Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees? (original) (raw)
Moffett, J. R. & Namboodiri, M. A. Tryptophan and the immune response. Immunol. Cell Biol.81, 247–265 (2003). CASPubMed Google Scholar
Pfefferkorn, E. R. Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl Acad. Sci. USA81, 908–912 (1984). CASPubMedPubMed Central Google Scholar
Yoshida, R. & Hayaishi, O. Induction of pulmonary indoleamine 2,3-dioxygenase by intraperitoneal injection of bacterial lipopolysaccharide. Proc. Natl Acad. Sci. USA75, 3998–4000 (1978). CASPubMedPubMed Central Google Scholar
Yoshida, R., Urade, Y., Tokuda, M. & Hayaishi, O. Induction of indoleamine 2,3-dioxygenase in mouse lung during virus infection. Proc. Natl Acad. Sci. USA76, 4084–4086 (1979). CASPubMedPubMed Central Google Scholar
Munn, D. H. et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science281, 1191–1193 (1998). CASPubMed Google Scholar
Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nature Rev. Cancer5, 263–274 (2005). CAS Google Scholar
Munn, D. H. et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J. Exp. Med.189, 1363–1372 (1999). CASPubMedPubMed Central Google Scholar
Lee, G. K. et al. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology107, 452–460 (2002). CASPubMedPubMed Central Google Scholar
Munn, D. H. et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity22, 633–642 (2005). CASPubMed Google Scholar
Frumento, G. et al. 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 (2002). CASPubMedPubMed Central Google Scholar
Terness, P. 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.196, 447–457 (2002). CASPubMedPubMed Central Google Scholar
Fallarino, F. et al. T cell apoptosis by kynurenines. Adv. Exp. Med. Biol.527, 183–190 (2003). CASPubMed Google Scholar
Chen, W., Liang, X., Peterson, A. J., Munn, D. H. & Blazar, B. R. The indoleamine 2,3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J. Immunol.181, 5396–5404 (2008). CASPubMed Google Scholar
Hayashi, T. et al. 3-Hydroxyanthranilic acid inhibits PDK1 activation and suppresses experimental asthma by inducing T cell apoptosis. Proc. Natl Acad. Sci. USA104, 18619–18624 (2007). CASPubMedPubMed Central Google Scholar
Uyttenhove, C. et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nature Med.9, 1269–1274 (2003). CASPubMed Google Scholar
Muller, A. J., DuHadaway, J. B., Donover, P. S., Sutanto-Ward, E. & Prendergast, G. C. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nature Med.11, 312–319 (2005). CASPubMed Google Scholar
Prendergast, G. C. Immune escape as a fundamental trait of cancer: focus on IDO. Oncogene27, 3889–3900 (2008). CASPubMed Google Scholar
Chang, M. Y. et al. Bin1 ablation in mammary gland delays tissue remodeling and drives cancer progression. Cancer Res.67, 100–107 (2007). CASPubMed Google Scholar
Ge, K. et al. Losses of the tumor suppressor BIN1 in breast carcinoma are frequent and reflect deficits in programmed cell death capacity. Int. J. Cancer85, 376–383 (2000). CASPubMed Google Scholar
Ge, K. et al. Loss of heterozygosity and tumor suppressor activity of Bin1 in prostate carcinoma. Int. J. Cancer86, 155–161 (2000). CASPubMed Google Scholar
Chang, M. Y. et al. Bin1 ablation increases susceptibility to cancer during aging, particularly lung cancer. Cancer Res.67, 7605–7612 (2007). CASPubMed Google Scholar
Tajiri, T. et al. Expression of a MYCN-interacting isoform of the tumor suppressor BIN1 is reduced in neuroblastomas with unfavorable biological features. Clin. Cancer Res.9, 3345–3355 (2003). CASPubMed Google Scholar
Ge, K. et al. Mechanism for elimination of a tumor suppressor: aberrant splicing of a brain-specific exon causes loss of function of Bin1 in melanoma. Proc. Natl Acad. Sci. USA96, 9689–9694 (1999). CASPubMedPubMed Central Google Scholar
Baban, B. et al. A minor population of splenic dendritic cells expressing CD19 mediates IDO-dependent T cell suppression via type I IFN signaling following B7 ligation. Int. Immunol.17, 909–919 (2005). CASPubMed Google Scholar
Fallarino, F. et al. Ligand and cytokine dependence of the immunosuppressive pathway of tryptophan catabolism in plasmacytoid dendritic cells. Int. Immunol.17, 1429–1438 (2005). CASPubMed Google Scholar
Mellor, A. L. et al. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J. Immunol.171, 1652–1655 (2003). CASPubMed Google Scholar
Munn, D. H. et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science297, 1867–1870 (2002). CASPubMed Google Scholar
Terness, P., Chuang, J. J., Bauer, T., Jiga, L. & Opelz, G. Regulation of human auto- and alloreactive T cells by indoleamine 2,3-dioxygenase (IDO)-producing dendritic cells: too much ado about IDO? Blood105, 2480–2486 (2005). CASPubMed Google Scholar
Terness, P., Chuang, J. J. & Opelz, G. The immunoregulatory role of IDO-producing human dendritic cells revisited. Trends Immunol.27, 68–73 (2006). CASPubMed Google Scholar
Löb, S. et al. Are indoleamine-2,3-dioxygenase producing human dendritic cells a tool for suppression of allogeneic T-cell responses? Transplantation83, 468–473 (2007). PubMed Google Scholar
Lee, J. R. et al. Pattern of recruitment of immunoregulatory antigen-presenting cells in malignant melanoma. Lab. Invest.83, 1457–1466 (2003). CASPubMed Google Scholar
Munn, D. H. et al. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest.114, 280–290 (2004). CASPubMedPubMed Central Google Scholar
Löb, S. et al. IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol. Immunother.58, 153–157 (2009). PubMed Google Scholar
Brandacher, G. et al. Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells. Clin. Cancer Res.12, 1144–1151 (2006). CASPubMed Google Scholar
Pan, K. et al. Expression and prognosis role of indoleamine 2,3-dioxygenase in hepatocellular carcinoma. J. Cancer Res. Clin. Oncol.134, 1247–1253 (2008). CASPubMed Google Scholar
Ishio, T. et al. Immunoactivative role of indoleamine 2,3-dioxygenase in human hepatocellular carcinoma. J. Gastroenterol. Hepatol.19, 319–326 (2004). CASPubMed Google Scholar
Riesenberg, R. et al. Expression of indoleamine 2,3-dioxygenase in tumor endothelial cells correlates with long-term survival of patients with renal cell carcinoma. Clin. Cancer Res.13, 6993–7002 (2007). CASPubMed Google Scholar
Brandacher, G., Winkler, C., Schroecksnadel, K., Margreiter, R. & Fuchs, D. Antitumoral activity of interferon-γ involved in impaired immune function in cancer patients. Curr. Drug Metab.7, 599–612 (2006). CASPubMed Google Scholar
Melichar, B., Solichova, D. & Freedman, R. S. Neopterin as an indicator of immune activation and prognosis in patients with gynecological malignancies. Int. J. Gynecol. Cancer16, 240–252 (2006). CASPubMed Google Scholar
Murr, C. et al. Neopterin as a prognostic parameter in patients with squamous-cell carcinomas of the oral cavity. Int. J. Cancer79, 476–480 (1998). CASPubMed Google Scholar
Murr, C. et al. Neopterin is an independent prognostic variable in females with breast cancer. Clin. Chem.45, 1998–2004 (1999). CASPubMed Google Scholar
Murr, C. et al. Increased neopterin concentrations in patients with cancer: indicator of oxidative stress? Anticancer Res.19, 1721–1728 (1999). CASPubMed Google Scholar
Prommegger, R. et al. Neopterin: a prognostic variable in operations for lung cancer. Ann. Thorac Surg.70, 1861–1864 (2000). CASPubMed Google Scholar
Weinlich, G., Murr, C., Richardsen, L., Winkler, C. & Fuchs, D. Decreased serum tryptophan concentration predicts poor prognosis in malignant melanoma patients. Dermatology214, 8–14 (2007). PubMed Google Scholar
Farrar, M. A. & Schreiber, R. D. The molecular cell biology of interferon-γ and its receptor. Annu. Rev. Immunol.11, 571–611 (1993). CASPubMed Google Scholar
Ozaki, Y., Edelstein, M. P. & Duch, D. S. Induction of indoleamine 2,3-dioxygenase: a mechanism of the antitumor activity of interferon gamma. Proc. Natl Acad. Sci. USA85, 1242–1246 (1988). CASPubMedPubMed Central Google Scholar
Takikawa, O., Kuroiwa, T., Yamazaki, F. & Kido, R. Mechanism of interferon-gamma action. Characterization of indoleamine 2,3-dioxygenase in cultured human cells induced by interferon-gamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J. Biol. Chem.263, 2041–2048 (1988). CASPubMed Google Scholar
Yoshida, R., Park, S. W., Yasui, H. & Takikawa, O. Tryptophan degradation in transplanted tumor cells undergoing rejection. J. Immunol.141, 2819–2823 (1988). CASPubMed Google Scholar
Yu, W. G. et al. Molecular mechanisms underlying IFN-γ-mediated tumor growth inhibition induced during tumor immunotherapy with rIL-12. Int. Immunol.8, 855–865 (1996). CASPubMed Google Scholar
Brunda, M. J. et al. Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J. Exp. Med.178, 1223–1230 (1993). CASPubMed Google Scholar
Nastala, C. L. et al. Recombinant IL-12 administration induces tumor regression in association with IFN-γ production. J. Immunol.153, 1697–1706 (1994). CASPubMed Google Scholar
Zou, J. P. et al. Systemic administration of rIL-12 induces complete tumor regression and protective immunity: response is correlated with a striking reversal of suppressed IFN-γ production by anti-tumor T cells. Int. Immunol.7, 1135–1145 (1995). CASPubMed Google Scholar
Friberg, M. et al. Indoleamine 2,3-dioxygenase contributes to tumor cell evasion of T cell-mediated rejection. Int. J. Cancer101, 151–155 (2002). CASPubMed Google Scholar
Hou, D. Y. et al. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res.67, 792–801 (2007). CASPubMed Google Scholar
Windbichler, G. H. et al. Interferon-gamma in the first-line therapy of ovarian cancer: a randomized phase III trial. Br. J. Cancer82, 1138–1144 (2000). CASPubMedPubMed Central Google Scholar
Giannopoulos, A. et al. The immunomodulating effect of interferon-γ intravesical instillations in preventing bladder cancer recurrence. Clin. Cancer Res.9, 5550–5558 (2003). CASPubMed Google Scholar
Hemmi, H. et al. A Toll-like receptor recognizes bacterial DNA. Nature408, 740–745 (2000). CASPubMed Google Scholar
Takeshita, F. et al. Cutting edge: Role of Toll-like receptor 9 in CpG DNA-induced activation of human cells. J. Immunol.167, 3555–3558 (2001). CASPubMed Google Scholar
Speiser, D. E. et al. Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J. Clin. Invest.115, 739–746 (2005). CASPubMedPubMed Central Google Scholar
Mellor, A. L. et al. Cutting edge: CpG oligonucleotides induce splenic CD19+ dendritic cells to acquire potent indoleamine 2,3-dioxygenase-dependent T cell regulatory functions via IFN type 1 signaling. J. Immunol.175, 5601–5605 (2005). CASPubMed Google Scholar
Wingender, G. et al. Systemic application of CpG-rich DNA suppresses adaptive T cell immunity via induction of IDO. Eur. J. Immunol.36, 12–20 (2006). CASPubMed Google Scholar
Fallarino, F. & Puccetti, P. Toll-like receptor 9-mediated induction of the immunosuppressive pathway of tryptophan catabolism. Eur. J. Immunol.36, 8–11 (2006). CASPubMed Google Scholar
Choi, B. K., Asai, T., Vinay, D. S., Kim, Y. H. & Kwon, B. S. 4-1BB-mediated amelioration of experimental autoimmune uveoretinitis is caused by indoleamine 2,3-dioxygenase-dependent mechanisms. Cytokine34, 233–242 (2006). CASPubMed Google Scholar
Mittler, R. S. et al. Anti-CD137 antibodies in the treatment of autoimmune disease and cancer. Immunol. Res.29, 197–208 (2004). CASPubMed Google Scholar
Seo, S. K. et al. 4-1BB-mediated immunotherapy of rheumatoid arthritis. Nature Med.10, 1088–1094 (2004). CASPubMed Google Scholar
Kim, J. A. et al. Divergent effects of 4–1BB antibodies on antitumor immunity and on tumor-reactive T-cell generation. Cancer Res.61, 2031–2037 (2001). CASPubMed Google Scholar
May, K. F. Jr., Chen, L., Zheng, P. & Liu, Y. Anti-4-1BB monoclonal antibody enhances rejection of large tumor burden by promoting survival but not clonal expansion of tumor-specific CD8+ T cells. Cancer Res.62, 3459–3465 (2002). CASPubMed Google Scholar
Melero, I., Johnston, J. V., Shufford, W. W., Mittler, R. S. & Chen, L. NK1.1 cells express 4–1BB (CDw137) costimulatory molecule and are required for tumor immunity elicited by anti-4-1BB monoclonal antibodies. Cell. Immunol.190, 167–172 (1998). CASPubMed Google Scholar
Melero, I. et al. Monoclonal antibodies against the 4–1BB T-cell activation molecule eradicate established tumors. Nature Med.3, 682–685 (1997). CASPubMed Google Scholar
Nam, K. O., Kang, W. J., Kwon, B. S., Kim, S. J. & Lee, H. W. The therapeutic potential of 4–1BB (CD137) in cancer. Curr. Cancer Drug Targets5, 357–363 (2005). CASPubMed Google Scholar
Baban, B. et al. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J. Reprod. Immunol.61, 67–77 (2004). CASPubMed Google Scholar
Knox, W. E. & Mehler, A. H. The conversion of tryptophan to kynurenine in liver. I. The coupled tryptophan peroxidase-oxidase system forming formylkynurenine. J. Biol. Chem.187, 419–430 (1950). CASPubMed Google Scholar
Minatogawa, Y., Suzuki, S., Ando, Y., Tone, S. & Takikawa, O. Tryptophan pyrrole ring cleavage enzymes in placenta. Adv. Exp. Med. Biol.527, 425–434 (2003). CASPubMed Google Scholar
Tatsumi, K. et al. Induction of tryptophan 2,3-dioxygenase in the mouse endometrium during implantation. Biochem. Biophys. Res. Commun.274, 166–170 (2000). CASPubMed Google Scholar
Suzuki, S. et al. Expression of indoleamine 2,3-dioxygenase and tryptophan 2,3-dioxygenase in early concepti. Biochem. J.355, 425–429 (2001). CASPubMedPubMed Central Google Scholar
Britan, A., Maffre, V., Tone, S. & Drevet, J. R. Quantitative and spatial differences in the expression of tryptophan-metabolizing enzymes in mouse epididymis. Cell Tissue Res.324, 301–310 (2006). CASPubMed Google Scholar
Haber, R., Bessette, D., Hulihan-Giblin, B., Durcan, M. J. & Goldman, D. Identification of tryptophan 2,3-dioxygenase RNA in rodent brain. J. Neurochem.60, 1159–1162 (1993). CASPubMed Google Scholar
Yamamoto, S. & Hayaishi, O. Tryptophan pyrrolase of rabbit intestine. D- and L-tryptophan-cleaving enzyme or enzymes. J. Biol. Chem.242, 5260–5266 (1967). CASPubMed Google Scholar
Yoshida, R. et al. Regulation of indoleamine 2,3-dioxygenase activity in the small intestine and the epididymis of mice. Arch. Biochem. Biophys.203, 343–351 (1980). CASPubMed Google Scholar
Yuasa, H. J. et al. Evolution of vertebrate indoleamine 2,3-dioxygenases. J. Mol. Evol.65, 705–714 (2007). CASPubMed Google Scholar
Yamane, T., Miller, D. L. & Hopfield, J. J. Discrimination between D- and L-tyrosyl transfer ribonucleic acids in peptide chain elongation. Biochemistry20, 7059–7064 (1981). CASPubMed Google Scholar
Cady, S. G. & Sono, M. 1-Methyl-DL-tryptophan, beta-(3-benzofuranyl)-DL-alanine (the oxygen analog of tryptophan), and beta-[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 (1991). CASPubMed Google Scholar
Peterson, A. C. et al. Evaluation of functionalized tryptophan derivates and related compounds as competitive inhibitors of indoleamine 2,3-dioxygenase. Med. Chem. Res.3, 531–544 (1994). CAS Google Scholar
Metz, R. et al. Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2,3-dioxygenase inhibitory compound D-1-methyl-tryptophan. Cancer Res.67, 7082–7087 (2007). CASPubMed Google Scholar
Ball, H. J. et al. Characterization of an indoleamine 2,3-dioxygenase-like protein found in humans and mice. Gene396, 203–213 (2007). CASPubMed Google Scholar
Lob, S. et al. Levo- but not dextro-1-methyl tryptophan abrogates the IDO activity of human dendritic cells. Blood111, 2152–2154 (2008). CASPubMed Google Scholar
Katz, J. B., Muller, A. J. & Prendergast, G. C. Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol. Rev.222, 206–221 (2008). CASPubMed Google Scholar
Agaugue, S., Perrin-Cocon, L., Coutant, F., Andre, P. & Lotteau, V. 1-Methyl-tryptophan can interfere with TLR signaling in dendritic cells independently of IDO activity. J. Immunol.177, 2061–2071 (2006). CASPubMed Google Scholar
Steinman, R. M. & Banchereau, J. Taking dendritic cells into medicine. Nature449, 419–426 (2007). CASPubMed Google Scholar
Kudo, Y. & Boyd, C. A. Characterisation of L-tryptophan transporters in human placenta: a comparison of brush border and basal membrane vesicles. J. Physiol.531, 405–416 (2001). CASPubMedPubMed Central Google Scholar
Curti, A. et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25− into CD25+ T regulatory cells. Blood109, 2871–2877 (2007). CASPubMed Google Scholar
Okamoto, T. et al. Transcriptional regulation of indoleamine 2,3-dioxygenase (IDO) by tryptophan and its analogue: Down-regulation of the indoleamine 2,3-dioxygenase (IDO) transcription by tryptophan and its analogue. Cytotechnology54, 107–113 (2007). CASPubMedPubMed Central Google Scholar
Alvarez-Salas, L. M. Nucleic acids as therapeutic agents. Curr. Top. Med. Chem.8, 1379–1404 (2008). CASPubMed Google Scholar
Huang, C., Li, M., Chen, C. & Yao, Q. Small interfering RNA therapy in cancer: mechanism, potential targets, and clinical applications. Expert Opin. Ther. Targets.12, 637–645 (2008). CASPubMed Google Scholar
Mocellin, S., Costa, R. & Nitti, D. RNA interference: ready to silence cancer? J. Mol. Med.84, 4–15 (2006). CASPubMed Google Scholar
Moreira, J. N., Santos, A. & Simoes, S. Bcl-2-targeted antisense therapy (Oblimersen sodium): towards clinical reality. Rev. Recent Clin. Trials1, 217–235 (2006). CASPubMed Google Scholar
Zheng, X. et al. Reinstalling antitumor immunity by inhibiting tumor-derived immunosuppressive molecule IDO through RNA interference. J. Immunol.177, 5639–5646 (2006). CASPubMed Google Scholar
Jeong, Y. I. et al. (–)-Epigallocatechin gallate suppresses indoleamine 2,3-dioxygenase expression in murine dendritic cells: evidences for the COX-2 and STAT1 as potential targets. Biochem. Biophys. Res. Commun.354, 1004–1009 (2007). CASPubMed Google Scholar
Lee, H. J. et al. Rosmarinic acid inhibits indoleamine 2,3-dioxygenase expression in murine dendritic cells. Biochem. Pharmacol.73, 1412–1421 (2007). PubMed Google Scholar
Kim, S. I. et al. _p_-Coumaric acid inhibits indoleamine 2,3-dioxygenase expression in murine dendritic cells. Int. Immunopharmacol7, 805–815 (2007). CASPubMed Google Scholar
Mehta, R. G. et al. Cancer chemopreventive activity of brassinin, a phytoalexin from cabbage. Carcinogenesis16, 399–404 (1995). CASPubMed Google Scholar
Park, E. J. & Pezzuto, J. M. Botanicals in cancer chemoprevention. Cancer Metastasis Rev.21, 231–255 (2002). CASPubMed Google Scholar
Banerjee, T. et al. A key in vivo antitumor mechanism of action of natural product-based brassinins is inhibition of indoleamine 2,3-dioxygenase. Oncogene27, 2851–2857 (2008). CASPubMed Google Scholar
Gaspari, P. et al. Structure-activity study of brassinin derivatives as indoleamine 2,3-dioxygenase inhibitors. J. Med. Chem.49, 684–692 (2006). CASPubMedPubMed Central Google Scholar
Brastianos, H. C. et al. Exiguamine A, an indoleamine-2,3-dioxygenase (IDO) inhibitor isolated from the marine sponge Neopetrosia exigua. J. Am. Chem. Soc.128, 16046–16047 (2006). CASPubMed Google Scholar
Carr, G., Chung, M. K., Mauk, A. G. & Andersen, R. J. Synthesis of indoleamine 2,3-dioxygenase inhibitory analogues of the sponge alkaloid exiguamine A. J. Med. Chem.51, 2634–2637 (2008). CASPubMed Google Scholar
Kumar, S. et al. Structure based development of phenylimidazole-derived inhibitors of indoleamine 2,3-dioxygenase. J. Med. Chem.51, 4968–4977 (2008). CASPubMedPubMed Central Google Scholar
Pereira, A., Vottero, E., Roberge, M., Mauk, A. G. & Andersen, R. J. Indoleamine 2,3-dioxygenase inhibitors from the Northeastern Pacific marine hydroid Garveia annulata. J. Nat. Prod.69, 1496–1499 (2006). CASPubMed Google Scholar
Sugimoto, H. et al. Crystal structure of human indoleamine 2,3-dioxygenase: catalytic mechanism of O2 incorporation by a heme-containing dioxygenase. Proc. Natl Acad. Sci. USA103, 2611–2616 (2006). CASPubMedPubMed Central Google Scholar
Boasso, A. et al. Combined effect of antiretroviral therapy and blockade of IDO in SIV-infected rhesus macaques. J. Immunol.182, 4313–4320 (2009). CASPubMed Google Scholar
Ogata, S. et al. Apoptosis induced by nicotinamide-related compounds and quinolinic acid in HL-60 cells. Biosci. Biotechnol. Biochem.64, 327–332 (2000). CASPubMed Google Scholar
Braun, D., Longman, R. S. & Albert, M. L. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood106, 2375–2381 (2005). CASPubMedPubMed Central Google Scholar
Lopez, A. S., 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.106, 163–171 (2006). CASPubMed Google Scholar
Belladonna, M. L. et al. Cutting edge: Autocrine TGF-β sustains default tolerogenesis by IDO-competent dendritic cells. J. Immunol.181, 5194–5198 (2008). CASPubMed Google Scholar
Gura, T. How embryos may avoid immune attack. Science281, 1122–1124 (1998). CASPubMed Google Scholar
Kotake, Y. & Masayama, I. The intermediary metabolism of tryptophan XVIII. The mechanism of formation of kynurenine from tryptophan Z. Physiol. Chem.243, 237–244 (1936). CAS Google Scholar
Thackray, S. J., Mowat, C. G. & Chapman, S. K. Exploring the mechanism of tryptophan 2,3-dioxygenase. Biochem. Soc. Trans.36, 1120–1123 (2008). CASPubMedPubMed Central Google Scholar
Zhang, Y. et al. Crystal structure and mechanism of tryptophan 2,3-dioxygenase, a heme enzyme involved in tryptophan catabolism and in quinolinate biosynthesis. Biochemistry46, 145–155 (2007). CASPubMed Google Scholar
Beutelspacher, S. C. et al. Expression of indoleamine 2,3-dioxygenase (IDO) by endothelial cells: implications for the control of alloresponses. Am. J. Transplant6, 1320–1330 (2006). CASPubMed Google Scholar
Pantoja, L. G., Miller, R. D., Ramirez, J. A., Molestina, R. E. & Summersgill, J. T. Inhibition of Chlamydia pneumoniae replication in human aortic smooth muscle cells by gamma interferon-induced indoleamine 2,3-dioxygenase activity. Infect. Immun.68, 6478–6481 (2000). CASPubMedPubMed Central Google Scholar
Oberdorfer, C., Adams, O., MacKenzie, C. R., De Groot, C. J. & Daubener, W. Role of IDO activation in anti-microbial defense in human native astrocytes. Adv. Exp. Med. Biol.527, 15–26 (2003). PubMed Google Scholar
Della Chiesa, M. et al. The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function. Blood108, 4118–4125 (2006). CASPubMed Google Scholar
Hwu, P. et al. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol.164, 3596–3599 (2000). CASPubMed Google Scholar
Fallarino, F. et al. Modulation of tryptophan catabolism by regulatory T cells. Nature Immunol.4, 1206–1212 (2003). CAS Google Scholar
Grohmann, U. et al. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nature Immunol.3, 1097–1101 (2002). CAS Google Scholar
Grohmann, U. et al. Reverse signaling through GITR ligand enables dexamethasone to activate IDO in allergy. Nature Med.13, 579–586 (2007). CASPubMed Google Scholar
Orabona, C. et al. CD28 induces immunostimulatory signals in dendritic cells via CD80 and CD86. Nature Immunol.5, 1134–1142 (2004). CAS Google Scholar
Fallarino, F. et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J. Immunol.176, 6752–6761 (2006). CASPubMed Google Scholar
Molano, A., Illarionov, P. A., Besra, G. S., Putterman, C. & Porcelli, S. A. Modulation of invariant natural killer T cell cytokine responses by indoleamine 2,3-dioxygenase. Immunol. Lett.117, 81–90 (2008). CASPubMedPubMed Central Google Scholar
Adikari, S. B., Lian, H., Link, H., Huang, Y. M. & Xiao, B. G. Interferon-γ-modified dendritic cells suppress B cell function and ameliorate the development of experimental autoimmune myasthenia gravis. Clin. Exp. Immunol.138, 230–236 (2004). CASPubMedPubMed Central Google Scholar
Ino, K. et al. Indoleamine 2,3-dioxygenase is a novel prognostic indicator for endometrial cancer. Br. J. Cancer95, 1555–1561 (2006). CASPubMedPubMed Central Google Scholar
Takao, M. et al. Increased synthesis of indoleamine-2,3-dioxygenase protein is positively associated with impaired survival in patients with serous-type, but not with other types of, ovarian cancer. Oncol. Rep.17, 1333–1339 (2007). CASPubMed Google Scholar