Detailed analysis and follow-up studies of a high-throughput screening for indoleamine 2,3-dioxygenase 1 (IDO1) inhibitors

European Journal of Medicinal Chemistry

Volumn 84, Issue , 2014, Pages 284-301

  Röhrig, Ute F ^a   Majjigapu, Somi Reddy ^a,b   Chambon, Marc ^b   Bron, Sylvian ^a   Pilotte, Luc ^c,d   Colau, Didier ^c,d   Van Den Eynde, Benoît J ^c,d   Turcatti, Gerardo ^b   Vogel, Pierre ^b   Zoete, Vincent ^a   Michielin, Olivier ^a,e,f  

^a SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^b EPFL   (Switzerland)

^c DE DUVE INSTITUTE   (Belgium)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^e LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^f UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Cancer immunotherapy; Enzyme inhibition; High throughput screening; In silico drug design; Indoleamine 2,3 dioxygenase; Molecular dynamics simulations; Structure activity relationship; Tryptophan metabolism

Indexed keywords

AMIODARONE; BIFONAZOLE; BUTOCONAZOLE; CICLOPIROX; ECONAZOLE; ENILCONAZOLE; IMIDAZOLE; INDOLEAMINE 2,3 DIOXYGENASE 1 INHIBITOR; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; ISOCONAZOLE; LIRANAFTATE; MERCAPTOPURINE; MICONAZOLE; NIFEDIPINE; NISOLDIPINE; OXICONAZOLE; PHENTERMINE; RALOXIFENE; SERTACONAZOLE; SULCONAZOLE; TIOCONAZOLE; UNCLASSIFIED DRUG; ANTIFUNGAL AGENT; ENZYME INHIBITOR; IDO1 PROTEIN, MOUSE; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3-DIOXYGENASE 1, HUMAN; 1 (2 ((2,4 DICHLOROBENZYL)OXY)ETHYL) 1H IMIDAZOLE; 1 (2 (2,4 DICHLOROPHENYL) 2 METHOXYETHYL) 1H IMIDAZOLE; 1 (2 CHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANOL; 1 (2,4 DICHLOROBENZYL) 1H IMIDAZOLE; 1 (2,4 DICHLOROPHENETHYL) 1H IMIDAZOLE; 1 (2,4 DICHLOROPHENYL) 2 (1H 1,2,3 TRIAZOL 5 YL)ETHANOL; 1 (2,4 DICHLOROPHENYL) 2 (1H 1,2,4 TRIAZOL 1 YL)ETHANOL; 1 (2,4 DICHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANOL; 1 (2,6 DICHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANOL; 1 (3 CHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANOL; 1 (3,4 DICHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANOL; 1 (4 CHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHANOL; 1 PHENYLETHYL 1H IMIDAZOLE; 2 (1 HYDROXY 2 (1H IMIDAZOL 1 YL)ETHYL)PHENOL; 2 (1H IMIDAZOL 1 YL) 1 PHENYLETHANOL; 3 ((1 (2,4 DICHLOROPHENYL) 2 (1H IMIDAZOL 1 YL)ETHOXY) METHYL)PYRIDINE; 4 (3 BROMOPHENYL) 1,2,3 TRIAZOLE; IMIDAZOLE DERIVATIVE; KETOCONAZOLE; TRIAZOLE DERIVATIVE; UNINDEXED DRUG;

ARTICLE; CYCLING; FOLLOW UP; FOOD AND DRUG ADMINISTRATION; HIGH THROUGHPUT SCREENING; IC 50; NONHUMAN; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMISTRY; DOSE RESPONSE; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MOUSE; STRUCTURE ACTIVITY RELATION; AGGREGATION; ANIMAL CELL; CHEMICAL MODIFICATION; CHEMICAL REACTIVITY; COMPUTER MODEL; CONTROLLED STUDY; DRUG ACTIVITY; DRUG APPROVAL; DRUG IDENTIFICATION; DRUG MECHANISM; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYMATIC ASSAY; ENZYME INHIBITION; IC50; IN VITRO STUDY; LD50; MOLECULAR DOCKING; OXIDATION REDUCTION POTENTIAL; REDOX CYCLING;

ANIMALS; ANTIFUNGAL AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MICE; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84904550453     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2014.06.078     Document Type: Article

References (117)

1. L. Vécsei, L. Szalárdy, F. Fülöp, and J. Toldi Kynurenines in the CNS: recent advances and new questions Nat. Rev. Drug Dis. 12 2013 64 82 10.1038/nrd3793
2. H. Barth, and S. Raghuraman Persistent infectious diseases say - IDO. Role of indoleamine-2,3-dioxygenase in disease pathogenesis and implications for therapy Crit. Rev. Microbiol. 40 2014 360 368 10.3109/1040841X.2012.742037
3. T.W. Stone, N. Stoy, and L.G. Darlington An expanding range of targets for kynurenine metabolites of tryptophan Trends Pharmacol. Sci. 34 2013 136 143 10.1016/j.tips.2012.09.006
4. D.H. Munn, and A.L. Mellor Indoleamine 2,3 dioxygenase and metabolic control of immune responses Trends Immunol. 34 2013 137 143 10.1016/j.it.2012. 10.001
5. S. Yamamoto, and O. Hayaishi Tryptophan pyrrolase of rabbit intestine. d- and l-tryptophan-cleaving enzyme or enzymes J. Biol. Chem. 242 1967 5260 5266
6. M. Platten, W. Wick, and B.J. Van den Eynde Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion Cancer Res. 72 2012 5435 5440 10.1158/0008-5472.CAN-12-0569
7. C. Uyttenhove, L. Pilotte, I. Théate, V. Stroobant, D. Colau, N. Parmentier, T. Boon, and B.J. Van den Eynde Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase Nat. Med. 9 2003 1269 1274 10.1038/nm934 (Pubitemid 37279849)
8. C. Du, and Y. Wang The immunoregulatory mechanisms of carcinoma for its survival and development J. Exp. Clin. Cancer Res. 30 2011 12 10.1186/1756-9966-30-12
9. C.A. Opitz, U.M. Litzenburger, F. Sahm, M. Ott, I. Tritschler, S. Trump, T. Schumacher, L. Jestaedt, D. Schrenk, M. Weller, M. Jugold, G.J. Guillemin, C.L. Miller, C. Lutz, B. Radlwimmer, I. Lehmann, A. von Deimling, W. Wick, and M. Platten An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor Nature 478 2011 197 203 10.1038/nature10491
10. L. Pilotte, P. Larrieu, V. Stroobant, D. Colau, E. Dolušić, R. Frédérick, E.D. Plaen, C. Uyttenhove, J. Wouters, B. Masereel, and B.J. Van den Eynde Reversal of tumoral immune resistance by inhibition of tryptophan 2,3-dioxygenase Proc. Natl. Acad. Sci. U. S. A. 109 2012 2497 2502 10.1073/pnas.1113873109
11. J. Godin-Ethier, L.-A. Hanafi, C.A. Piccirillo, and R. Lapointe Indoleamine 2,3-dioxygenase expression in human cancers: clinical and immunologic perspectives Clin. Canc. Res. 17 2011 6985 6991 10.1158/1078-0432. CCR-11-1331
12. J.B. Katz, A.J. Muller, and G.C. Prendergast Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape Immunol. Rev. 222 2008 206 221 10.1111/j.1600-065X.2008.00610.x (Pubitemid 351430372)
13. G.C. Prendergast Immune escape as a fundamental trait of cancer: focus on IDO Oncogene 27 2008 3889 3900 10.1038/onc.2008.35 (Pubitemid 351913639)
14. A.J. Muller, J.B. DuHadaway, P.S. Donover, E. Sutanto-Ward, and G.C. Prendergast Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene bin1, potentiates cancer chemotherapy Nat. Med. 11 2005 312 319 10.1038/nm1196 (Pubitemid 40460560)
15. X. Liu, N. Shin, H.K. Koblish, G. Yang, Q. Wang, K. Wang, L. Leffet, M.J. Hansbury, B. Thomas, M. Rupar, P. Waeltz, K.J. Bowman, P. Polam, R.B. Sparks, E.W. Yue, Y. Li, R. Wynn, J.S. Fridman, T.C. Burn, A.P. Combs, R.C. Newton, and P.A. Scherle Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity Blood 115 2010 3520 3530 10.1182/blood-2009-09-246124
16. E. Dolušić, and R. Frédérick Indoleamine 2,3-dioxygenase inhibitors: a patent review (2008-2012) Expert Opin. Ther. Targets 23 2013 1367 1381 10.1517/13543776.2013.827662
17. E.W. Yue, B. Douty, B. Wayland, M. Bower, X. Liu, L. Leffet, Q. Wang, K.J. Bowman, M.J. Hansbury, C. Liu, M. Wei, Y. Li, R. Wynn, T.C. Burn, H.K. Koblish, J.S. Fridman, B. Metcalf, P.A. Scherle, and A.P. Combs Discovery of potent competitive inhibitors of indoleamine 2,3-dioxygenase with in vivo pharmacodynamic activity and efficacy in a mouse melanoma model J. Med. Chem. 52 2009 7364 7367 10.1021/jm900518f
18. H.K. Koblish, M.J. Hansbury, K.J. Bowman, G. Yang, C.L. Neilan, P.J. Haley, T.C. Burn, P. Waeltz, R.B. Sparks, E.W. Yue, A.P. Combs, P.A. Scherle, K. Vaddi, and J.S. Fridman Hydroxyamidine inhibitors of indoleamine-2,3- dioxygenase potently suppress systemic tryptophan catabolism and the growth of ido-expressing tumors Mol. Cancer Ther. 9 2010 489 498 10.1158/1535-7163.MCT-09- 0628
19. M.R. Mautino, F.A. Jaipuri, J. Waldo, S. Kumar, J. Adams, C. Van Allen, A. Marcinowicz-Flick, D. Munn, N.N. Vahanian, and C.J. Link NLG919, a novel indoleamine-2,3-dioxygenase (IDO)-pathway inhibitor drug candidate for cancer therapy [abstract] Proceedings of the 104th Annual Meeting of the American Association for Cancer Research; 2013 Apr 6-10; Washington, DC Cancer Res. vol. 73 2013 Philadelphia (PA)
20. N. Thorne, D.S. Auld, and J. Inglese Apparent activity in high-throughput screening: origins of compound-dependent assay interference Curr. Opin. Chem. Biol. 14 2010 315 324 10.1016/j.cbpa.2010.03.020
21. E. Vottero, A. Balgi, K. Woods, S. Tugendreich, T. Melese, R.J. Andersen, A.G. Mauk, and M. Roberge Inhibitors of human indoleamine 2,3-dioxygenase identified with a target-based screen in yeast Biotechnol. J. 1 2006 282 288 10.1002/biot.200600001
22. M. Cerejo, G. Andrade, C. Roca, J. Sousa, C. Rodrigues, R. Pinheiro, S. Chatterjee, H. Vieira, and P. Calado A powerful yeast-based screening assay for the identification of inhibitors of indoleamine 2,3-dioxygenase J. Biomol. Screen. 17 2012 1362 1371 10.1177/1087057112452595
23. D. Meininger, L. Zalameda, Y. Liu, L.P. Stepan, L. Borges, J.D. McCarter, and C.L. Sutherland Purification and kinetic characterization of human indoleamine 2,3-dioxygenases 1 and 2 (IDO1 and IDO2) and discovery of selective IDO1 inhibitors Biochim. Biophys. Acta 1814 2011 1947 1954 10.1016/j.bbapap. 2011.07.023
24. P. Tomek, B.D. Palmer, J.U. Flanagan, S.-P.S. Fung, D.J.A. Bridewell, J.F. Jamie, and L.-M. Ching Formation of an N-formylkynurenine-derived fluorophore and its use for measuring indoleamine 2,3-dioxygenase 1 activity Anal. Bioanal. Chem. 405 2013 2515 2524 10.1007/s00216-012-6650-y
25. S.-P.S. Fung, H. Wang, P. Tomek, C.J. Squire, J.U. Flanagan, B.D. Palmer, D.J. Bridewell, S.M. Tijono, J.F. Jamie, and L.-M. Ching Discovery and characterisation of hydrazines as inhibitors of the immune suppressive enzyme, indoleamine 2,3-dioxygenase 1 (IDO1) Bioorg. Med. Chem. 21 2013 7595 7603 10.1016/j.bmc.2013.10.037
26. S.M. Bakmiwewa, A. Fatokun, A. Tran, R.J. Payne, N.H. Hunt, and H.J. Ball Identification of selective inhibitors of indoleamine 2,3-dioxygenase 2 Bioorg. Med. Chem. Lett. 22 2012 7641 7646 10.1016/j.bmcl.2012.10.010
27. A. Mullard Drug repurposing programmes get lift off Nat. Rev. Drug Dis. 11 2012 505 506 10.1038/nrd3776
28. J. Seidler, S.L. McGovern, T.N. Doman, and B.K. Shoichet Identification and prediction of promiscuous aggregating inhibitors among known drugs J. Med. Chem. 46 2003 4477 4486 10.1021/jm030191r (Pubitemid 37238749)
29. 2 by redox cycling in reducing environments Assay Drug Dev. Technol. 8 2010 152 174 10.1089/adt.2009.0247
30. M. Hann, B. Hudson, X. Lewell, R. Lifely, L. Miller, and N. Ramsden Strategic pooling of compounds for high-throughput screening J. Chem. Inf. Comput. Sci. 39 1999 897 902 10.1021/ci990423o
31. J.F. Blake Identification and evaluation of molecular properties related to preclinical optimization and clinical fate Med. Chem. 1 2005 649 655 10.2174/15734060577459808
32. J.R. Huth, R. Mendoza, E.T. Olejniczak, R.W. Johnson, D.A. Cothron, Y. Liu, C.G. Lerner, J. Chen, and P.J. Hajduk ALARM NMR: a rapid and robust experimental method to detect reactive false positives in biochemical screens J. Am. Chem. Soc. 127 2005 217 224 10.1021/ja0455547 (Pubitemid 40094385)
33. J.B. Baell, and G. Holloway New substructure filters for removal of pan assay interference compounds (PAINS) from screening libraries and for their exclusion in bioassays J. Med. Chem. 53 2010 2719 2740 10.1021/jm901137j
34. R.F. Bruns, and I. Watson Rules for identifying potentially reactive or promiscuous compounds J. Med. Chem. 55 2012 9763 9772 10.1021/jm301008n
35. J.T. Pearson, S. Siu, D.P. Meininger, L.C. Wienkers, and D.A. Rock In vitro modulation of cytochrome p450 reductase supported indoleamine 2,3-dioxygenase activity by allosteric effectors cytochrome b(5) and methylene blue Biochemistry 49 2010 2647 2656 10.1021/bi100022c
36. L. Lor, J. Schneck, D.E. McNulty, E. Diaz, M. Brandt, S.H. Thrall, and B. Schwartz A simple assay for detection of small-molecule redox activity J. Biomol. Screen. 12 2007 881 890 10.1177/1087057107304113 (Pubitemid 47340702)
37. 2 in HTS buffers containing strong reducing reagents-real hits or promiscuous artifacts? Curr. Opin. Chem. Biol. 15 2011 174 182 10.1016/j.cbpa.2010.10.022
38. B.K. Shoichet Screening in a spirit haunted world Drug Discov. Today 11 2006 607 615 10.1016/j.drudis.2006.05.014
39. B.Y. Feng, and B.K. Shoichet A detergent-based assay for the detection of promiscuous inhibitors Nat. Protoc. 1 2006 550 553 10.1038/nprot.2006.77
40. U.F. Röhrig, L. Awad, A. Grosdidier, P. Larrieu, V. Stroobant, D. Colau, V. Cerundolo, A.J.G. Simpson, P. Vogel, B.J. Van den Eynde, V. Zoete, and O. Michielin Rational design of indoleamine 2,3-dioxygenase inhibitors J. Med. Chem. 53 2010 1172 1189 10.1021/jm9014718
41. U.F. Röhrig, S.R. Majjigapu, A. Grosdidier, S. Bron, V. Stroobant, L. Pilotte, D. Colau, P. Vogel, B.J. Van den Eynde, V. Zoete, and O. Michielin Rational design of 4-aryl-1,2,3-triazoles for indoleamine 2,3-dioxygenase 1 inhibition J. Med. Chem. 55 2012 5270 5290 10.1021/jm300260v
42. T. Ohnishi, F. Hirata, and O. Hayaish Indoleamine 2,3-dioxygenase. Potassium superoxide as substrate J. Biol. Chem. 252 1977 4643 4647 (Pubitemid 8155986)
43. J.-H. Zhang A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screen. 4 1999 67 73 10.1177/108705719900400206 (Pubitemid 29278954)
44. Y. Eberhard, S.P. McDermott, X. Wang, M. Gronda, A. Venugopal, T.E. Wood, R. Hurren, A. Datti, R. a. Batey, J. Wrana, W.E. Antholine, J.E. Dick, J. Dick, and A.D. Schimmer Chelation of intracellular iron with the antifungal agent ciclopirox olamine induces cell death in leukemia and myeloma cells Blood 114 2009 3064 3073 10.1182/blood-2009-03-209965
45. M.O. Griffin, E. Fricovsky, G. Ceballos, and F. Villarreal Tetracyclines: a pleitropic family of compounds with promising therapeutic properties. Review of the literature Am. J. Physiol. Cell P. H. 299 2010 C539 C548 10.1152/ajpcell.00047.2010
46. N. Strushkevich, S. Usanov, and H.-W. Park Structural basis of human CYP51 inhibition by antifungal azoles J. Mol. Biol. 397 2010 1067 1078 10.1016/j.jmb.2010.01.075
47. S.F. Muakkassah, and W.C. Yang Mechanism of the inhibitory action of phenelzine on microsomal drug metabolism J. Pharmacol. Exp. Ther. 219 1981 147 155 (Pubitemid 11018643)
48. C.J.D. Austin, F. Astelbauer, P. Kosim-Satyaputra, H.J. Ball, R.D. Willows, J.F. Jamie, and N.H. Hunt Mouse and human indoleamine 2,3-dioxygenase display some distinct biochemical and structural properties Amino Acids 36 2009 99 106 10.1007/s00726-008-0037-6
49. A.C. Terentis, M. Freewan, T.S.S. Plaza, M.J. Raftery, R. Stocker, and S.R. Thomas The selenazal drug ebselen potently inhibits indoleamine 2,3-dioxygenase by targeting enzyme cysteine residues Biochemistry 49 2010 591 600 10.1021/bi901546e
50. B. Shoichet, A. Doak, and K. Ziebart Aggregator Advisor 2013 http://advisor.bkslab.org
51. A.J. Ryan, N.M. Gray, P.N. Lowe, and C.-w. Chung Effect of detergent on "promiscuous" inhibitors J. Med. Chem. 46 2003 3448 3451 10.1021/jm0340896 (Pubitemid 36909819)
52. H.C. Brastianos, E. Vottero, B.O. Patrick, R.V. Soest, T. Matainaho, A.G. Mauk, and R.J. Andersen Exiguamine a, an indoleamine-2,3-dioxygenase (IDO) inhibitor isolated from the marine sponge neopetrosia exigua J. Am. Chem. Soc. 128 2006 16046 16047 10.1021/ja067211 (Pubitemid 44936592)
53. R. Andersen, A. Pereira, X.-H. Huang, G. Mauk, E. Vottero, M. Roberge, A. Balgi. Indoleamine 2,3-Dioxygenase (IDO) Inhibitors. Patent WO 2006/005185 (01 2006).
54. A. Pereira, E. Vottero, M. Roberge, A.G. Mauk, and R.J. Andersen Indoleamine 2,3-dioxygenase inhibitors from the northeastern pacific marine hydroid garveia annulata J. Nat. Prod. 69 2006 1496 1499 10.1021/np060111x (Pubitemid 44899767)
55. R. Andersen, M. Leblanc, H. Brastianos, E. Vottero, M. Roberge, G. Mauk, G. Carr. Substituted Quinone Indoleamine 2,3-Dioxygenase (IDO) Inhibitors and Synthesis and Uses Thereof. Patent WO 2008/052352 (05 2008).
56. G. Carr, M.K.W. Chung, A.G. Mauk, and R.J. Andersen Synthesis of indoleamine 2,3-dioxygenase inhibitory analogues of the sponge alkaloid exiguamine a J. Med. Chem. 51 2008 2634 2637 10.1021/jm800143h (Pubitemid 351620784)
57. S. Kumar, W. Malachowski, J. Duhadaway, J. Lalonde, P. Carroll, D. Jaller, R. Metz, G. Prendergast, and A. Muller Indoleamine 2,3-dioxygenase is the anticancer target for a novel series of potent naphthoquinone-based inhibitors J. Med. Chem. 51 2008 1706 1718 10.1021/jm7014155 (Pubitemid 351438852)
58. G. Carr, W. Tay, H. Bottriell, S.K. Andersen, A.G. Mauk, and R.J. Andersen Plectosphaeroic acids a, b, and c, indoleamine 2,3-dioxygenase inhibitors produced in culture by a marine isolate of the fungus Plectosphaerella cucumerina Org. Lett. 11 2009 2996 2999 10.1021/ol900972j
59. E. Dolušić, P. Larrieu, C. Meinguet, D. Colette, A. Rives, S. Blanc, T. Ferain, L. Pilotte, V. Stroobant, J. Wouters, B. Van den Eynde, B. Masereel, E. Delfourne, and R. Frédérick Indoleamine 2,3-dioxygenase inhibitory activity of derivatives of marine alkaloid tsitsikammamine A Bioorg. Med. Chem. Lett. 23 2013 47 54 10.1016/j.bmcl.2012.11. 036
60. D.J. Bridewell, J. Sperry, J.R. Smith, P. Kosim-Satyaputra, L.-M. Ching, J.F. Jamie, and M. Brimble Natural product-inspired pyranonaphthoquinone inhibitors of indoleamine 2,3-dioxygenase-1 (IDO-1) Aust. J. Chem. 66 2013 40 10.1071/CH12393
61. R. Pasceri, D. Siegel, D. Ross, and C.J. Moody Aminophenoxazinones as inhibitors of indoleamine 2,3-dioxygenase (IDO). Synthesis of exfoliazone and chandrananimycin A J. Med. Chem. 56 2013 3310 3317 10.1021/jm400049z
62. H.E. Flick, J.M. Lalonde, W.P. Malachowski, and A.J. Muller The tumor-selective cytotoxic agent β-lapachone is a potent inhibitor of IDO1 Int. J. Tryptophan Res. 6 2013 35 45 10.4137/IJTR.S12094
63. G. Pantouris, and C.G. Mowat Antitumour agents as inhibitors of tryptophan 2,3-dioxygenase Biochem. Biophys. Res. Commun. 443 2014 28 31 10.1016/j.bbrc.2013.11.037
64. P. Rana, R. Naven, A. Narayanan, Y. Will, and L.H. Jones Chemical motifs that redox cycle and their associated toxicity MedChemComm 4 2013 1175 10.1039/c3md00149k
65. S. Bittner When quinones meet amino acids: chemical, physical and biological consequences Amino acids 30 2006 205 224 10.1007/s00726-005-0298-2 (Pubitemid 43724048)
66. S. Kumar, D. Jaller, B. Patel, J.M. LaLonde, J.B. DuHadaway, W.P. Malachowski, G.C. Prendergast, and A.J. Muller Structure based development of phenylimidazole-derived inhibitors of indoleamine 2,3-dioxygenase J. Med. Chem. 51 2008 4968 4977 10.1021/jm800512z
67. M. Mautino, S. Kumar, F. Jaipuri, J. Waldo, T. Kesharwani, N. N. Vahanian, C. J. Link, J. Lalonde, G. Prendergast, A. Muller, W. Malachowski. IDO Inhibitors. Patent WO 2009/132238.
68. M. Mautino, S. Kumar, F. Jaipuri, J. Waldo, T. Kesharwani, X. Zhang. Imidazole Derivatives as IDO Inhibitors. Patent WO 2011/056652.
69. M. Mautino, S. Kumar, J. Waldo, F. Jaipuri, T. Kesharwani, X. Zhang. Fused Imidazole Derivatives Useful as IDO Inhibitors. Patent WO 2012/142237.
70. 2 incorporation by a heme-containing dioxygenase Proc. Natl. Acad. Sci. U. S. A. 103 2006 2611 2616 10.1073/pnas.0508996103
71. E. Dolušić, P. Larrieu, S. Blanc, F. Sapunaric, J. Pouyez, L. Moineaux, D. Colette, V. Stroobant, L. Pilotte, D. Colau, T. Ferain, G. Fraser, M. Galleni, J.-M. Frère, B. Masereel, B. Van den Eynde, J. Wouters, and R. Frédérick Discovery and preliminary SARS of keto-indoles as novel indoleamine 2,3-dioxygenase (IDO) inhibitors Eur. J. Med. Chem. 46 2011 3058 3065 10.1016/j.ejmech.2011.02.049
72. J.R. Smith, K.J. Evans, A. Wright, R.D. Willows, J.F. Jamie, and R. Griffith Novel indoleamine 2,3-dioxygenase-1 inhibitors from a multistep in silico screen Bioorg. Med. Chem. 20 2012 1354 1363 10.1016/j.bmc.2011.10.068
73. A. Grosdidier, V. Zoete, and O. Michielin Fast docking using the charmm force field with eadock dss J. Comput. Chem. 32 2011 2149 2159 10.1002/jcc.21797
74. E. Cuevas Yañez, A. Canul Sánchez, J.M. Serrano Becerra, J.M. Muchowski, and R. Cruz Almanza Synthesis of miconazole and Analogs through a Carbenoid Intermediate Rev. Soc. Quim. Mex. 48 2004 49 52
75. J.Z. Vlahakis, C. Lazar, G. Roman, D. Vukomanovic, K. Nakatsu, and W.A. Szarek Heme oxygenase inhibition by α-(1H-imidazol-1-yl)-ω- phenylalkanes: effect of introduction of heteroatoms in the alkyl linker ChemMedChem 7 2012 897 902 10.1002/cmdc.201100602
76. G. Roman, J.Z. Vlahakis, D. Vukomanovic, K. Nakatsu, and W.A. Szarek Heme oxygenase inhibition by 1-aryl-2-(1h-imidazol-1-yl/1h-1,2,4-triazol-1-yl) ethanones and their derivatives ChemMedChem 5 2010 1541 1555 10.1002/cmdc.201000120
77. J.-X. Wang, X. Jia, T. Meng, and L. Xin Rapid and solvent-free synthesis of Homoallyl or Homopropargyl alcohols mediated by zinc powder Synthesis 2005 2005 2838 2844 10.1055/s-2005-872178 (Pubitemid 41680047)
78. T. Jin, S. Kamijo, and Y. Yamamoto Copper-catalyzed synthesis of N-unsubstituted 1,2,3-triazoles from nonactivated terminal alkynes Eur. J. Org. Chem. 18 2004 3789 3791 10.1002/ejoc.200400442
79. D. Dehe, I. Munstein, A. Reis, and W.R. Thiel Mild transition-metal-free amination of fluoroarenes catalyzed by fluoride ions J. Org. Chem. 76 2011 1151 1154 10.1021/jo102063s
80. K. Matsuno, K. Takai, Y. Isaka, Y. Unno, M. Sato, O. Takikawa, and A. Asai S-benzylisothiourea derivatives as small-molecule inhibitors of indoleamine-2,3-dioxygenase Bioorg. Med. Chem. Lett. 20 2010 5126 5129 10.1016/j.bmcl.2010.07.025
81. A. Grosdidier, V. Zoete, and O. Michielin EADock: docking of small molecules into protein active sites with a multiobjective evolutionary optimization Proteins 67 2007 1010 1025 10.1002/prot.21367 (Pubitemid 46753948)
82. A. Grosdidier, V. Zoete, and O. Michielin Blind docking of 260 protein-ligand complexes with EADock 2.0 J. Comput. Chem. 30 2009 2021 2030 10.1002/jcc.21202
83. V. Zoete, A. Grosdidier, M. Cuendet, and O. Michielin Use of the FACTS solvation model for protein-ligand docking calculations. Application to EADock J. Mol. Recognit. 23 2010 457 461 10.1002/jmr.1012
84. V. Zoete, A. Grosdidier, T. Schuepbach, O. Michielin, Attracting Cavities (manuscript in preparation).
85. A.D. MacKerell Jr., D. Bashford, M. Bellott, R.L. Dunbrack Jr., J.D. Evanseck, M.J. Field, S. Fischer, J. Gao, H. Guo, S. Ha, D. Joseph-McCarthy, L. Kuchnir, K. Juczera, F.T.K. Lau, C. Mattos, S. Michnik, T. Ngo, D.T. Nguyen, B. Prodhom, W.E. Reiher III, B. Roux, M. Schlenkrich, J.C. Smith, R. Stote, J. Straub, M. Watanabe, J. Wiórkiewicz-Kuczera, D. Yin, and M. Karplus All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 102 1998 3586 3616 10.1021/jp973084f (Pubitemid 128576688)
86. U. Haberthür, and A. Caflisch Facts: fast analytical continuum treatment of solvation J. Comput. Chem. 29 2008 701 715 10.1002/jcc.20832 (Pubitemid 351364845)
87. V. Zoete, A. Grosdidier, M. Cuendet, and O. Michielin Use of the FACTS solvation model for protein-ligand docking calculations. Application to EADock J. Mol. Recognit. 23 2010 457 461 10.1002/jmr.1012
88. V. Zoete, M.A. Cuendet, A. Grosdidier, and O. Michielin SwissParam: a fast force field generation tool for small organic molecules J. Comput. Chem. 32 2011 2359 2368 10.1002/jcc.21816
89. U.F. Röhrig, A. Grosdidier, V. Zoete, and O. Michielin Docking to heme proteins J. Comput. Chem. 30 2009 2305 2315 10.1002/jcc.21244
90. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447 10.1021/ct700301q
91. A.D. MacKerell, M. Feig, and C.L. Brooks Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations J. Comput. Chem. 25 2004 1400 1415 10.1002/jcc.20065
92. P. Bjelkmar, P. Larsson, M.A. Cuendet, B. Hess, and E. Lindahl Implementation of the CHARMM force field in GROMACS: analysis of protein stability effects from correction maps, virtual interaction sites, and water models J. Chem. Theory Comput. 6 2010 459 466 10.1021/ct900549r
93. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.W. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1983 926 10.1063/1.445869
94. U. Essmann, L. Perera, M.L. Berkowitz, T. Darden, H. Lee, and L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 10.1063/1.470117
95. B. Hess P-LINCS: a parallel linear constraint solver for molecular simulation J. Chem. Theory Comput. 4 2008 116 122 10.1021/ct700200b
96. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101 10.1063/1.2408420 (Pubitemid 46068390)
97. H.J.C. Berendsen, J.P.M. Postma, W.F. van Gunsteren, A. DiNola, and J.R. Haak Molecular dynamics with coupling to an external bath J. Chem. Phys. 81 1984 3684 10.1063/1.448118
98. M.J.S. Dewar, E.G. Zoebisch, E.F. Healy, and J.J.P. Stewart AM1: a new general purpose quantum mechanical molecular model J. Am. Chem. Soc. 107 1985 3902 3909 10.1021/ja00299a024
99. M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G.A. Petersson, H. Nakatsuji, M. Caricato, X. Li, H.P. Hratchian, A.F. Izmaylov, J. Bloino, G. Zheng, J.L. Sonnenberg, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, J.A. Montgomery Jr., J.E. Peralta, F. Ogliaro, M. Bearpark, J.J. Heyd, E. Brothers, K.N. Kudin, V.N. Staroverov, R. Kobayashi, J. Normand, K. Raghavachari, A. Rendell, J.C. Burant, S.S. Iyengar, J. Tomasi, M. Cossi, N. Rega, J.M. Millam, M. Klene, J.E. Knox, J.B. Cross, V. Bakken, C. Adamo, J. Jaramillo, R. Gomperts, R.E. Stratmann, O. Yazyev, A.J. Austin, R. Cammi, C. Pomelli, J.W. Ochterski, R.L. Martin, K. Morokuma, V.G. Zakrzewski, G.A. Voth, P. Salvador, J.J. Dannenberg, S. Dapprich, A.D. Daniels, Ö. Farkas, J.B. Foresman, J.V. Ortiz, J. Cioslowski, and D.J. Fox Gaussian 09 Revision A.1 2009 Gaussian Inc Wallingford CT
100. R.V. Bensasson, S. Sowlati-Hashjin, V. Zoete, D. Dauzonne, and C.F. Matta Physicochemical properties of exogenous molecules correlated with their biological efficacy as protectors against carcinogenesis and inflammation Int. Rev. Phys. Chem. 32 2013 393 434 10.1080/0144235X.2013.767669
101. V. Barone, and M. Cossi Quantum calculation of molecular energies and energy gradients in solution by a conductor solvent model J. Phys. Chem. A 102 1998 1995 10.1021/jp9716997
102. M. Cossi, N. Rega, G. Scalmani, and V. Barone Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model J. Comput. Chem. 24 2003 669 10.1002/jcc.10189
103. E.J. Lynch, A.L. Speelman, B.A. Curry, C.S. Murillo, and J.G. Gillmore Expanding and testing a computational method for predicting the ground state reduction potentials of organic molecules on the basis of empirical correlation to experiment J. Org. Chem. 77 2012 6423 6430 10.1021/jo300853k
104. A. Becke Density-functional thermochemistry. iii. The role of exact exchange J. Chem. Phys. 98 1993 5648 5652 10.1063/1.464913
105. C. Lee, W. Yang, and R. Parr Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. B 37 1988 785 789 10.1103/PhysRevB.37.785
106. D.D. Méndez-Hernández, P. Tarakeshwar, D. Gust, T. a. Moore, A.L. Moore, and V. Mujica Simple and accurate correlation of experimental redox potentials and DFT-calculated HOMO/LUMO energies of polycyclic aromatic hydrocarbons J. Mol. Model 19 2013 2845 2848 10.1007/s00894-012-1694-7
107. W.N. Cannon, C.E. Powell, and R.G. Jones Studies of imidazoles. VII. Substituted 1-phenethylimidazoles and related compounds J. Org. Chem. 22 1957 1323 1326 10.1021/jo01362a008
108. M.R. Cuberes, M. Moreno-Mañas, and A. Trius α-Lithiation of N-arylmethylimidazoles and triazoles: a general method for the synthesis of 1,2-diaryl-1-(N-azolyl)-ethanes Synthesis 1985 1985 302 304 10.1055/s-1985-31187
109. Y. Wahbi, C. Tournaire, R. Caujolle, M. Payard, M. Linas, and J. Seguela Aliphatic ethers and esters of 1-(2,4-dichlorophenyl)-2-(1H-imidazolyl) ethanol: study of antifungal activity against yeasts and hydrophobic character Eur. J. Med. Chem. 29 1994 701 706 10.1016/0223-5234(94)90032-9 (Pubitemid 24319790)
110. G.M. Dulcevscaia, V.C. Kravtsov, F.Z. Macaev, G.G. Duca, E.P. Stingachi, S.I. Pogrebnoi, V.V. Boldescu, S.F. Clapco, J.P. Tiurina, A.A. Deseatnic-Ciloci, J. Lipkowski, S.-X. Liu, S. Decurtins, and S.G. Baca New copper(II) complexes with isoconazole: synthesis, structures and biological properties Polyhedron 52 2013 106 114 10.1016/j.poly.2012.10.040
111. R. Torregrosa, I.M. Pastor, and M. Yus Solvent-free direct regioselective ring opening of epoxides with imidazoles Tetrahedron 63 2007 469 473 10.1016/j.tet.2006.10.055 (Pubitemid 44838792)
112. Y. Iwasaki, T. Fujita, H. Yabe, H. Hirao, K. Kitagawa, S. Futaki, T. Inoue, T. Matsuzaki, and T. Akita Synthesis and antifungal activity of a series of novel 2-propen-1-one Yakugaku Zasshi 108 1988 942 950 (Pubitemid 18267211)
113. G. Sharma-Singh, D.A. Brown, F.S. Pullen, and A.G. Wright Open access capillary electrophoresis. A walk up capillary electrophoresis service for the synthetic chemist J. Chromatogr. A 888 2000 219 227 (Pubitemid 30440712)
114. E. F. Godefroi, J. Heeres. 1-(Beta-aryl)Ethyl-Imidazole Derivatives. Patent DE 1940388 (1970).
115. Z.-F. Li, and F.-Y. Luo Jingxi Huagong 22 2005 619 624
116. K. Oh, K. Nakai, K. Yamada, and Y. Yoshizawa Synthesis of novel triazole derivatives as potent inhibitor of allene oxide synthase (CYP74A), a key enzyme in jasmonic acid biosynthesis J. Pestic. Sci. 37 2012 80 84 10.1584/jpestics. D11-006
117. E.F. Pettersen, T. Goddard, C. Huang, G. Couch, D. Greenblatt, E. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612 10.1002/jcc.20084