α-Galactosylceramide modulates the induction of indoleamine 2,3-dioxygenase in antigen presenting cells

Biochemical Pharmacology

Volumn 76, Issue 6, 2008, Pages 738-750

  Fallarini, Silvia ^a   Paoletti, Tiziana ^a   Panza, Luigi ^a   Lombardi, Grazia ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Glycolipid; IFN ; iNKT cells; l Kynurenines; Monocytes

Indexed keywords

1 O (ALPHA GALACTOPYRANOSYL) 2 HEXACOSANOYLAMINO 1,3,4 OCTADECANETRIOL; ALPHA GALACTOSYLCERAMIDE; CD1D ANTIGEN; GAMMA INTERFERON; GLYCOLIPID; IMMUNOMODULATING AGENT; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 2; KYNURENINE; TRYPTOPHAN;

ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CELL FUNCTION; CELL LINE; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE RELEASE; DRUG POTENCY; DRUG STRUCTURE; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MONOCYTE; MONONUCLEAR CELL; MOUSE; NATURAL KILLER T CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGEN-PRESENTING CELLS; CELL LINE, TUMOR; CELLS, CULTURED; ENZYME INDUCTION; GALACTOSYLCERAMIDES; HL-60 CELLS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON TYPE II; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL; MONOCYTES; T-LYMPHOCYTE SUBSETS;

EID: 50549099054     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2008.07.001     Document Type: Article

References (60)

1. Beckman E.M., Porcelli S.A., Morita C.T., Behar S.M., Furlong S.T., and Brenner M.B. Recognition of a lipid antigen by CD1-restricted alpha beta+ T cells. Nature 372 (1994) 691-694
2. Kawano T., Cui J., Koezuka Y., Toura I., Kaneko Y., Motoki K., et al. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 278 (1997) 1626-1629
3. Burdin N., Brossay L., Koezuka Y., Smiley S.T., Grusby M.J., Gui M., et al. Selective ability of mouse CD1 to present glycolipids: alpha-galactosylceramide specifically stimulates V alpha 14+ NK T lymphocytes. J Immunol 161 (1998) 3271-3281
4. De Libero G., and Mori L. Recognition of lipid antigens by T cells. Nat Rev Immunol 5 (2005) 485-496
5. Bricard G., and Porcelli S.A. Antigen presentation by CD1 molecules and the generation of lipid-specific T cell immunity. Cell Mol Life Sci 64 (2007) 1824-1840
6. Zajonc D.M., and Kronenberg M. CD1 mediated T cell recognition of glycolipids. Curr Opin Struct Biol 17 (2007) 521-529
7. Barral D.C., and Brenner M.B. CD1 antigen presentation: how it works. Nat Rev Immunol 7 (2007) 929-941
8. Angénieux C., Fraisier V., Maître B., Racine V., Van der Wel N., Fricker D., et al. The cellular pathway of CD1e in immature and maturing dendritic cells. Traffic 6 (2005) 286-302
9. Kronenberg M. Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 23 (2005) 877-900
10. Parekh V.V., Lalani S., and Van Kaer L. The in vivo response of invariant natural killer T cells to glycolipid antigens. Int Rev Immunol 26 (2007) 31-48
11. Fujii S., Shimizu K., Hemmi H., Fukui M., Bonito A.J., Chen G., et al. Glycolipid alpha-C-galactosylceramide is a distinct inducer of dendritic cell function during innate and adaptive immune responses of mice. Proc Natl Acad Sci USA 103 (2006) 11252-11257
12. Galli G., Pittoni P., Tonti E., Malzone C., Uematsu Y., Tortoli M., et al. Invariant NKT cells sustain specific B cell responses and memory. Proc Natl Acad Sci USA 104 (2007) 3984-3989
13. Bendelac A., Savage P.B., and Teyton L. The biology of NKT cells. Annu Rev Immunol 25 (2007) 297-336
14. Tupin E., Kinjo Y., and Kronenberg M. The unique role of natural killer T cells in the response to microorganisms. Nat Rev Microbiol 5 (2007) 405-417
15. Yang Y., Ueno A., Bao M., Wang Z., Im J.S., Porcelli S., et al. Control of NKT cell differentiation by tissue-specific microenvironments. J Immunol 171 (2003) 5913-5920
16. Molano A., Illarionov P.A., Besra G.S., Putterman C., and Porcelli S.A. Modulation of invariant natural killer T cell cytokine responses by indoleamine 2,3-dioxygenase. Immunol Lett 117 (2008) 81-90
17. Natori T., Akimoto K., Motoki K., Koezuka Y., and Higa T. Development of KRN7000, derived from agelasphin produced by Okinawan sponge. Nippon Yakurigaku Zasshi 110 (1997) 63P-68P
18. Kobayashi E., Motoki K., Uchida T., Fukushima H., and Koezuka Y. KRN7000, a novel immunomodulator, and its antitumor activities. Oncol Res 7 (1995) 529-534
19. Hong S., Scherer D.C., Singh N., Mendiratta S.K., Serizawa I., Koezuka Y., et al. Lipid antigen presentation in the immune system: lessons learned from CD1d knockout mice. Immunol Rev 169 (1999) 31-44
20. Koch M., Stronge V.S., Shepherd D., Gadola S.D., Mathew B., Ritter G., et al. The crystal structure of human CD1d with and without alpha-galactosylceramide. Nat Immunol 6 (2005) 819-826
21. Hung L.C., Lin C.C., Hung S.K., Wu B.C., Jan M.D., Liou S.H., et al. A synthetic analog of alpha-galactosylceramide induces macrophage activation via the TLR4-signaling pathways. Biochem Pharmacol 73 (2007) 1957-1970
22. King N.J., and Thomas S.R. Molecules in focus: indoleamine 2,3-dioxygenase. Int J Biochem Cell Biol 39 (2007) 2167-2172
23. Mac Kenzie C.R., Heseler K., Müller A., and Däubener W. Role of indoleamine 2,3-dioxygenase in antimicrobial defence and immuno-regulation: tryptophan depletion versus production of toxic kynurenines. Curr Drug Metab 8 (2007) 237-244
24. Munn D.H., Zhou M., Attwood J.T., Bondarev I., Conway S.J., Marshall B., et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281 (1998) 1191-1193
25. Beutelspacher S.C., Pillai R., Watson M.P., Tan P.H., Tsang J., McClure M.O., et al. Function of indoleamine 2,3-dioxygenase in corneal allograft rejection and prolongation of allograft survival by over-expression. Eur J Immunol 36 (2006) 690-700
26. Munn D.H., and Mellor A.L. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 117 (2007) 1147-1154
27. Ryan J.M., Barry F., Murphy J.M., and Mahon B.P. Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 149 (2007) 353-363
28. Ueno A., Cho S., Cheng L., Wang J., Hou S., Nakano H., et al. Transient upregulation of indoleamine 2,3-dioxygenase in dendritic cells by human chorionic gonadotropin downregulates autoimmune diabetes. Diabetes 56 (2007) 1686-1693
29. Sakurai K., Zou J.P., Tschetter J.R., Ward J.M., and Shearer G.M. Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J Neuroimmunol 129 (2002) 186-196
30. Gurtner G.J., Newberry R.D., Schloemann S.R., McDonald K.G., and Stenson W.F. Inhibition of indoleamine 2,3-dioxygenase augments trinitrobenzene sulfonic acid colitis in mice. Gastroenterology 125 (2003) 1762-1773
31. Hayashi T., Beck L., Rossetto C., Gong X., Takikawa O., Takabayashi K., et al. Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J Clin Invest 114 (2004) 270-279
32. Grohmann U., Fallarino F., Bianchi R., Orabona C., Vacca C., Fioretti M.C., et al. A defect in tryptophan catabolism impairs tolerance in nonobese diabetic mice. J Exp Med 198 (2003) 153-160
33. Mellor A.L., Baban B., Chandler P., Marshall B., Jhaver K., Hansen A., et al. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol 171 (2003) 1652-1655
34. Du M.X., Sotero-Esteva W.D., and Taylor M.W. Analysis of transcription factors regulating induction of indoleamine 2,3-dioxygenase by IFN-gamma. J Interferon Cytokine Res 20 (2000) 133-142
35. Dai W., and Gupta S.L. Regulation of indoleamine 2,3-dioxygenase gene expression in human fibroblasts by interferon-gamma. Upstream control region discriminates between interferon-gamma and interferon-alpha. J Biol Chem 265 (1990) 19871-19877
36. Fujigaki H., Saito K., Fujigaki S., Takemura M., Sudo K., Ishiguro H., et al. The signal transducer and activator of transcription 1alpha and interferon regulatory factor 1 are not essential for the induction of indoleamine 2,3-dioxygenase by lipopolysaccharide: involvement of p38 mitogen-activated protein kinase and nuclear factor-kappaB pathways, and synergistic effect of several proinflammatory cytokines. J Biochem 139 (2006) 655-662
37. Jung I.D., Lee C.M., Jeong Y.I., Lee J.S., Park W.S., Han J., et al. Differential regulation of indoleamine 2,3-dioxygenase by lipopolysaccharide and interferon gamma in murine bone marrow derived dendritic cells. FEBS Lett 581 (2007) 1449-1456
38. Puccetti P., and Grohmann U. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 7 (2007) 817-823
39. Munn D.H., Sharma M.D., Baban B., Harding H.P., Zhang Y., Ron D., et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22 (2005) 633-642
40. Frumento G., Rotondo R., Tonetti M., Damonte G., Benatti U., and Ferrara G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 196 (2002) 459-468
41. Fallarino F., Grohmann U., Vacca C., Bianchi R., Orabona C., Spreca A., et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ 9 (2002) 1069-1077
42. Della Chiesa M., Carlomagno S., Frumento G., Balsamo M., Cantoni C., Conte R., et al. The tryptophan catabolite l-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function. Blood 108 (2006) 4118-4125
43. Platten M., Ho P.P., Youssef S., Fontoura P., Garren H., Hur E.M., et al. Treatment of autoimmune neuroinflammation with a synthetic tryptophan metabolite. Science 310 (2005) 850-855
44. Böyum A. Separation of leukocytes from blood and bone marrow. Introduction. Scand J Clin Lab Invest 21 (1968) 77-89
45. Brunelleschi S., Penengo L., Lavagno L., Santoro C., Colangelo D., Viano I., et al. Macrophage stimulating protein (MSP) evokes superoxide anion production by human macrophages of different origin. Br J Pharmacol 134 (2001) 1285-1295
46. Sköld M., and Behar S.M. Role of CD1d-restricted NKT cells in microbial immunity. Infect Immun 71 (2003) 5447-5455
47. Chen Q., and Ross A.C. Retinoic acid regulates CD1d gene expression at the transcriptional level in human and rodent monocytic cells. Exp Biol Med 232 (2007) 488-494
48. Janda J. Spectral changes of a cationic dye after interaction with endotoxins. Biochem J 124 (1971) 73P-74P
49. Braun D., Longman R.S., and Albert M.L. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 106 (2005) 2375-2381
50. Lee H.J., Jeong Y.I., Lee T.H., Jung I.D., Lee J.S., Lee C.M., et al. Rosmarinic acid inhibits indoleamine 2,3-dioxygenase expression in murine dendritic cells. Biochem Pharmacol 73 (2007) 1412-1421
51. Yu K.O., Im J.S., Molano A., Dutronc Y., Illarionov P.A., Forestier C., et al. Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of alpha-galactosylceramides. Proc Natl Acad Sci USA 102 (2005) 3383-3388
52. Wu D., Xing G.W., Poles M.A., Horowitz A., Kinjo Y., Sullivan B., et al. Bacterial glycolipids and analogs as antigens for CD1d-restricted NKT cells. Proc Natl Acad Sci USA 102 (2005) 1351-1356
53. Liu Y., Goff R.D., Zhou D., Mattner J., Sullivan B.A., Khurana A., et al. A modified alpha-galactosyl ceramide for staining and stimulating natural killer T cells. J Immunol Methods 312 (2006) 34-39
54. Matto P., Modica E., Franchini L., Facciotti F., Mori L., De Libero G., et al. A general and stereoselective route to alpha- or beta-galactosphingolipids via a common four-carbon building block. J Org Chem 72 (2007) 7757-7760
55. Berkers C.R., and Ovaa H. Immunotherapeutic potential for ceramide-based activators of iNKT cells. Trends Pharmacol Sci 26 (2005) 252-257
56. Miyake S., and Yamamura T. Therapeutic potential of CD1d-restricted invariant natural killer T cell-based treatment for autoimmune diseases. Int Rev Immunol 26 (2007) 73-94
57. Munn D.H., Sharma M.D., Lee J.R., Jhaver K.G., Johnson T.S., Keskin D.B., et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297 (2002) 1867-1870
58. Yue S.C., Shaulov A., Wang R., Balk S.P., and Exley M.A. CD1d ligation on human monocytes directly signals rapid NF-kappaB activation and production of bioactive IL-12. Proc Natl Acad Sci USA 102 (2005) 11811-11816
59. Luo S.Y., Kulkarni S.S., Chou C.H., Liao W.M., and Hung S.C. A concise synthesis of tetrahydroxy-LCB, alpha-galactosyl ceramide, and 1,4-dideoxy-1,4-imino-l-ribitol via d-allosamines as key building blocks. J Org Chem 71 (2006) 1226-1229
60. Wang J., Simonavicius N., Wu X., Swaminath G., Reagan J., Tian H., et al. Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. J Biol Chem 281 (2006) 22021-22028