The indoleamine-2,3-dioxygenase (IDO) inhibitor 1-methyl-d-tryptophan upregulates IDO1 in human cancer cells

PLoS ONE

Volumn 6, Issue 5, 2011, Pages

  Opitz, Christiane A ^a,b   Litzenburger, Ulrike M ^a,b   Opitz, Uta ^c   Sahm, Felix ^a,b   Ochs, Katharina ^a,b   Lutz, Christian ^c   Wick, Wolfgang ^a,b   Platten, Michael ^a,b  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c Wilex Biotechnology GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL DEXTRO TRYPTOPHAN; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; KYNURENINE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; 1 METHYL TRYPTOPHAN; 1-METHYL-TRYPTOPHAN; DRUG DERIVATIVE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; SMALL INTERFERING RNA; TRYPTOPHAN;

ARTICLE; CANCER CELL; CELL CYCLE PROGRESSION; CELL PROLIFERATION; COCULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TUMOR ESCAPE; UPREGULATION; CELL CYCLE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME IMMUNOASSAY; ENZYMOLOGY; FEMALE; GENETICS; METABOLISM; OVARY TUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MAP KINASE KINASE 4; OVARIAN NEOPLASMS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRYPTOPHAN; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 79956302084     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019823     Document Type: Article

References (44)

1. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, et al. (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281: 1191-1193.
2. Opitz CA, Wick W, Steinman L, Platten M, (2007) Tryptophan degradation in autoimmune diseases. Cell Mol Life Sci 64: 2542-2563.
3. Platten M, Ho PP, Youssef S, Fontoura P, Garren H, et al. (2005) Treatment of autoimmune neuroinflammation with a synthetic tryptophan metabolite. Science 310: 850-855.
4. Zelante T, Fallarino F, Bistoni F, Puccetti P, Romani L, (2009) Indoleamine 2,3-dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect 11: 133-141.
5. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC, (2005) Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med 11: 312-319.
6. Munn DH, Mellor AL, (2007) Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J Clin Invest 117: 1147-1154.
7. Uyttenhove C, Pilotte L, Theate I, Stroobant V, Colau D, et al. (2003) Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 9: 1269-1274.
8. Sharma MD, Hou DY, Liu Y, Koni PA, Metz R, et al. (2009) Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes. Blood 113: 6102-6111.
9. Schroecksnadel K, Fiegl M, Prassl K, Winkler C, Denz HA, et al. (2007) Diminished quality of life in patients with cancer correlates with tryptophan degradation. J Cancer Res Clin Oncol 133: 477-485.
10. Okamoto A, Nikaido T, Ochiai K, Takakura S, Saito M, et al. (2005) Indoleamine 2,3-dioxygenase serves as a marker of poor prognosis in gene expression profiles of serous ovarian cancer cells. Clin Cancer Res 11: 6030-6039.
11. Takao M, Okamoto A, Nikaido T, Urashima M, Takakura S, et al. (2007) 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.
12. Ino K, Yamamoto E, Shibata K, Kajiyama H, Yoshida N, et al. (2008) Inverse correlation between tumoral indoleamine 2,3-dioxygenase expression and tumor-infiltrating lymphocytes in endometrial cancer: its association with disease progression and survival. Clin Cancer Res 14: 2310-2317.
13. Ino K, Yoshida N, Kajiyama H, Shibata K, Yamamoto E, et al. (2006) Indoleamine 2,3-dioxygenase is a novel prognostic indicator for endometrial cancer. Br J Cancer 95: 1555-1561.
14. Pan K, Wang H, Chen MS, Zhang HK, Weng DS, et al. (2008) Expression and prognosis role of indoleamine 2,3-dioxygenase in hepatocellular carcinoma. J Cancer Res Clin Oncol 134: 1247-1253.
15. Brandacher G, Perathoner A, Ladurner R, Schneeberger S, Obrist P, et al. (2006) Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells. Clin Cancer Res 12: 1144-1151.
16. Ozaki Y, Edelstein MP, Duch DS, (1988) Induction of indoleamine 2,3-dioxygenase: a mechanism of the antitumor activity of interferon gamma. Proc Natl Acad Sci U S A 85: 1242-1246.
17. Takikawa O, Kuroiwa T, Yamazaki F, Kido R, (1988) 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.
18. Yoshida R, Park SW, Yasui H, Takikawa O, (1988) Tryptophan degradation in transplanted tumor cells undergoing rejection. J Immunol 141: 2819-2823.
19. Yu WG, Yamamoto N, Takenaka H, Mu J, Tai XG, et al. (1996) Molecular mechanisms underlying IFN-gamma-mediated tumor growth inhibition induced during tumor immunotherapy with rIL-12. Int Immunol 8: 855-865.
20. Giannopoulos A, Constantinides C, Fokaeas E, Stravodimos C, Giannopoulou M, et al. (2003) The immunomodulating effect of interferon-gamma intravesical instillations in preventing bladder cancer recurrence. Clin Cancer Res 9: 5550-5558.
21. Marth C, Windbichler GH, Hausmaninger H, Petru E, Estermann K, et al. (2006) Interferon-gamma in combination with carboplatin and paclitaxel as a safe and effective first-line treatment option for advanced ovarian cancer: results of a phase I/II study. Int J Gynecol Cancer 16: 1522-1528.
22. Windbichler GH, Hausmaninger H, Stummvoll W, Graf AH, Kainz C, et al. (2000) Interferon-gamma in the first-line therapy of ovarian cancer: a randomized phase III trial. Br J Cancer 82: 1138-1144.
23. Ishio T, Goto S, Tahara K, Tone S, Kawano K, et al. (2004) Immunoactivative role of indoleamine 2,3-dioxygenase in human hepatocellular carcinoma. J Gastroenterol Hepatol 19: 319-326.
24. Riesenberg R, Weiler C, Spring O, Eder M, Buchner A, et al. (2007) 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.
25. Lob S, Konigsrainer A, Rammensee HG, Opelz G, Terness P, (2009) Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees? Nat Rev Cancer 9: 445-452.
26. Lob S, Konigsrainer A, Zieker D, Brucher BL, Rammensee HG, et al. (2009) IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol Immunother 58: 153-157.
27. Metz R, Duhadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, et al. (2007) 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.
28. Lob S, Konigsrainer A, Schafer R, Rammensee HG, Opelz G, et al. (2008) Levo- but not dextro-1-methyl tryptophan abrogates the IDO activity of human dendritic cells. Blood 111: 2152-2154.
29. Opitz CA, Litzenburger UM, Lutz C, Lanz TV, Tritschler I, et al. (2009) Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells 27: 909-919.
30. Chon SY, Hassanain HH, Gupta SL, (1996) Cooperative role of interferon regulatory factor 1 and p91 (STAT1) response elements in interferon-gamma-inducible expression of human indoleamine 2,3-dioxygenase gene. J Biol Chem 271: 17247-17252.
31. Agaugue S, Perrin-Cocon L, Coutant F, Andre P, Lotteau V, (2006) 1-Methyl-tryptophan can interfere with TLR signaling in dendritic cells independently of IDO activity. J Immunol 177: 2061-2071.
32. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, et al. (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372: 739-746.
33. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST, et al. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 98: 13681-13686.
34. Cady SG, Sono M, (1991) 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.
35. Hou DY, Muller AJ, Sharma MD, DuHadaway J, Banerjee T, et al. (2007) Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res 67: 792-801.
36. Qian F, Villella J, Wallace PK, Mhawech-Fauceglia P, Tario JD Jr, et al. (2009) Efficacy of levo-1-methyl tryptophan and dextro-1-methyl tryptophan in reversing indoleamine-2,3-dioxygenase-mediated arrest of T-cell proliferation in human epithelial ovarian cancer. Cancer Res 69: 5498-5504.
37. Corrigall VM, Vittecoq O, Panayi GS, (2009) Binding immunoglobulin protein-treated peripheral blood monocyte-derived dendritic cells are refractory to maturation and induce regulatory T-cell development. Immunology 128: 218-226.
38. Fujigaki H, Saito K, Fujigaki S, Takemura M, Sudo K, et al. (2006) 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: 655-662.
39. Wang Y, Lawson MA, Dantzer R, Kelley KW, (2009) LPS-induced indoleamine 2,3-dioxygenase is regulated in an interferon-gamma-independent manner by a JNK signaling pathway in primary murine microglia. Brain Behav Immun.
40. Okamoto T, Tone S, Kanouchi H, Miyawaki C, Ono S, et al. (2007) 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. Cytotechnology 54: 107-113.
41. Lanz T, Opitz C, Ho P, Agrawal A, Lutz C, et al. (2009) Mouse mesenchymal stem cells suppress antigen-specific TH-cell immunity independent of indoleamine 2,3-dioxygenase 1 (IDO1). Stem Cells Dev.
42. Boasso A, Vaccari M, Fuchs D, Hardy AW, Tsai WP, et al. (2009) Combined effect of antiretroviral therapy and blockade of IDO in SIV-infected rhesus macaques. J Immunol 182: 4313-4320.
43. Schmitt M, Pawlita M, (2009) High-throughput detection and multiplex identification of cell contaminations. Nucleic Acids Res 37: e119.
44. Herve C, Beyne P, Jamault H, Delacoux E, (1996) Determination of tryptophan and its kynurenine pathway metabolites in human serum by high-performance liquid chromatography with simultaneous ultraviolet and fluorimetric detection. J Chromatogr B Biomed Appl 675: 157-161.