IDO metabolite produced by EBV-transformed B cells inhibits surface expression of NKG2D in NK cells via the c-Jun N-terminal kinase (JNK) pathway

Immunology Letters

Volumn 136, Issue 2, 2011, Pages 187-193

  Song, Hyunkeun ^a   Park, Hyunjin ^a   Kim, Jiyoung ^a   Park, Gabin ^a   Kim, Yeong Seok ^a   Kim, Sung Mok ^a   Kim, Daejin ^b   Seo, Su Kil ^a   Lee, Hyun Kyung ^c   Cho, DaeHo ^d   Hur, Daeyoung ^a  

^a Inje University College of Medicine   (South Korea)

^b Chung Ang University College of Medicine   (South Korea)

^c Inje University College of Medicine   (South Korea)

^d Sookmyung Women's University   (South Korea)

Author keywords

IDO; L kynurenine; Natural killer cells; NKG2D; Tumor immunity

Indexed keywords

ANISOMYCIN; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 18; KYNURENINE; NATURAL KILLER CELL RECEPTOR NKG2D;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL SURFACE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; EPSTEIN BARR VIRUS INFECTION; HUMAN; HUMAN CELL; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CELL LINE, TUMOR; CULTURE MEDIA, CONDITIONED; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; K562 CELLS; KILLER CELLS, NATURAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; SIGNAL TRANSDUCTION;

EID: 79953027646     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2011.01.009     Document Type: Article

References (50)

1. Young L.S., Rickinson A.B. Epstein-Barr virus: 40 years on. Nat Rev Cancer 2004, 4:757-768.
2. Munz C., Moormann A. Immune escape by Epstein-Barr virus associated malignancies. Semin Cancer Biol 2008, 18:381-387.
3. Nanbo A., Inoue K., Adachi-Takasawa K., Takada K. Epstein-Barr virus RNA confers resistance to interferon-alpha-induced apoptosis in Burkitt's lymphoma. EMBO J 2002, 21:954-965.
4. Thorley-Lawson D.A., Gross A. Persistence of the Epstein-Barr virus and the origins of associated lymphomas. N Engl J Med 2004, 350:1328-1337.
5. Muller A., Schmitt L., Raftery M., Schonrich G. Paralysis of B7 co-stimulation through the effect of viral IL-10 on T cells as a mechanism of local tolerance induction. Eur J Immunol 1998, 28:3488-3498.
6. Sengupta S., den Boon J.A., Chen I.H., Newton M.A., Dahl D.B., Chen M., et al. Genome-wide expression profiling reveals EBV-associated inhibition of MHC Class I expression in nasopharyngeal carcinoma. Cancer Res 2006, 66:7999-8006.
7. Raulet D.H. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 2004, 5:996-1002.
8. Trinchieri G. Biology of natural killer cells. Adv Immunol 1989, 47:187-376.
9. Diepstra A., Poppema S., Boot M., Visser L., Nolte I.M., Niens M., et al. HLA-G protein expression as a potential immune escape mechanism in classical Hodgkin's lymphoma. Tissue Antigens 2008, 71:219-226.
10. Lodoen M.B., Lanier L.L. Viral modulation of NK cell immunity. Nat Rev Microbiol 2005, 3:59-69.
11. Orange J.S., Fassett M.S., Koopman L.A., Boyson J.E., Strominger J.L. Viral evasion of natural killer cells. Nat Immunol 2002, 3:1006-1012.
12. Cerwenka A., Lanier L.L. NKG2D ligands: unconventional MHC class I-like molecules exploited by viruses and cancer. Tissue Antigens 2003, 61:335-343.
13. Wen C., He X., Ma H., Hou N., Wei C., Song T., et al. Hepatitis C virus infection downregulates the ligands of the activating receptor NKG2D. Cell Mol Immunol 2008, 5:475-478.
14. Cosman D., Mullberg J., Sutherland C.L., Chin W., Armitage R., Fanslow W., et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001, 14:123-133.
15. Pende D., Cantoni C., Rivera P., Vitale M., Castriconi R., Marcenaro S., et al. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of nonepithelial origin. Eur J Immunol 2001, 31:1076-1086.
16. Gasser S., Orsulic S., Brown E.J., Raulet D.H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005, 436:1186-1190.
17. Groh V., Rhinehart R., Randolph-Habecker J., Topp M.S., Riddell S.R., Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2001, 2:255-260.
18. Raulet D.H. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003, 3:781-790.
19. Welte S.A., Sinzger C., Lutz S.Z., Singh-Jasuja H., Sampaio K.L., Eknigk U., et al. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur J Immunol 2003, 33:194-203.
20. Groh V., Wu J., Yee C., Spies T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002, 419:734-738.
21. Pende D., Rivera P., Marcenaro S., Chang C.C., Biassoni R., Conte R., et al. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res 2002, 62:6178-6186.
22. Salih H.R., Antropius H., Gieseke F., Lutz S.Z., Kanz L., Rammensee H.G., et al. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 2003, 102:1389-1396.
23. Lee J.C., Lee K.M., Kim D.W., Heo D.S. Elevated TGF-beta1 secretion and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol 2004, 172:7335-7340.
24. Song H., Hur D.Y., Kim K.E., Park H., Kim T., Kim C.W., et al. IL-2/IL-18 prevent the down-modulation of NKG2D by TGF-beta in NK cells via the c-Jun N-terminal kinase (JNK) pathway. Cell Immunol 2006, 242:39-45.
25. 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 2006, 108:4118-4125.
26. Mellor A.L., Munn D.H. Tryptophan catabolism and T-cell tolerance: immunosuppression by starvation?. Immunol Today 1999, 20:469-473.
27. Munn D.H., Shafizadeh E., Attwood J.T., Bondarev I., Pashine A., Mellor A.L. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med 1999, 189:1363-1372.
28. Taylor M.W., Feng G.S. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J 1991, 5:2516-2522.
29. Fallarino F., Grohmann U., Vacca C., Bianchi R., Orabona C., Spreca A., et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ 2002, 9:1069-1077.
30. Frumento G., Rotondo R., Tonetti M., Damonte G., Benatti U., 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 2002, 196:459-468.
31. Lee G.K., Park H.J., Macleod M., Chandler P., Munn D.H., Mellor A.L. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology 2002, 107:452-460.
32. Terness P., Bauer T.M., Rose L., Dufter C., Watzlik A., Simon H., et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med 2002, 196:447-457.
33. Katz J.B., Muller A.J., Prendergast G.C. Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol Rev 2008, 222:206-221.
34. Prendergast G.C. Immune escape as a fundamental trait of cancer: focus on IDO. Oncogene 2008, 27:3889-3900.
35. Zamanakou M., Germenis A.E., Karanikas V. Tumor immune escape mediated by indoleamine 2,3-dioxygenase. Immunol Lett 2007, 111:69-75.
36. Lichtenfels R., Biddison W.E., Schulz H., Vogt A.B., Martin R. CARE-LASS (calcein-release-assay), an improved fluorescence-based test system to measure cytotoxic T lymphocyte activity. J Immunol Methods 1994, 172:227-239.
37. Jonjic S., Babic M., Polic B., Krmpotic A. Immune evasion of natural killer cells by viruses. Curr Opin Immunol 2008, 20:30-38.
38. Powers C., DeFilippis V., Malouli D., Fruh K. Cytomegalovirus immune evasion. Curr Top Microbiol Immunol 2008, 325:333-359.
39. Sun J.C., Lanier L.L. The natural selection of herpesviruses and virus-specific NK Cell receptors. Viruses 2009, 1:362.
40. McSharry B.P., Burgert H.G., Owen D.P., Stanton R.J., Prod'homme V., Sester M., et al. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol 2008, 82:4585-4594.
41. Nattermann J., Nischalke H.D., Hofmeister V., Kupfer B., Ahlenstiel G., Feldmann G., et al. HIV-1 infection leads to increased HLA-E expression resulting in impaired function of natural killer cells. Antivir Ther 2005, 10:95-107.
42. Fallarino F., Vacca C., Orabona C., Belladonna M.L., Bianchi R., Marshall B., et al. Functional expression of indoleamine 2,3-dioxygenase by murine CD8 alpha(+) dendritic cells. Int Immunol 2002, 14:65-68.
43. 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 2002, 297:1867-1870.
44. Bellmann-Weiler R., Schroecksnadel K., Holzer C., Larcher C., Fuchs D., Weiss G. IFN-gamma mediated pathways in patients with fatigue and chronic active Epstein Barr virus-infection. J Affect Disord 2008, 108:171-176.
45. Ohga S., Nomura A., Takada H., Hara T. Immunological aspects of Epstein-Barr virus infection. Crit Rev Oncol Hematol 2002, 44:203-215.
46. Okamoto T., Tone S., Kanouchi H., Miyawaki C., Ono S., Minatogawa Y. Transcriptional regulation of indoleamine 2,3-dioxygenase (IDO) by tryptophan and its analogue: downregulation of the indoleamine 2,3-dioxygenase (IDO) transcription by tryptophan and its analogue. Cytotechnology 2007, 54:107-113.
47. Sun T., Chen X.H., Tang Z.D., Cai J., Wang X.Y., Wang S.C., et al. Novel 1-alkyl-tryptophan derivatives downregulate IDO1 and IDO2 mRNA expression induced by interferon-gamma in dendritic cells. Mol Cell Biochem 2010, 342:29-34.
48. Zwirner N.W., Fuertes M.B., Girart M.V., Domaica C.I., Rossi L.E. Cytokine-driven regulation of NK cell functions in tumor immunity: role of the MICA-NKG2D system. Cytokine Growth Factor Rev 2007, 18:159-170.
49. Peraldi M.N., Berrou J., Dulphy N., Seidowsky A., Haas P., Boissel N., et al. Oxidative stress mediates a reduced expression of the activating receptor NKG2D in NK cells from end-stage renal disease patients. J Immunol 2009, 182:1696-1705.
50. Li W., Yamamoto H., Kubo S., Okamura H. Modulation of innate immunity by IL-18. J Reprod Immunol 2009, 83:101-105.