Biochemical characteristics and inhibitor selectivity of mouse indoleamine 2,3-dioxygenase-2

Amino Acids

Volumn 39, Issue 2, 2010, Pages 565-578

  Austin, Christopher Jonathan Daraius ^a   Mailu, B M ^b   Maghzal, G J ^a   Sanchez Perez, A ^a   Rahlfs, S ^b   Zocher, K ^b   Yuasa, H J ^c   Arthur, J W ^a   Becker, K ^b   Stocker, R ^a   Hunt, N H ^a   Ball, H J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c Kochi University   (Japan)

Author keywords

Cytochrome b5; Electron donation; IDO2; Oxidation reduction

Indexed keywords

1 METHYL DEXTRO TRYPTOPHAN; CYTOCHROME B5; INDOLEAMINE 2,3 DIOXYGENASE; INDOLEAMINE 2,3 DIOXYGENASE 1; INDOLEAMINE 2,3 DIOXYGENASE 2; INDOLEAMINE 2,3 DIOXYGENASE INHIBITOR; UNCLASSIFIED DRUG; NITRIC OXIDE; RECOMBINANT PROTEIN; TRYPTOPHAN; TRYPTOPHAN METHYL ESTER;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME KINETICS; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; THERMOSTABILITY; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; ENZYME STABILITY; HUMAN; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; ENZYME STABILITY; HUMANS; HYDROGEN-ION CONCENTRATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KINETICS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NITRIC OXIDE; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TRYPTOPHAN;

MAMMALIA;

EID: 84755160743     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-010-0475-9     Document Type: Article

References (57)

1. Austin CJD, Mizdrak J, Matin A, Sirijovski N, Kosim-Satyaputra P, Willows RD, Roberts TH, Truscott RJW, Polekhina G, Parker MW, Jamie JF (2004) Optimised expression and purification of recombinant human indoleamine 2, 3-dioxygenase. Protein Expr Purif 37:392-398. doi:10.1016/j.pep. 2004.06.025
2. Austin CJ, Astelbauer F, Kosim-Satyaputra P, Ball HJ, Willows RD, Jamie JF, Hunt NH (2009) Mouse and human indoleamine 2, 3-dioxygenase display some distinct biochemical and structural properties. Amino Acids 36:99-106. doi:10.1007/s00726-008-0037-6
3. Ball HJ, Sanchez-Perez A, Weiser S, Austin CJD, Astelbauer F, Miu J, McQuillan JA, Stocker R, Jermiin LS, Hunt NH (2007) Characterization of an indoleamine 2, 3-dioxygenase-like protein found in humans and mice. Gene 396:203-213
4. Ball HJ, Yuasa HJ, Austin CJ, Weiser S, Hunt NH (2009) Indoleamine 2, 3-dioxygenase-2; a new enzyme in the kynurenine pathway. Int J Biochem Cell Biol. doi: 10.1016/j.biocel.2008.01.005
5. Beadle GW, Mitchell HK, Nyc JF (1947) Kynurenine as an intermediate in the formation of nicotinic acid from tryptophane by neurospora. Proc Natl Acad Sci USA 33:155-158. doi: 10.1073/pnas.33.6.155
6. Calalb MB, Polte TR, Hanks SK (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 15:954-963
7. Chen R, Li L, Weng Z (2003) ZDOCK: an initial-stage proteindocking algorithm. Proteins 52:80-87
8. Comeau SR, Gatchell DW, Vajda S, Camacho CJ (2004) ClusPro: a fully automated algorithm for protein-protein docking. Nucleic Acids Res 32: W96-W99
9. Danesch U, Hashimoto S, Renkawitz R, Schutz G (1983) Transcriptional regulation of the tryptophan oxygenase gene in rat liver by glucocorticoids. J Biol Chem 258:4750-4753
10. Danesch U, Gloss B, Schmid W, Schutz G, Schule R, Renkawitz R (1987) Glucocorticoid induction of the rat tryptophan oxygenase gene is mediated by two widely separated glucocorticoid responsive elements. EMBO J 6:625-630
11. Delcarte J, Fauconnier M, Jacques P, Matsui K, Thonart P, Marlier M (2003) Optimisation of expression and immobilized metal ion affinity chromatographic purification of recombinant (His) 6-tagged cytochrome P450 hydroperoxide lyase in Escherichia coli. J Chromatogr B Anal Technol Biomed Life Sci 786:229-236. doi:10.1016/S1570-0232 (02) 00815-2
12. Fallarino I, Grohmann U, Vacca C, Bianchi R, Orabona C, Spreca A, Fioretti MC, Puccetti P (2002) T cell apoptosis by tryptophan catabolism. Cell Death Differ 9:1069-1077. doi:10.1038/sj.cdd.4401073
13. Feis A, Marzocchi MP, Paoli M, Smulevich G (1994) Spin state and axial ligand bonding in the hydroxide complexes of metmyoglobin, methemoglobin, and horseradish peroxidase at room and low temperatures. Biochemistry 33:4577-4583. doi:10.1021/bi00181a019
14. Frey AB, Monu N (2008) Signaling defects in anti-tumor T cells. Immunol Rev 222:192-205. doi:10.1111/j.1600-065X.2008. 00606.x
15. Haber R, Bessette D, Hulihangiblin B, Durcan MJ, Goldman D (1993) Identification of tryptophan 2, 3-dioxygenase RNA in rodent brain. J Neurochem 60:1159-1162. doi:10.1111/j.1471-4159. 1993.tb03269.x
16. Hansen AM, Driussi C, Turner V, Takikawa O, Hunt NH (2000) Tissue distribution of indoleamine 2, 3-dioxygenase in normal and malaria-infected tissue. Redox Rep 5:112-115. doi:10.1179/135100000101535384
17. Hansen AM, Ball HJ, Mitchell AJ, Miu J, Takikawa O, Hunt NH (2004) Increased expression of indoleamine 2, 3-dioxygenase in murine malaria infection is predominantly localised to the vascular endothelium. Int J Parasitol 34:1309-1319. doi: 10.1016/j.ijpara.2004.07.008 (Pubitemid 39469988)
18. Harrison RG, Weiner JS (1949) Vascular patterns of the mammalian testis and their functional significance. J Exp Biol 26:304-316
19. Heyes MP, Morrison PF (1997) Quantification of local de novo synthesis versus blood contributions to quinolinic acid concentrations in brain and systemic tissues. J Neurochem 68:280-288. doi:10.1046/j.1471-4159.1997.68010280. x
20. Heyes MP, Brew BJ, Saito K, Quearry BJ, Price RW, Lee K, Bhalla RB, der M, Markey SP (1992a) Interrelationships between quinolinic acid, neuroactive kynurenines, neopterin and beta-2-microglobulin in cerebrospinal-fluid and serum of HIV-1-infected patients. J Neuroimmunol 40:71-80. doi:10.1016/0165-5728 (92) 90214-6
21. Heyes MP, Saito K, Crowley JS, Davis LE, Demitrack MA, der M, Dilling LA, Elia J, Kruesi MJP, Lackner A, Larsen SA, Lee K, Leonard HL, Markey SP, Martin A, Milstein S, Mouradian MM, Pranzatelli MR, Quearry BJ, Salazar A, Smith M, Strauss SE, Sunderland T, Swedo SW, Tourtellotte WW (1992b) Quinolinic acid and kynurenine pathway metabolism in inflammatory and noninflammatory neurological disease. Brain 115:1249-1273
22. Honig A, Rieger L, Kapp M, Sutterlin M, Dietl J, Kammerer U (2004) Indoleamine 2, 3-dioxygenase (IDO) expression in invasive extravillous trophoblast supports role of the enzyme for materno-fetal tolerance. J Reprod Immunol 61:79-86. doi: 10.1016/j.jri.2003.11.002 (Pubitemid 38446981)
23. Hou DY, Muller AJ, Sharma MD, DuHadaway J, Banerjee T, Johnson M, Mellor AL, Prendergasts GC, Munn DH (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. doi:10.1158/0008-5472. CAN-06-2925
24. Hunt NH, Golenser J, Chan-Ling T, Parekh S, Rae C, Potter S, Medana IM, Miu J, Ball HJ (2006) Immunopathogenesis of cerebral malaria. Int J Parasitol 36:569-582. doi:10.1016/j.ijpara.2006.02.016 (Pubitemid 43674512)
25. Kehoe JW, Bertozzi CR (2000) Tyrosine sulfation: a modulator of extracellular protein-protein interactions. Chem Biol 7:57-61. doi:10.1016/S1074-5521 (00) 00093-4
26. Kim YH, Berry AH, Spencer DS, Stites WE (2001) Comparing the effect on protein stability of methionine oxidation versus mutagenesis: steps toward engineering oxidative resistance in proteins. Protein Eng 14:343-347. doi:10.1093/protein/14.5.343
27. Knox WE (1966) The regulation of tryptophan pyrrolase activity by tryptophan. Adv Enzyme Regul 4:287-297
28. Kuma F (1981) Properties of methemoglobin reductase and kinetic study of methemoglobin reduction. J Biol Chem 256:5518-5523
29. Kurokawa H, Lee DS, Watanabe M, Sagami I, Mikami B, Raman CS, Shimizu T (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. J Biol Chem 279:20186-20193. doi:10.1074/jbc. M314199200
30. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227:680-685. doi: 10.1038/227680a0
31. Lyskov S, Gray JJ (2008) The RosettaDock server for local proteinprotein docking. Nucleic Acids Res 36: W233-W238
32. Maghzal GJ, Thomas SR, Hunt NH, Stocker R (2008) Cytochrome b5, not superoxide anion radical, is a major reductant of indoleamine 2, 3-dioxygenase in human cells. J Biol Chem 283:12014-12025. doi:10.1074/jbc. M710266200
33. Metz R, DuHadaway JB, Kamasani U, Laury-Kleintop L, Muller AJ, Prendergast GC (2007) Novel tryptophan catabolic enzyme IDO2 is the preferred biochemical target of the antitumor indoleamine 2, 3-dioxygenase inhibitory compound D-1-methyltryptophan. Cancer Res 67:7082-7087. doi:10.1158/0008-5472. CAN-07-1872
34. Novak N (2006) Targeting dendritic cells in allergen immunotherapy. Immunol Allergy Clin N Am 26:307-319. doi:10.1016/j.iac. 2006.02.010
35. Peitsch MC (1995) Protein modeling by e-mail (vol 13, pg 658, 1995). Biotechnology 13:723. doi:10.1038/nbt0895-723
36. Peterson AC, Migawa MT, Martin MM, Hamaker LK, Czerwinski KC, Zhang W, Arend RA, Fisette PL, Ozaki Y, Will JA, Brown RR, Cook JM (1994) Evaluation of functionalized tryptophan derivatives and related compounds as competitive inhibitors of indoleamine 2, 3-dioxygenase. Med Chem Res 4:531-544
37. Pfefferkorn ER, Eckel M, Rebhun S (1986) Interferon-gamma suppresses the growth of Toxoplasma gondii in human fibroblasts through starvation of tryptophan. Mol Biochem Parasitol 20:215-224. doi:10.1016/0166-6851 (86) 90101-5
38. Schenkman JB, Jansson I (2003) The many roles of cytochrome b5. Pharmacol Ther 97:139-152. doi:10.1016/S0163-7258 (02) 00327-3
39. Shimizu T, Nomiyama S, Hirata F, Hayaishi O (1978) Indoleamine 2, 3-dioxygenase-purification and some properties. J Biol Chem 253:4700-4706
40. Silbernagl S (1988) The renal handling of amino acids and oligopeptides. Physiol Rev 68:911-1007
41. Sono M (1989) The roles of superoxide anion and methylene-blue in the reductive activation of indoleamine 2, 3-dioxygenase by ascorbic-acid or by xanthine oxidase-hypoxanthine. J Biol Chem 264:1616-1622
42. Southan MD, Truscott RJW, Jamie JF, Pelosi L, Walker MJ, Maeda H, Iwamoto Y, Tone S (1996) Structural requirements of the competitive binding site of recombinant human indoleamine 2, 3-dioxygenase. Med Chem Res 6:343-352
43. Stone TW, Mackay GM, Forrest CM, Clark CJ, Darlington LG (2003) Tryptophan metabolites and brain disorders. Clin Chem Lab Med 41:852-859. doi:10.1515/CCLM.2003.129 (Pubitemid 37010175)
44. Sugimoto H, Oda S, Otsuki T, Hino T, Yoshida T, Shiro Y (2006) Crystal structure of human indoleamine 2, 3-dioxygenase: catalytic mechanism of O-2 incorporation by a heme-containing dioxygenase. Proc Natl Acad Sci USA 103:2611-2616. doi: 10.1073/pnas.0508996103
45. Suzuki T, Kawamichi H, Imai K (1998) A myoglobin evolved from indoleamine 2, 3-dioxygenase, a tryptophan-degrading enzyme. Comp Biochem Physiol B Biochem Mol Biol 121:117-128. doi: 10.1016/S0305-0491 (98) 10086-X
46. Suzuki S, Tone S, Takikawa O, Kubo T, Kohno I, Minatogawa Y (2001) Expression of indoleamine 2, 3-dioxygenase and tryptophan 2, 3-dioxygenase in early concepti. Biochem J 355:425-429. doi:10.1042/0264-6021:3550425 (Pubitemid 32397802)
47. 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 interferongamma and evaluation of the enzyme-mediated tryptophan degradation in its anticellular activity. J Biol Chem 263:2041-2048
48. Tankiewicz A, Pawlak D, Topczewska-Bruns J, Buczko W (2003) Kidney and liver kynurenine pathway enzymes in chronic renal failure. Adv Exp Med Biol 527:409-414 (Pubitemid 38197669)
49. Terentis AC, Thomas SR, Takikawa O, Littlejohn TK, Truscott RJW, Armstrong RS, Yeh SR, Stocker R (2002) The heme environment of recombinant human indoleamine 2, 3-dioxygenase-structural properties and substrate-ligand interactions. J Biol Chem 277:15788-15794. doi:10.1074/jbc. M200457200
50. Thomas SR, Stocker R (1999) Redox reactions related to indoleamine 2, 3-dioxygenase and tryptophan metabolism along the kynurenine pathway. Redox Rep 4:199-220. doi:10.1179/135100099 101534927
51. Thomas SR, Terentis AC, Cai H, Takikawa O, Levina A, Lay PA, Freewan M, Stocker R (2007) Post-translational regulation of human indoleamine 2, 3-dioxygenase activity by nitric oxide. J Biol Chem 282:23778-23787. doi:10.1074/jbc. M700669200
52. Unneberg P, Merelo JJ, Chacon P, Moran F (2001) SOMCD: method for evaluating protein secondary structure from UV circular dichroism spectra. Proteins Struct Funct Genet 42:460-470. doi: 10.1002/1097-0134 (20010301) 42:4<460:AID-PROT50>3.0. CO;2-U
53. van Gunsteren WF, Billeter SR, Eising A, Hünenberger PH, Krüger P, Mark AE, Scott WRP, Tironi IG (1996) Biomolecular simulations: the GROMOS96 manual and user guide. VdF Hochschulverlag ETHZ, Zürich
54. Vottero E, Mitchell DA, Page MJ, MacGillivray RTA, Sadowski IJ, Roberge M, Mauk AG (2006) Cytochrome b5 is a major reductant in vivo of human indoleamine 2, 3-dioxygenase expressed in yeast. Febs Lett 580:2265-2268. doi:10.1016/j.febslet.2006.03.034
55. Williams CA, Harry RA, McLeod JD (2007) Apoptotic cells induce dendritic cell-mediated suppression via interferon-gammainduced IDO. Immunology. doi:10.1111/j.1365-2567.2007. 02743.x
56. World Health Organization (1999) WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, 4th edn. Published on behalf of the World Health Organization by Cambridge University Press, Cambridge, UK, 128 p
57. Yuasa HJ, Takubo M, Takahashi A, Hasegawa T, Noma H, Suzuki T (2007) Evolution of vertebrate indoleamine 2, 3-dioxygenases. J Mol Evol 65:705-714. doi:10.1007/s00239-007-9049-1