Effects of various phytochemicals on indoleamine 2,3-dioxygenase 1 activity: Galanal is a novel, competitive inhibitor of the enzyme

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Yamamoto, Rie ^a   Yamamoto, Yasuko ^a   Imai, Shinjiro ^b   Fukutomi, Ryuta ^c   Ozawa, Yoshio ^d   Abe, Masako ^d   Matuo, Yushi ^a   Saito, Kuniaki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF SHIZUOKA   (Japan)

^c NISSHIN SEIFUN GROUP INC   (Japan)

^d TAKASAKI UNIVERSITY OF HEALTH AND WELFARE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYL TRYPTOPHAN; ANDROGRAPHOLIDE; AVENA SATIVA EXTRACT; CURCUMIN; DOCOSAHEXAENOIC ACID; EPIGALLOCATECHIN GALLATE; GALANAL; GAMMA INTERFERON; GLABRIDIN; I KAPPA B ALPHA; I KAPPA B KINASE ALPHA; ICOSAPENTAENOIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; ISOORIENTIN; LUTEOLIN; MESSENGER RNA; METHANOL; MULBERRY EXTRACT; MYRICETIN; OLIVETOL; PLANT EXTRACT; PLANT MEDICINAL PRODUCT; QUERCETIN; SOUR ORANGE EXTRACT; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG; DITERPENE; ENZYME INHIBITOR;

ANIMAL CELL; ARTICLE; COMPETITIVE INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME INHIBITOR INTERACTION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IC 50; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION; ZINGIBER MIOGA; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; ENZYME INDUCTION; HEK293 CELL LINE; KINETICS; METABOLISM; SIGNAL TRANSDUCTION;

DITERPENES; ENZYME INDUCTION; ENZYME INHIBITORS; HEK293 CELLS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; KINETICS; NF-KAPPA B; PHYTOCHEMICALS; PLANT EXTRACTS; SIGNAL TRANSDUCTION;

EID: 84895769830     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088789     Document Type: Article

References (46)

1. Hassanain HH, Chon SY, Gupta SL (1993) Differential regulation of human indoleamine 2,3-dioxygenase gene-expression by interferon-gamma and interferon-alpha-analysis of the regulatory region of the gene and identification of an interferon-gamma-inducible DNA-binding factor. Journal of Biological Chemistry 268: 5077-5084. (Pubitemid 23081633)
2. Fujigaki H, Saito K, Fujigaki S, Takemura M, Sudo K, et al. (2006) The signal transducer and activator of transcription 1 alpha 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-kappa B pathways, and synergistic effect of several proinflammatory cytokines. Journal of Biochemistry 139: 655-662. (Pubitemid 43973911)
3. Fujigaki S, Saito K, Sekikawa K, Tone S, Takikawa O, et al. (2001) Lipopolysaccharide induction of indoleamine 2,3-dioxygenase is mediated dominantly by an IFN-gamma-independent mechanism. European Journal of Immunology 31: 2313-2318. (Pubitemid 32785349)
4. Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, et al. (2002) Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. Journal of Experimental Medicine 196: 459-468.
5. Sharma MD, Hou D-Y, 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.
6. Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, et al. (2002) CTLA-4-Ig regulates tryptophan catabolism in vivo. Nature Immunology 3: 1097-1101. (Pubitemid 35363664)
7. 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. (Pubitemid 28406294)
8. Palafox D, Llorente L, Alberu J, Torres-Machorro A, Camorlinga N, et al. (2010) The role of indoleamine 2,3 dioxygenase in the induction of immune tolerance in organ transplantation. Transplantation Reviews 24: 160-165.
9. Boasso A, Vaccari M, Fuchs D, Hardy AW, Tsai W-P, et al. (2009) HIV-induced tryptophan catabolism: pathogenic mechanism and target for immunotherapy. Amino Acids 37: 89-89.
10. Romani L, Fallarino F, De Luca A, Montagnoli C, D'Angelo C, et al. (2008) Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451: 211-U212.
11. 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. (Pubitemid 41567343)
12. Myint AM, Schwarz MJ, Muller N (2012) The role of the kynurenine metabolism in major depression. Journal of Neural Transmission 119: 245-251.
13. Muller AJ, Scherle PA (2006) Targeting the mechanisms of tumoral immune tolerance with small-molecule inhibitors. Nature Reviews Cancer 6: 613-625. (Pubitemid 44140859)
14. Bridewell DJA, Sperry J, Smith JR, Kosim-Satyaputra P, Ching L-M, et al. (2013) Natural Product-Inspired Pyranonaphthoquinone Inhibitors of Indoleamine 2,3-Dioxygenase-1 (IDO-1). Australian Journal of Chemistry 66: 40-49.
15. Jeong Y-I, Jung ID, Lee JS, Lee C-M, Lee J-D, et al. (2007) (-)-Epigallocatechin gallate suppresses indoleamine 2,3-dioxygenase expression in murine dendritic cells: Evidences for the COX-2 and STAT1 as potential targets. Biochemical and Biophysical Research Communications 354.
16. Jeong Y-I, Kim SW, Jung ID, Lee JS, Chang JH, et al. (2009) Curcumin Suppresses the Induction of Indoleamine 2,3-Dioxygenase by Blocking the Janus-activated Kinase-Protein Kinase C delta-STAT1 Signaling Pathway in Interferon-gamma-stimulated Murine Dendritic Cells. Journal of Biological Chemistry 284.
17. Abe M, Ozawa Y, Uda Y, Yamada Y, Morimitsu Y, et al. (2002) Labdane-type diterpene dialdehyde, pungent principle of myoga, Zingiber mioga Roscoe. Bioscience Biotechnology and Biochemistry 66: 2698-2700. (Pubitemid 39251147)
18. Hoshi M, Ito H, Fujigaki H, Takemura M, Takahashi T, et al. (2009) Indoleamine 2,3-dioxygenase is highly expressed in human adult T-cell leukemia/lymphoma and chemotherapy changes tryptophan catabolism in serum and reduced activity. Leuk Res 33: 39-45.
19. Fujigaki S, Saito K, Takemura M, Fujii H, Wada H, et al. (1998) Species differences in L-tryptophan-kynurenine pathway metabolism: quantification of anthranilic acid and its related enzymes. Arch Biochem Biophys 358: 329-335. (Pubitemid 28480952)
20. Fujigaki H, Saito K, Lin F, Fujigaki S, Takahashi K, et al. (2006) Nitration and inactivation of IDO by peroxynitrite. Journal of Immunology 176: 372-379. (Pubitemid 43023283)
21. Prendergast GC, Metz R Novel isolated indoleamine 2,3-dioxygenase-2 protein, useful for treating melanoma, hepatitis C viral infection, prion disease, metabolic disorders, cardiovascular disease, age related disorders and neurological disorders. Lankenau Inst Medical Res; Prendergast G C; Metz R.
22. 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. Nature Medicine 9: 1269-1274. (Pubitemid 37279849)
23. Liu X, Newton RC, Friedman SM, Scherle PA (2009) Indoleamine 2,3-Dioxygenase, an Emerging Target for Anti-Cancer Therapy. Current Cancer Drug Targets 9: 938-952.
24. Soliman H, Mediavilla-Varela M, Antonia S (2010) Indoleamine 2,3-Dioxygenase Is It an Immune Suppressor? Cancer Journal 16: 354-359.
25. Munn DH, Sharma MD, Hou D, Baban B, Lee JR, et al. (2004) Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. Journal of Clinical Investigation 114: 280-290. (Pubitemid 39071633)
26. Wang D, Saga Y, Mizukami H, Sato N, Nonaka H, et al. (2012) Indoleamine-2,3-dioxygenase, an immunosuppressive enzyme that inhibits natural killer cell function, as a useful target for ovarian cancer therapy. International Journal of Oncology 40: 929-934.
27. Loeb S, Koenigsrainer A, Zieker D, Bruecher BLDM, Rammensee H-G, et al. (2009) IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunology Immunotherapy 58: 153-157.
28. Meininger D, Zalameda L, Liu Y, Stepan LP, Borges L, et al. (2011) Purification and kinetic characterization of human indoleamine 2,3-dioxygenases 1 and 2 (IDO1 and IDO2) and discovery of selective IDO1 inhibitors. Biochimica Et Biophysica Acta-Proteins and Proteomics 1814: 1947-1954.
29. Hou D-Y, 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 Research 67: 792-801. (Pubitemid 46192220)
30. Cerejo M, Andrade G, Roca C, Sousa J, Rodrigues C, et al. (2012) A Powerful Yeast-Based Screening Assay for the Identification of Inhibitors of Indoleamine 2,3-Dioxygenase. Journal of Biomolecular Screening 17: 1362-1371.
31. Lancellotti S, Novarese L, De Cristofaro R (2011) Biochemical Properties of Indoleamine 2,3-dioxygenase: From Structure to Optimized Design of Inhibitors. Current Medicinal Chemistry 18: 2205-2214.
32. Smith JR, Evans KJ, Wright A, Willows RD, Jamie JF, et al. (2012) Novel indoleamine 2,3-dioxygenase-1 inhibitors from a multistep in silico screen. Bioorganic & Medicinal Chemistry 20: 1354-1363.
33. Abe M, Ozawa Y, Morimitsu Y, Kubota K (2008) Mioganal, a Novel Pungent Principle in Myoga (Zingiber mioga Roscoe) and a Quantitative Evaluation of Its Pungency. Bioscience Biotechnology and Biochemistry 72: 2681-2686.
34. Sun T, Chen X-H, Tang Z-D, Cai J, Wang X-Y, et al. (2010) Novel 1-alkyl-tryptophan derivatives downregulate IDO1 and IDO2 mRNA expression induced by interferon-gamma in dendritic cells. Molecular and Cellular Biochemistry 342: 29-34.
35. Saito K, Chen CY, Masana M, Crowley JS, Markey SP, et al. (1993) 4-Chloro-3-hydroxyanthranilate, 6-chlorotryptophan and norharmane attenuate quinolinic acid formation by interferon-gamma-stimulated monocytes (THP-1 Cells). Biochemical Journal 291: 11-14. (Pubitemid 23107741)
36. Liu X, Shin N, Koblish HK, Yang G, Wang Q, et al. (2010) Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity. Blood 115: 3520-3530.
37. Kumar S, Malachowski WP, DuHadaway JB, LaLonde JM, Carroll PJ, et al. (2008) Indoleamine 2,3-dioxygenase is the anticancer target for a novel series of potent naphthoquinone-based inhibitors (vol 51, pg 1712, 2008). Journal of Medicinal Chemistry 51: 7325-7325.
38. Banerjee T, DuHadaway JB, Gaspari P, Sutanto-Ward E, Munn DH, et al. (2008) A key in vivo antitumor mechanism of action of natural product-based brassinins is inhibition of indoleamine 2,3-dioxygenase. Oncogene 27: 2851-2857. (Pubitemid 351620442)
39. Matsuno K, Takai K, Isaka Y, Unno Y, Sato M, et al. (2010) S-Benzylisothiourea derivatives as small-molecule inhibitors of indoleamine-2,3-dioxygenase. Bioorganic & Medicinal Chemistry Letters 20: 5126-5129.
40. Yue EW, Douty B, Wayland B, Bower M, Liu X, et al. (2009) Discovery of Potent Competitive Inhibitors of Indoleamine 2,3-Dioxygenase with in Vivo Pharmacodynamic Activity and Efficacy in a Mouse Melanoma Model. Journal of Medicinal Chemistry 52: 7364-7367.
41. Huang Q, Zheng M, Yang S, Kuang C, Yu C, et al. (2011) Structure-activity relationship and enzyme kinetic studies on 4-aryl-1H-1,2, 3-triazoles as indoleamine 2,3-dioxygenase (IDO) inhibitors. European Journal of Medicinal Chemistry 46: 5680-5687.
42. 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. Archives of Biochemistry and Biophysics 291: 326-333.
43. Banerjee T, DuHadaway JB, Gaspari P, Sutanto-Ward E, Munn DH, et al. (2013) A key in vivo antitumor mechanism of action of natural product-based brassinins is inhibition of indoleamine 2,3-dioxygenase. Oncogene 27(20):2851-7. (Pubitemid 351620442)
44. Kumar A, Takada Y, Boriek AM, Aggarwal BB (2004) Nuclear factor-kappa B: its role in health and disease. Journal of Molecular Medicine-Jmm 82: 434-448. (Pubitemid 39044283)
45. Nakanishi C, Toi M (2005) Nuclear factor-kappa B inhibitors as sensitizers to anticancer drugs. Nature Reviews Cancer 5: 297-309. (Pubitemid 40488635)
46. Pahl HL (1999) Activators and target genes of Rel/NF-kappa B transcription factors. Oncogene 18: 6853-6866.