Establishment of a human indoleamine 2, 3-dioxygenase 2 (hIDO2) bioassay system and discovery of tryptanthrin derivatives as potent hIDO2 inhibitors

European Journal of Medicinal Chemistry

Volumn 123, Issue , 2016, Pages 171-179

  Li, Juanjuan ^a   Li, Yang ^a   Yang, Dan ^a   Hu, Nan ^a   Guo, Zhanling ^a   Kuang, Chunxiang ^b   Yang, Qing ^a,c  

^a FUDAN UNIVERSITY   (China)

^b TONGJI UNIVERSITY   (China)

^c EAST CHINA UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

3 dioxygenase 2; IDO2 bioassay system; IDO2 inhibitor; Indoleamine 2; Tryptanthrin derivatives

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; TRYPTOPHAN DERIVATIVE; ENZYME INHIBITOR; INDOLEAMINE 2,3-DIOXYGENASE 2, HUMAN; QUINAZOLINE DERIVATIVE; RECOMBINANT PROTEIN; TRYPTANTHRINE;

ARTICLE; BIOASSAY; CONTROLLED STUDY; DRUG POTENCY; DRUG SCREENING; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; HUMAN; HUMAN CELL; IC50; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RECOMBINANT PLASMID; STRUCTURE ACTIVITY RELATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ENZYME ASSAY;

CLINICAL ENZYME TESTS; ENZYME INHIBITORS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INHIBITORY CONCENTRATION 50; QUINAZOLINES; RECOMBINANT PROTEINS;

EID: 84979650397     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2016.07.013     Document Type: Article

References (42)

1. [1] Liu, X., Newton, R.C., Friedman, S.M., Scherle, P.A., Indoleamine 2,3-Dioxygenase, an emerging target for Ant-Cancer therapy. Curr. Cancer Drug Tar 9 (2009), 938–952.
2. [2] Kolodziej, L.R., Paleolog, E.M., Williams, R.O., Kynurenine metabolism in health and disease. Amino Acids 41 (2011), 1173–1183.
3. [3] Yamamoto, S., Hayaishi, O., Tryptophan pyrrolase of rabbit intestine. D-and Ltryptophan-cleaving enzyme or enzymes. J. Biol. Chem. 242 (1976), 5260–5266.
4. [4] Takikawa, O., Yoshida, R., Kido, R., Hayaishi, O., Tryptophan degradation in mice initiated by indoleamine 2,3-dioxygenase. J. Biol. Chem. 261 (1986), 3648–3653.
5. [5] Sono, M., Roach, M., Coulter, E., Dawson, J., Heme-containing oxygenases. Chem. Rev. 96 (1996), 2841–2888.
6. [6] Batabyal, D., S.R Yeh, Human tryptophan dioxygenase: a comparison to indoleamine 2, 3-dioxygenase. J. Am. Chem. Soc. 129 (2007), 15690–15701.
7. [7] Hansen, A.M., Driussi, C., Turner, V., Takikawa, O., Hunt, N.H., Tissue distribution of indoleamine 2, 3-dioxygenase in normal and malaria-infected tissue. Redox Rep. 5 (2000), 112–115.
8. [8] Heyes, M.P., Morrison, P.F., Quantification of local de novo synthesis versus blood contributions to quinolinic acid concentrations in brain and systemic tissues. J. Neurochem. 68 (1997), 280–288.
9. [9] Stone, T.W., Mackay, G.M., Forrest, C.M., Clark, C.J., Darlington, L.G., Tryptophan metabolites and brain disorders. Clin. Chem. Lab. Med. 41 (2003), 852–859.
10. [10] Suzuki, S., Tone, S., Takikawa, O., Kubo, T., Kohno, I., Minatogawa, Y., Expression of indoleamine 2,3-dioxygenase and tryptophan 2,3-dioxygenase in early concepti. Biochem. J. 355 (2001), 425–429.
11. [11] Munn, D.H., Zhou, M., Attwood, J.T., Bondarev, I., Conway, S.J., Marshall, B., Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281 (1998), 1191–1193.
12. [12] Honig, A., Rieger, L., Kapp, M., Sutterlin, M., Dietl, J., Kammerer, U., Indoleamine 2,3-dioxygenase (IDO) expression in invasive extravillous trophoblast supports role of the enzyme for materno-fetal tolerance. J. Reprod. Immunol. 61 (2004), 79–86.
13. [13] Frey, A.B., Monu, N., Signaling defects in anti-tumor T cells. Immunol. Rev. 222 (2008), 192–205.
14. [14] Novak, N., Targeting dendritic cells in allergen immunotherapy. Immunol. Allergy Clin. N. Am. 26 (2006), 307–319.
15. [15] Heyes, M.P., Saito, K., Crowley, J.S., Davis, L.E., Demitrack, M.A., Der, M., Dilling, L.A., Elia, J., Kruesi, M.J.P., Lackner, A., Larsen, S.A., Lee, K., Leonard, H.L., Markey, S.P., Martin, A., Milstein, S., Mouradian, M.M.M.R., Pranzatelli, Quearry, B.J., Salazar, A., Smith, M., Strauss, S.E., Sunderland, T., Swedo, S.W., Tourtellotte, W.W., Quinolinic acid and kynurenine pathway metabolism in inflammatory and non-inflammatory neurological disease. Brain 115 (1992), 1249–1273.
16. [16] Metz, R., DuHadaway, J.B., Kamasani, U., Laury-Kleintop, L., Muller, A.J., Prendergast, G.C., Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2, 3-dioxygenase inhibitory compound D-1-methyltryptophan. Cancer Res. 67 (2007), 7082–7087.
17. [17] Ball, H.J., Sanchez-Perez, A., Weiser, S., Austin, C.J.D., Astelbauer, F., Miu, J., McQuillan, J.A., Stocker, R., Jermiin, L.S., Hunt, N.H., Characterization of an indoleamine 2, 3-dioxygenase-like protein found in humans and mice. Gene 396 (2007), 203–213.
18. [18] Yuasa, H.J., Takubo, M., Takahashi, A., Hasegawa, T., Noma, H., Suzuki, T., Evolution of vertebrate indoleamine 2,3-dioxygenases. J. Mol. Evol. 65 (2007), 705–714.
19. [19] Yuasa, H.J., Ball, H.J., Ho, Y.F., Austin, C.J., Whittington, C.M., Belov, K., Maghzal, G.J., Jermiin, L.S., Hunt, N.H., Characterization and evolution of vertebrate indoleamine 2, 3-dioxygenases IDOs from monotremes and marsupials. Comp. Biochem. Physiol. B 153 (2009), 137–144.
20. [20] Yuasa, H.J., Ball, H.J., Austin, C.J.D., Hunt, N.H., 1-L-methyltryptophan is a more effective inhibitor of vertebrate IDO2 enzymes than 1-D-methyltryptophan. Comp. Biochem. Physiol. B 157 (2010), 10–15.
21. [21] Yuasa, H.J., Mizuno, K., Ball, H.J., Low efficiency IDO2 enzymes are conserved in lower vertebrates, whereas higher efficiency IDO1 enzymes are dispensable. FEBS J. 282 (2015), 2735–2745.
22. [22] Opitz, C.A., Litzenburger, U.M., Sahm, F., Ott, M., Tritschler, I., et al. An endogenous tumor-promoting ligand of the human aryl hydrocarbon receptor. Nature 478 (2011), 197–203.
23. [23] Prendergast, G.C., Metz, R., Muller, A.J., Merlo, L.M.F., L.Mandik-Nayak,IDO2 in immunomodulation and autoimmune disease. Front. Immunol., 5, 2014, 585.
24. [24] Kollgaard, T., Klausen, T.W., Idorn, M., Holmgaard, R.B., Straten, P.T., Andersen, M.H., Association of a functional Indoleamine 2,3-dioxygenase 2 genotype with specific immune responses. Oncoimmunology 1 (2012), 441–447.
25. [25] Eldredge, H.B., Denittis, A., Duhadaway, J.B., Chernick, M., Metz, R., Prendergast, G.C., Concurrent whole brain radiotherapy and short-course chloroquine inpatients with brain metastases: a pilot trial. J. Radiat. Oncol., 2, 2013, 3.
26. [26] Metz, R., Smith, C., DuHadaway, J.B., Chandler, P., Baban, B., Merlo, L.M.F., Pigott, E., Keough, M.P., Rust, S., Mellor, A.L., Mandik-Nayak, L., Muller, A.J., Prendergast, G.C., IDO2 is critical for IDO1-mediated T-cell regulation and exerts a non-redundant function in inflammation. Int. Immunol. 26 (2014), 357–367.
27. [27] Qian, F., Liao, J., Villella, J., Edwards, R., Kalinski, P., Lele, S., Effects of 1-methyltryptophan stereoisomers on IDO2 enzyme activity and IDO2-mediated arrest of human T cell proliferation. Cancer Immunol. Immunother. 61 (2012), 2013–2020.
28. [28] Lob, S., Konigsrainer, A., Zieker, D., Brucher, B.L., Rammensee, H.G., Opelz, G., IDO1 and IDO2 are expressed in human tumors: levo- but not dextro-1-methyl tryptophan inhibits tryptophan catabolism. Cancer Immunol. Immunother. 58 (2009), 153–157.
29. [29] Austin, C.J.D., Mailu, B.M., Maghzal, G.J., Sanchez-Perez, A., Rahlfs, S., Zocher, K., Yuasa, H.J., Arthur, J.W., Becker, K., Stocker, R., Hunt, N.H., Ball, H.J., Biochemical characteristics and inhibitor selectivity of mouse indoleamine 2,3-dioxygenase-2. Amino Acids 39 (2010), 565–578.
30. [30] Pantouris, G., Serys, M., Yuasa, H.J., Ball, H.J., Mowat, C.G., Human indoleamine 2, 3-dioxygenase-2 has substrate specificity and inhibition characteristics distinct from those of indoleamine 2, 3-dioxygenase-1. Amino Acids 46 (2014), 2155–2163.
31. [31] Lob, S., Konigsrainer, A., Schafer, R., Rammensee, H.G., Opelz, G., Terness, P., Levo- but not dextro-1-methyl tryptophan abrogates the IDO activity of human dendritic cells. Blood 111 (2008), 2152–2154.
32. [32] Ball, H.J., Yuasa, H.J., Austin, C.J., Weiser, S., Hunt, N.H., Indoleamine 2,3-dioxygenase-2: a new enzyme in the kynurenine pathway. Int. J. Biochem, Cell Biol. 41 (2009), 467–471.
33. [33] Bakmiwewa, S.M., Fatokun, A.A., Tran, A., Payne, R.J., Hunt, N.H., Ball, H.J., Identification of selective inhibitors of indoleamine 2,3-dioxygenase 2. Bioorg Med. Chem. Lett. 22 (2012), 7641–7646.
34. [34] Yu, C.J., Zheng, M.F., Kuang, C.X., Huang, W., Yang, Q., Oren-gedoku-to and its constituents with therapeutic potential in Alzheimer's disease inhibit indoleamine 2, 3-dioxygenase activity in vitro. Alzheimer's Dis. 22 (2010), 257–266.
35. [35] C.X. Kuang, L.L. Kong, Preparation of 5-halo-4-aryl-1H-1,2,3–triazoles, China patent. Appl. No.: 200910054881.
36. [36] Jiang, Y.B., Kuang, C.X., Yang, Q., CuI-catalyzed synthesis of 4-aryl-1H-1,2,3-triazoles from anti-3-aryl-2,3-dibromopropanoic acids and sodium azide. Synthesis 24 (2010), 4256–4260.
37. [37] Huang, Q., Zheng, M.F., Yang, S.S., Yu, C.J., Kuang, C.X., Yang, Q., Structure−activity relationship and enzyme kinetic studies on 4-aryl-1H-1,2,3-triazoles as indoleamine 2,3-dioxygenase (IDO) inhibitors. Eur. J. Med. Chem. 46 (2011), 5680–5687.
38. [38] Yang, S.S., Li, X.S., Hu, F., Li, Y.L., Yang, Y.Y., Yan, J., Kuang, C.X., Yang, Q., Discovery of tryptanthrin derivatives as potent inhibitors of indoleamine 2,3-Dioxygenase with therapeutic activity in lewis lung Cancer (LLC) tumor-bearing mice. J. Med. Chem. 56 (2013), 8321–8331.
39. [39] Meininger, D., Zalameda, L., Liu, Y., Stepan, L.P., Borges, L., McCarter, J.D., Sutherland, C.L., Purification and kinetic characterization of human indoleamine 2,3-dioxygenases 1 and 2 (IDO1 and IDO2) and discovery of selective IDO1 inhibitors. BBA-Proteins Protom 1814 (2011), 1947–1954.
40. [40] Austin, C.J.D., Mizdrak, J., Matin, A., Sirijovski, N., Satyaputra, P.K., Willows, R.D., Roberts, T.H., Truscott, R.J.W., Polekhina, G., Parker, M.W., Jamie, J.F., Optimized expression and purification of recombinant human indoleamine 2,3-dioxygenase. Protein Expres Purif. 37 (2004), 392–398.
41. [41] Takikawa, O., Kuroiwa, T., Yamazaki, F., 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 (1988), 2041–2048.
42. [42] Austin, C.J.D., Astelbauer, F., Satyaputra, P.K., Ball, H.J., Willows, R.D., Jamie, J.F., Hunt, N.H., Mouse and human indoleamine 2, 3-dioxygenase display some distinct biochemical and structural properties. Amino Acids 36 (2009), 99–106.