1-Methyl-tryptophan can interfere with TLR signaling in dendritic cells independently of IDO activity

Journal of Immunology

Volumn 177, Issue 4, 2006, Pages 2061-2071

  Agaugué, Sophie ^a   Perrin Cocon, Laure ^a   Coutant, Frédéric ^a   André, Patrice ^a   Lotteau, Vincent ^a,b  

^a UNIVERSITÉ LYON 1   (France)

^b University Lyon i   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLTRYPTOPHAN; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; INTERLEUKIN 13; INTERLEUKIN 5; LIGAND; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN C FOS; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TRANSCRIPTION FACTOR; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CELL MATURATION; CELL POLARITY; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FETUS WASTAGE; GRAFT REJECTION; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; MONOCYTE; NORMAL HUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL; TUMOR REJECTION;

EID: 33746912362     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.4.2061     Document Type: Article

References (58)

1. Shimizu, T., S. Nomiyama, F. Hirata, and O. Hayaishi. 1978. Indoleamine 2,3-dioxygenase: purification and some properties. J. Biol. Chem. 253: 4700-4706.
2. Taylor, M. W., and G. S. Feng. 1991. Relationship between interferon-γ, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5: 2516-2522.
3. Bodaghi, B., O. Goureau, D. Zipeto, L. Laurent, J. L. Virelizier, and S. Michelson. 1999. Role of IFN-γ-induced indoleamine 2,3-dioxygenase and inducible nitric oxide synthase in the replication of human cytomegalovirus in retinal pigment epithelial cells. J. Immunol. 162: 957-964.
4. Byrne, G. I., L. K. Lehmann, and G. J. Landry. 1986. Induction of tryptophan catabolism is the mechanism for γ-interferon-mediated inhibition of intracellular Chlamyidia psittaci replication in T24 cells. Infect. Immun. 53: 347-351.
5. Daubener, W., and C. R. MacKenzie. 1999. IFN-γ activated indoleamine 2,3-dioxygenase activity in human cells is an antiparasitic and an antibacterial effector mechanism. Adv. Exp. Med. Biol. 467: 517-524.
6. Pfefferkorn, E. R., and P. M. Guyre. 1984. Inhibition of growth of Toxoplasma gondii in cultured fibroblasts by human recombinant γ-interferon. Infect. Immun. 44: 211-216.
7. Nagineni, C. N., K. Pardhasaradhi, M. C. Martins, B. Detrick, and J. J. Hooks. 1996. Mechanisms of interferon-induced inhibition of Toxoplasma gondii replication in human retinal pigment epithelial cells. Infect. Immun. 64: 4188-4196.
8. Aune, T. M., and S. L. Pogue. 1989. Inhibition of tumor cell growth by interferon-γ is mediated by two distinct mechanisms dependent upon oxygen tension: induction of tryptophan degradation and depletion of intracellular nicotinamide adenine dinucleolide. J. Clin. Invest. 84: 863-875.
9. Friberg, M., R. Jennings, M. Alsarraj, S. Dessureault, A. Cantor, M. Extermann, A. L. Mellor, D. H. Munn, and S. J. Antonia. 2002. Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. Int. J. Cancer 101: 151-155.
10. Uyttenhove, C., L. Pilotte, I. Theate, V. Stroobant, D. Colau, N. Parmentier, T. Boon, and B. J. Van den Eynde. 2003. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med. 9: 1269-1274.
11. Munn, D. H., M. Zhou, J. T. Altwood, I. Bondarev, S. J. Conway, B. Marshall, C. Brown, and A. L. Mellor. 1998. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 1191-114.
12. Alexander, A. M., M. Crawford, S. Bertera, W. A. Rudert, O. Takikawa, P. D. Robbins, and M. Trucco. 2002. Indoleamine 2,3-dioxygenase expression in transplanted NOD islets prolongs graft survival after adoptive transfer of diabetogenic splenocytes. Diabetes 51: 356-365.
13. + subset. J. Immunol. 165: 1357-1363.
14. + dendritic cells expressing indoleamine 2,3-dioxygenase. J. Immunol. 167: 708-714.
15. Grohmann, U., F. Fallarino, S. Silla, R. Bianchi, M. L. Belladonna, C. Vacca, A. Micheletti, M. C. Fioretti, and P. Puccetti. 2001. CD40 ligation ablates the tolerogenic potential of lymphoid dendritic cells. J. Immunol. 166: 277-283.
16. Sakurai, K., J. P. Zou, J. R. Tschetter, J. M. Ward, and G. M. Shearer. 2002 Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 129: 186-196.
17. Li, Y., E. E. Tredget, and A. Ghahary. 2004. Cell surface expression of MHC class I antigen is suppressed in indoleamine 2,3-dioxygenase genetically modified keratinocytes: implications in allogeneic skin substitute engraftment. Hum. Immunol. 65: 114-123.
18. Frumento, G., R. Rotondo, M. Tonetti, G. Damonte, U. Benatti, and G. B. Ferrara. 2002. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med. 196: 459-468.
19. Hwu, P., M. X. Du, R. Lapointe, M. Do, M. W. Taylor, and H. A. Young. 2000. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol. 164: 3596-3599.
20. Munn, D. H., E. Shafizadeh, J. T. Attwood, I. Bondarev, A. Pashine, and A. L. Mellor. 1999. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med. 189: 1363-1372.
21. Munn, D. H., M. D. Sharma, J. R. Lee, K. G. Jhaver, T. S. Johnson, D. B. Keskin, B. Marshall, P. Chandler, S. J. Antonia, R. Burgess, et al. 2002. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297: 1867-1870.
22. Terness, P., T. M. Bauer, L. Rose, C. Dufter, A. Watzlik, H. Simon, and G. Opelz. 2002. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J. Exp. Med. 196: 447-457.
23. Mellor, A. L., B. Baban, P. Chandler, B. Marshall, K. Jhaver, A. Hansen, P. A. Koni, M. Iwashima, and D. H. Munn. 2003. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J. Immunol. 171: 1652-1655.
24. Mellor, A. L., D. B. Keskin, T. Johnson, P. Chandler, and D. H. Munn. 2002. Cells expressing indoleamine 2,3-dioxygenase inhibit T cell responses. J. Immunol. 168: 3771-3776.
25. Takeda, K., and S. Akira. 2004. TLR signaling pathways. Semin. Immunol. 16: 3-4.
26. Kalinski, P., C. M. Hilkens, E. A. Wierenga, and M. L. Kapsenberg. 1999. T-cell priming by type-1 and lype-2 polarized dendritic cells: the concept of a third signal. Immunol. Today 20: 561-567.
27. Lanzavecchia, A., and F. Sallusto. 2001. The instructive role of dendritic cells on T cell responses: lineages, plasticity and kinetics. Curr. Opin. Immunol. 13: 291-298.
28. Langenkamp, A., M. Messi, A. Lanzavecchia, and F. Sallusto. 2000. Kinetics of dendritic cell activation: impact on priming of TH1: TH2 and nonpolarized T cells. Nat. Immunol. 1: 311-316.
29. Moser, M., and K. M. Murphy. 2000. Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 1: 199-194.
30. Vieira, P. L., E. C. de Jong, E. A. Wierenga, M. L. Kapsenberg, and P. Kalinski. 2000. Development of Th1-inducing capacity in myeloid dendritic cells requires environmental instruction. J. Immunol. 164: 4507-4512.
31. Lutz, M. B., and G. Schuler. 2002. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 23: 445-449.
32. Fujigaki, S., K. Saito, K. Sekikawa, S. Tone, O. Takikawa, H. Fujii, H. Wada, A. Noma, and M. Seishima. 2001. Lipopolysaccharide induction of indoleamine 2,3-dioxygenase is mediated dominantly by an IFN-γ-independent mechanism. Eur. J. Immunol. 31: 2313-2318.
33. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falorni, P. Candeloro, M. L. Belladonna, R. Bianchi, M. C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3: 1097-1104.
34. Yoshida. R., J. Imanishi, T. Oku, T. Kishida, and O. Hayaishi. 1981. Induction of pulmonary indoleamine 2,3-dioxygenase by interferon. Proc. Natl. Acad. Sci. USA 78: 129-132.
35. Yoshida, R., Y. Urade, M. Tokuda, and O. Hayaishi. 1979. Induction of indoleamine 2,3-dioxygenase in mouse lung during virus infection. Proc. Natl. Acad. Sci. USA 76: 4084-4086.
36. Yoshida, R., and O. Hayaishi. 1978. Induction of pulmonary indoleamine 2,3-dioxygenase by intraperitoneal injection of bacterial lipopolysaccharide. Proc. Natl. Acad. Sci. USA 75: 3998-4000.
37. Braun, D., R. S. Longman, and M. L. Albert. 2005. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood 106: 2375-2381.
38. + dendritic cells. Int. Immunol. 14: 65-68.
39. Fallarino, F., C. Asselin-Paturel, C. Vacca, R. Bianchi, S. Gizzi, M. C. Fioretti, G. Trinchieti, U. Grohmann, and P. Puccetti. 2004. Murine plasmacytoid dendritic cells initiate the immunosuppressive pathway of tryptophan catabolism in response to CD200 receptor engagement. J. Immunol. 173: 3748-3754.
40. Munn, D. H., M. D. Sharma, D. Hou, B. Baban, J. R. Lee, S. J. Antonia, J. L. Messina, P. Chandler, P. A. Koni, and A. L. Mellor. 2004. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest. 114: 280-290.
41. Terness, P., J. J. Chuang, T. Bauer, L. Jiga, and G. Opelz. 2005. Regulation of human auto- and alloreactive T cells by indoleamine 2,3-dioxygenase (IDO)-producing dendritic cells: too much ado about IDO? Blood 105: 2480-2486.
42. Terness, P., J. J. Chuang, and G. Opelz. 2006. The immunoregulatory role of IDO-producing human dendritic cells revisited. Trends Immunol. 27: 68-73.
43. Hwang, S. L., N. P. Chung, J. K. Chan, and C. L. Lin. 2005. Indoleamine 2, 3-dioxygenase (IDO) is essential for dendritic cell activation and chemotactic responsiveness to chemokines. Cell Res. 15: 167-175.
44. Takikawa, O., T. Kuroiwa, F. Yamazaki, and R. Kido. 1988. Mechanism of interferon-γ action: characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon-γ and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J. Biol. Chem. 263: 2041-2048.
45. Ardeshna, K. M., A. R. Pizzey, S. Devereux, and A. Khwaja. 2000. The PI3 kinase, p.38 SAP kinase, and NF-κB signal transduction pathways are involved in the survival and maturation of lipopolysaccharide-stimulated human monocyte-derived dendritic cells. Blood 96: 1039-1046.
46. + T cell memory responses. J. Immunol. 172: 6047-6056.
47. Reseigno, M., M. Martino, C. L. Sutherland, M. R. Gold, and P. Ricciardi-Castagnoli. 1998. Dendritic cell survival and maturation are regulated by different signaling pathways. J. Exp. Med. 188: 2175-2180.
48. Puig-Kroger, A., M. Relloso, O. Fernandez-Capetillo, A. Zubiaga, A. Silva, C. Bernabeu, and A. L. Corbi. 2001. Extracellular signal-regulated protein kinase signaling pathway negatively regulates the phenotypic and functional maturation of monocyte-derived human dendritic cells. Blood 98: 2175-2182.
49. Agrawal, S., A. Agrawal, B. Doughty, A. Gerwitz, J. Blenis, T. Van Dyke, and B. Pulendran. 2003. Cutting edge: different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171: 4984-4989.
50. Cady, S. G., and M. Sono. 1991. 1-Methyl-DL-tryptophan, β-(3-benzofuranyl)-DL-alanine (the oxygen analog of tryptophan), and β-[3-benzo(b)thienyl]-DL-alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2,3-dioxygenase. Arch. Biochem. Biophys. 291: 326-333.
51. Hayashi, T., L. Beck, C. Rossetto, X. Gong, O. Takikawa, K. Takabayashi, D. H. Broide, D. A. Carson, and E. Raz. 2004. Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J. Clin. Invest. 114: 270-279.
52. Idzko, M., E. Panther, C. Stratz, T. Muller, H. Bayer, G. Zissel, T. Durk, S. Sorichter, F. Di Virgilio, M. Geissler, et al. 2004. The serotoninergic receptors of human dendritic cells: identification and coupling to cytokine release. J. Immunol. 172: 6011-6019.
53. O'Connell, P. J., X. Wang, M. Leon-Ponte, C. Griffiths, S. C. Pingle, and G. P. Ahern. 2006. A novel form of immune signaling revealed by transmission of the inflammatory mediator serotonin between dendritic cells and T cells. Blood 107: 1010-1017.
54. Rengarajan, J., S. J. Szabo, and L. H. Glimcher. 2000. Transcriptional regulation of Th1/Th2 polarization. Immunol. Today 21: 479-474.
55. Yano, S., P. Ghosh, H. Kusaba, M. Buchholz, and D. L. Longo. 2003. Effect of promoter methylation on the regulation of IFN-γ gene during in vitro differentiation of human peripheral blood T cells into a Th2 population. J. Immunol. 171: 2510-2516.
56. Agarwal, S., and A. Rao. 1998. Modulation of chromatin structure regulates cytokine gene expression during T cell differentiation. Immunity 9: 765-775.
57. Lee, H. J., N. Takemoto, H. Kurata, Y. Kamogawa, S. Miyatake, A. O'Garra. and N. Arai. 2000. GATA-3 induces T helper cell type 2 (Th2) cytokine expression and chromatin remodeling in committed Th1 cells. J. Exp. Med. 192: 105-115.
58. Fields, P. E., S. T. Kim, and R. A. Flavell. 2002. Cutting edge: changes in histone acetylation at the IL-4 and IFN-γ loci accompany Th1/Th2 differentiation. J. Immunol. 169: 647-650.