Nitrotyrosine residues in placenta. Evidence of peroxynitrite formation and action. Hypertension 1996 28 : 488 93.
45. Hara N, Fujii T, Yamashita T, Kozuma S, Okai T, Taketani Y. Altered expression of human leukocyte antigen G (HLA-G) on extravillous trophoblasts in preeclampsia: immunohistological demonstration with anti-HLA-G specific antibody "87G" and anti-cytokeratin antibody "CAM5.2". Am J Reprod Immunol 1996 36 : 349 58.
46. Yie SM, Li LH, Li YM, Librach C. HLA-G protein concentrations in maternal serum and placental tissue are decreased in preeclampsia. Am J Obstet Gynecol 2004 191 : 525 9.
47. Wiendl H, Mitsdoerffer M, Hofmeister V et al. A functional role of HLA-G expression in human gliomas: an alternative strategy of immune escape. J Immunol 2002 168 : 4772 80.
48. LeMaoult J, Caumartin J, Daouya M, Favier B, Le Rond S, Gonzalez A, Carosella ED. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood 2007 109 : 2040 8.