815
Views
0
CrossRef citations to date
0
Altmetric
Review

Research Progress of Indoleamine 2,3-Dioxygenase Inhibitors

, , , , &
Pages 185-201 | Published online: 16 Feb 2015

References

  • Zamanakou M , GermenisAE, KaranikasV. Tumor immune escape mediated by indoleamine 2, 3-dioxygenase. Immunol. Lett.111 (2), 69–75 (2007).
  • Uyttenhove PL , ThéateI, StroobantVet al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2, 3-dioxygenase. Nat. Med.9 (10), 1269–1274 (2003).
  • Pearson JT , SiuS, MeiningerDP, WienkersLC, RockDA. In vitro modulation of cytochrome P450 reductase supported indoleamine 2,3-dioxygenase activity by allosteric effectors cytochrome b(5) and methylene blue. Biochemistry49, 2647–2656 (2010).
  • Capece L , Lewis-BallesterA, BatabyalDet al. The first step of the dioxygenation reaction carried out by tryptophan dioxygenase and indoleamine 2,3-dioxygenase as revealed by quantum mechanical/molecular mechanical studies. J. Biol. Inorg. Chem.15 (6), 811–823 (2010).
  • Rafice S , ChauhanN, EfimovI, BasranJ, RavenE. Oxidation of L-tryptophan in biology: a comparison between tryptophan 2, 3-dioxygenase and indoleamine 2, 3-dioxygenase. Biochem. Soc. Trans.37 (2), 408 (2009).
  • Munn DH . Blocking IDO activity to enhance anti-tumor immunity. Front. Biosci.4, 734–745 (2012).
  • Werner-Felmayer G , WernerER, FuchsD, HausenA, ReibneggerG, WachterH. Characteristics of interferon induced tryptophan metabolism in human cells in vitro. Biochim. Biophys. Acta1012, 142–147 (1989).
  • Mellor AL , MunnDH. Creating immune privilege: active local suppression that benefits friends, but protects foes. Nat. Rev. Immunol.8, 74–80 (2008).
  • Munn DH , MellorAL. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J. Clin. Invest.117, 1147–1154 (2007).
  • Heyes MP , SaitoK, MarkeySP. Human macrophages convert L-tryptophan into the neurotoxin quinolinic acid. Biochem. J.283, 633–635 (1992).
  • Chiarugi A , CalvaniM, MeliE, TraggiaiE, MoroniF. Synthesis and release of neurotoxic kynurenine metabolites by human monocyte-derived macrophages. J. Neuroimmunol.120 (1), 190–198 (2001).
  • Munn DH , SharmaMD, BabanBet al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity22, 633–642 (2005).
  • Munn DH . Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest.114 (2), 280–290 (2004).
  • Frumento G , RotondoR, TonettiMet 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).
  • Fallarino F , GrohmannU, KwangWHet al. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immun.4, 1206–1212 (2003).
  • Hwu P , DuMX, LapointeR, TaylorMW, YoungHA. Indoleamine 2, 3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J. Immunol.164 (7), 3596–3599 (2000).
  • Platten M , WickW, Van den EyndeBJ. Tryptophan catabolism in cancer: beyond IDO and tryptophan depletion. Cancer Res.72, 5435–5440 (2012).
  • Uyttenhove C , PilotteL, ThéateIet al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2, 3-dioxygenase. Nat. Med.9 (10), 1269–1274 (2003).
  • Okamoto A , NikaidoT, OchiaiKet al. Indoleamine 2, 3-dioxygenase serves as a marker of poor prognosis in gene expression profiles of serous ovarian cancer cells. Clin. Cancer Res.11 (16), 6030–6039 (2005).
  • Pan K , WangH, ChenMSet al. Expression and prognosis role of indoleamine 2,3-dioxygenase in hepatocellular carcinoma. J. Cancer Res. Clin.134 (11), 1247–1253 (2008).
  • Muller AJ , DuHadawayJB, DonoverPS, Sutanto-WardE, PrendergastGC. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat. Med.11 (3), 312–319 (2005).
  • Cady SG , SonoM. 1-methyl-dl-tryptophan, β-(3-benzofuranyl)-dl-alanine (the oxygen analog of tryptophan), and β-[3-benzo (b) thienyl]-dl-alanine (the sulfur analog of tryptophan) are competitive inhibitors for indoleamine 2, 3-dioxygenase. Arch. Biochem. Biophys.291 (2), 326–333 (1991).
  • Peterson AC , La LoggiaAJ, HamakerLKet al. Evaluation of substituted β-carbolines as noncompetitive indolamine 2,3-dioxygenase inhibitors. Med. Chem. Res.3 (7), 473–482 (1993).
  • Muller A , HeselerK, SchmidtSK, SpekkerK, MackenzieCR, DaubenerW. The missing link between indoleamine 2,3-dioxygenase mediated antibacterial and immunoregulatory effects. J. Cell. Mol. Med.13, 1125–1135 (2009).
  • Sono M , RoachMP, CoulterED, DawsonJH. Heme-containing oxygenases. Chem. Rev.96 (7), 2841–2888 (1996).
  • Knox WE , MehlerAH. The conversion of tryptophan to kynurenine in liver. I. The coupled tryptophan peroxidase oxidase system forming formylkynurenine. J. Biol. Chem.187, 419–430 (1950).
  • Shimizu T , NomiyamaS, HirataF, HayaishiO. Indoleamine 2, 3-dioxygenase, purification and some properties. J. Biol. Chem.253 (13), 4700–4706 (1978).
  • Ball HJ , Sanchez-PerezA, WeiserSet al. Characterization of an indoleamine 2, 3-dioxygenase-like protein found in humans and mice. Gene396 (1), 203–213 (2007).
  • Metz R , DuhadawayJB, KamasaniU, Laury-KleintopL, MullerAJ, PrendergastGC. 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 (15), 7082–7087 (2007).
  • Witkiewicz AK , CostantinoCL, MetzRet al. Genotyping and expression analysis of IDO2 in human pancreatic cancer: a novel, active target. J. Am. Coll. Surgeons208 (5), 781–787 (2009).
  • Sono M , HayaishiO. The reaction mechanism of indoleamine 2, 3-dioxygenase. Biochem. Rev.50, 173–181 (1980).
  • Sono M , TaniguchiT, WatanabeY, HayaishiO. Indoleamine 2,3-dioxygenase. Equilibrium studies of the tryptophan binding to the ferric, ferrous, and CO-bound enzymes. J. Biol. Chem.255, 1339–1345 (1980).
  • Kobayashi K , HayashiK, SonoM. Effects of tryptophan and pH on the kinetics of superoxide radical binding to indoleamine 2,3-dioxygenase studied by pulse radiolysis. J. Biol. Chem.264, 15280–15283 (1989).
  • Sugimoto H , OdaS, OtsukiTet al. Crystal structure of human indoleamine 2, 3-dioxygenase: catalytic mechanism of O2 incorporation by a heme-containing dioxygenase. Proc. Natl Acad. Sci. USA103 (8), 2611–2616 (2006).
  • Rohrig UF , AwadL, GrosdidierAEet al. Rational design of indoleamine 2,3-dioxygenase inhibitors. J. Med. Chem.53, 1172–1189 (2010).
  • Dolušić E , FrédérickR. Indoleamine 2,3-dioxygenase inhibitors: a patent review (2008 ‐‐ 2012). Expert Opin. Ther. Pat.23 (10), 1367–1381 (2013).
  • Mautino M , KumarS, JaipuriF, WaldoJ, KesharwaniT, ZhangX : WO2011056652 (2011).
  • Kwidzinski E , BunseJ, AktasOet al. Indolamine 2, 3-dioxygenase is expressed in the CNS and down-regulates autoimmune inflammation. FASEB J.19 (10), 1347–1349 (2005).
  • Owens MJ , NemeroffCB. Role of serotonin in the pathophysiology of depression: focus on the serotonin transporter. Clin. Chem.40 (2), 288–295 (1994).
  • Munn DH , ZhouM, AttwoodJTet al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science281 (5380), 1191–1193 (1998).
  • Eguchi N , WatanabeY, KawanishiK, HashimotoY, HayaishiO. Inhibition of indoleamine 2, 3-dioxygenase and tryptophan 2, 3-dioxygenase by β-carboline and indole derivatives. Arch. Biochem. Biophys.232 (2), 602–609 (1984).
  • Sono M , CadySG. Enzyme kinetic and spectroscopic studies of inhibitor and effector interactions with indoleamine 2, 3-dioxygenase. 1. Norharman and 4-phenylimidazole binding to the enzyme as inhibitors and heme ligands. Biochemistry28 (13), 5392–5399 (1989).
  • Muller AJ , MalachowskiW, PrendergastGC. Indoleamine 2,3-dioxygenase in cancer: targeting pathological immune tolerance with small-molecule inhibitors. Expert Opin. Ther. Targets9, 831–849 (2005).
  • Macchiarulo A , CamaioniE, NutiR, PellicciariR. Highlights at the gate of tryptophan catabolism: a review on the mechanisms of activation and regulation of indoleamine 2, 3-dioxygenase (IDO), a novel target in cancer disease. Amino Acids37 (2), 219–229 (2009).
  • Carr G , ChungMK, MaukAG, AndersenRJ. Synthesis of indoleamine 2, 3-dioxygenase inhibitory analogues of the sponge alkaloid exiguamine A. J. Med. Chem.51 (9), 2634–2637 (2008).
  • Hou DY , MullerAJ, SharmaMDet al. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res.67 (2), 792–801 (2007).
  • Banerjee T , DuHadawayJ, GaspariPet al. Antitumor properties of chemopreventive natural product brassinin are based upon inhibition of indoleamine 2, 3-dioxygenase (IDO). Oncogene27 (20), 2851–2857 (2008).
  • Tanaka M , LiX, HikawaHet al. Synthesis and biological evaluation of novel tryptoline derivatives as indoleamine 2,3-dioxygenase (IDO) inhibitors. Bioorg. Med. Chem.21 (5), 1159–1165 (2013).
  • Gaspari P , BanerjeeT, MalachowskiWPet al. Structure-activity study of brassinin derivatives as indoleamine 2, 3-dioxygenase inhibitors. J. Med. Chem.49 (2), 684–692 (2006).
  • Dolusic E , LarrieuP, BlancSet al. Discovery and preliminary SARs of keto-indoles as novel indoleamine 2,3-dioxygenase (IDO) inhibitors. Eur. J. Med. Chem.46 (7), 3058–3065 (2011).
  • Shoichet BK . Virtual screening of chemical libraries. Nature432 (7019), 862–865 (2004).
  • Dolušić E , LarrieuP, BlancSet al. Discovery and preliminary SARs of keto-indoles as novel indoleamine 2, 3-dioxygenase (IDO) inhibitors. Eur. J. Med. Chem.46 (7), 3058–3065 (2011).
  • Nakashima H , UtoY, NakataEet al. Synthesis and biological activity of 1-methyl-tryptophan-tirapazamine hybrids as hypoxia-targeting indoleamine 2,3-dioxygenase inhibitors. Bioorg. Med. Chem.16 (18), 8661–8669 (2008).
  • Takikawa O , KuroiwaT, YamazakiF, KidoR. 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 (4), 2041–2048 (1988).
  • Fahy E , AndersenRJ, Van DuyneGD, ClardyJ. Metabolites of the marine hydroid Garveia annulata: garveatins B and C, 2-hydroxygarvin A, and garvin A quinone. J. Org. Chem.51 (1), 57–61 (1986).
  • Fahy E , AndersenRJ, HeCH, ClardyJ. Garveatin A, an antimicrobial 1-(4H)-anthracenone derivative from the hydroid Garveia annulata. J. Org. Chem.50 (7), 1149–1150 (1985).
  • Pereira A , VotteroE, RobergeM, MaukAG, AndersenRJ. Indoleamine 2, 3-dioxygenase inhibitors from the northeastern Pacific marine hydroid Garveia annulata. J. Nat. Prod.69 (10), 1496–1499 (2006).
  • Brastianos HC , VotteroE, PatrickBOet al. Exiguamine A, an indoleamine-2, 3-dioxygenase (IDO) inhibitor isolated from the marine sponge Neopetrosia exigua. J. Am. Chem. Soc.128 (50), 16046–16047 (2006).
  • Kumar S , MalachowskiWP, DuHadawayJBet al. Indoleamine 2, 3-dioxygenase is the anticancer target for a novel series of potent naphthoquinone-based inhibitors. J. Med. Chem.51 (6), 1706–1718 (2008).
  • Lamson DW , PlazaSM. The anticancer effects of vitamin K. Altern. Med. Rev.8, 303–318 (2003).
  • Raymond JA , AlbanP, XinHH, EduardoV, MichelR, ArunaB : US20090042868A1 (2009).
  • Bridewell DJ , SperryJ, SmithJRet al. Natural product-inspired pyranonaphthoquinone inhibitors of indoleamine 2, 3-dioxygenase-1 (IDO-1). Aust. J. Chem.66 (1), 40–49 (2012).
  • Flick HE , LaLondeJM, MalachowskiWP, MullerAJ. The tumor-selective cytotoxic agent β-Lapachone is a potent inhibitor of IDO1. Int. J. Tryptophan Res.6, 35 (2013).
  • Volgraf M , LumbJP, BrastianosHCet al. Biomimetic synthesis of the IDO inhibitors exiguamine A and B. Nat. Chem. Biol.4 (9), 535–537 (2008).
  • Lu C , LinY, YehSR. Inhibitory substrate binding site of human indoleamine 2, 3-dioxygenase. J. Am. Chem. Soc.131 (36), 12866–12867 (2009).
  • Atkins S , ClarkI, SosnowskaD, HirschP, KerryB. Detection and quantification of Plectosphaerella cucumerina, a potential biological control agent of potato cyst nematodes, by using conventional PCR, real-time PCR, selective media, and baiting. Appl. Environ. Microbiol.69 (8), 4788–4793 (2003).
  • Legentil L , BenelL, BertrandV, LesurB, DelfourneE. Synthesis and antitumor characterization of pyrazolic analogues of the marine pyrroloquinoline alkaloids: wakayin and tsitsikammamines. J. Med. Chem.49 (10), 2979–2988 (2006).
  • Dolušic´ E , LarrieuP, MeinguetCet al. Indoleamine 2,3-dioxygenase inhibitory activity of derivatives of marine alkaloid tsitsikammamine A. Bioorg. Med. Chem. Lett.23 (1), 47–54 (2013).
  • Mautino M , KumarS, JaipuriFet al. : WO2009132238 (2009).
  • Kumar S , JallerD, PatelBet al. Structure based development of phenylimidazole-derived inhibitors of indoleamine 2, 3-dioxygenase. J. Med. Chem.51 (16), 4968–4977 (2008).
  • Mautino M , KumarS, JaipuriF, WaldoJ, KesharwaniT, ZhangX : WO2011056652 (2011).
  • Mautino M , KumarS, WaldoJ, JaipuriF, KesharwaniT, ZhangX : WO2012142237 (2012).
  • Huang Q , ZhengM, YangS, KuangC, YuC, YangQ. 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 (11), 5680–5687 (2011).
  • Roöhrig UF , MajjigapuSR, GrosdidierALet al. Rational design of 4-aryl-1, 2, 3-triazoles for indoleamine 2, 3-dioxygenase 1 inhibition. J. Med. Chem.55 (11), 5270–5290 (2012).
  • Combs AP , TakvorianA, ZhuW, SparksRB : WO2007075598 (2007).
  • Yue EW , DoutyB, WaylandBet al. 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 (23), 7364–7367 (2009).
  • Combs A , YueE, SparksRet al. : WO2010005958 (2010).
  • Combs A , GlassB : WO2007095050 (2007).
  • Combs A , GlassB, SparksR, YueEW : WO2008036642 (2008).
  • Combs A , GlassB, SparksR, YueEW : WO2008036653 (2008).
  • Matsuno K , TakaiK, IsakaYet al. S-Benzylisothiourea derivatives as small-molecule inhibitors of indoleamine-2, 3-dioxygenase. Bioorg. Med. Chem. Lett.20 (17), 5126–5129 (2010).
  • Vottero E , BalgiA, WoodsKet al. Inhibitors of human indoleamine 2, 3‐dioxygenase identified with a target‐based screen in yeast. Biotechnol. J.1 (3), 282–288 (2006).
  • Terentis AC , FreewanM, Sempertegui PlazaTS, RafteryMJ, StockerR, ThomasSR. The selenazal drug ebselen potently inhibits indoleamine 2,3-dioxygenase by targeting enzyme cysteine residues. Biochemistry49 (3), 591–600 (2010).
  • Meininger D , ZalamedaL, LiuYet al. Purification and kinetic characterization of human indoleamine 2,3-dioxygenases 1 and 2 (IDO1 and IDO2) and discovery of selective IDO1 inhibitors. Biochim. Biophys. Acta1814 (12), 1947–1954 (2011).
  • Chun XK , YongW, ShuJWet al. : WO2013107164 (2013).
  • Kuehnl S , SchroecksnadelS, TemmlVet al. Lignans from Carthamus tinctorius suppress tryptophan breakdown via indoleamine 2, 3-dioxygenase. Phytomedicine20 (13), 1190–1195 (2013).
  • Temml V , KuehnlS, SchusterD, SchwaigerS, StuppnerH, FuchsD. Interaction of Carthamus tinctorius lignan arctigenin with the binding site of tryptophan-degrading enzyme indoleamine 2, 3-dioxygenase. FEBS Open Bio.3, 450–452 (2013).
  • Liu X , ShinN, KoblishHKet al. Selective inhibition of IDO1 effectively regulates mediators of antitumor immunity. Blood115 (17), 3520–3530 (2010).
  • Koblish HK , HansburyMJ, BowmanKJet al. Hydroxyamidine inhibitors of indoleamine-2,3-dioxygenase potently suppress systemic tryptophan catabolism and the growth of IDO-expressing tumors. Mol. Cancer Ther.9, 489–498 (2010).
  • Reniers J , MeinguetC, MoineauxLet al. Synthesis and inhibition study of monoamine oxidase, indoleamine 2,3-dioxygenase and tryptophan 2,3-dioxygenase by 3,8-substituted 5H-indeno [1,2-c] pyridazin-5-one derivatives. Eur. J. Med. Chem.46 (12), 6104–6111 (2011).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.