Redox and spectroscopic properties of human indoleamine 2,3-dioxygenase and a His303Ala variant: Implications for catalysis

Biochemistry

Volumn 44, Issue 43, 2005, Pages 14318-14328

  Papadopoulou, Nektaria D ^a   Mewies, Martin ^a   McLean, Kirsty J ^a   Seward, Harriet E ^a   Svistunenko, Dimitri A ^b   Munro, Andrew W ^a   Raven, Emma Lloyd ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF ESSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CATALYSIS; CONFORMATIONS; IRON; LIVING SYSTEMS STUDIES; REDOX REACTIONS; SPECTROSCOPIC ANALYSIS;

HEME ENZYMES; INDOLEAMINE 2,3-DIOXYGENASE; OXIDATIVE CLEAVAGE; SUBSTRATE-BINDING;

ENZYMES;

ALANINE; ENZYME VARIANT; FERRIC ION; FERROUS ION; FORMYLKYNURENINE; HEME; HISTIDINE; HYDROXIDE; INDOLEAMINE 2,3 DIOXYGENASE; KYNURENINE; LIGAND; NITROGEN; OXYGEN; RECOMBINANT ENZYME; TRYPTOPHAN; UNCLASSIFIED DRUG;

ABSORPTION SPECTROSCOPY; ALKALINITY; ARTICLE; BINDING ASSAY; CATALYSIS; CATALYST; CHEMICAL INTERACTION; CHEMICAL REACTION; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROCHEMISTRY; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ASSAY; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYME SUBSTRATE; HUMAN; INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PH; PRIORITY JOURNAL; REDUCTION; SITE DIRECTED MUTAGENESIS; STEADY STATE; ULTRAVIOLET SPECTROSCOPY;

ALANINE; BINDING SITES; CATALYSIS; FERRIC COMPOUNDS; FERROUS COMPOUNDS; HEME; HISTIDINE; HUMANS; HYDROGEN-ION CONCENTRATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LIGANDS; OXIDATION-REDUCTION; SPECTROPHOTOMETRY; TEMPERATURE; VARIATION (GENETICS);

MAMMALIA;

EID: 27444436075     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0513958     Document Type: Article

References (67)

1. Sono, M., Roach, M. P., Coulter, E. D., and Dawson, J. H. (1996)-Heme-containing oxygenases, Chem. Rev. 96, 2841-2887.
2. Hayaishi, O, T. O., and Yoshida, R. (1990) Indoleamine 2,3-dioxygenase: Properties and functions of a Superoxide utilizing enzyme, Prog, Inorg. Chem. 38, 75-94.
3. Thomas, S. R., and Stocker, R. (1999) Redox reactions related to indoleamine 2,3-dioxygenase and tryptophan metabolism along the kynurenine pathway, Redox Rep. 4, 199-220.
4. Kerr, S. J., Armati, P. J., Pemberton, L. A., Smythe, G., Tattam, B., and Brew, B. J. (1997) Kynurenine pathway inhibition reduces neurotoxicity of HIV-1-infected macrophages, Neurology 49, 1671-1681.
5. Grohmann, U., Fallarino, F., and Pucceti, P. (2003) Trends Immunol. 24, 242-248.
6. Aquilina, J. A., Carver, J. A., and Truscott, R. J. W. (1997) Exp. Eye Res. 64, 727-735.
7. Munn, D. H., Zhou, M., Attwood, J. T., Bondarev, I., Conway, S. J., Marshall, B., Brown, C., and Mellor, A. L. (1998) Prevention of allogeneic fetal rejection by tryprophan catabolism, Science 281, 1191-1193.
8. Yamamoto, S., and Hayaishi, O. (1967) Tryptophan pyrrolase of rabbit intestine, J. Biol. Chem. 242, 5260-5266.
9. Higuchi, K., and Hayaishi, O. (1967) Enzymic formation of D-kynurenine from D-tryptophan, Arch. Biochem. Biophys. 120, 397-403.
10. Taniguchi, T., Sono, M., Hirata, F., Hayaishi, O., Tamura, M., Hayashi, K., Iizuka, T., and Ishimura, Y. (1979) Indolemine 2,3-dioxygenase-Kinetic studies on the binding of superoxide anion and molecular oxygen to enzyme, J. Biol. Chem. 254, 3288-3294.
11. Sono, M. (1990) Spectroscopic and equilibrium studies of ligand and organic substrate binding to indoleamine 2,3-dioxygenase, Biochemistry 29, 1451-1460.
12. Sono, M. (1986) Spectroscopic and equilibrium properties of the indoleamine 2,3-dioxygenase tryptophan O-2 ternary complex and of analogous enzyme derivatives-Tryptophan binding to ferrous enzyme adducts with dioxygen, nitric oxide, and carbon monoxide, Biochemistry 25, 6089-6097.
13. Sono, M., Tanigushi, T., Watanabe, Y., and Hayaishi, O. (1980) Inoleamine 2,3-dioxygenase-Equilibrium studies of the tryptophan binding to the ferric, ferrous, and CO-bound enzymes, J. Biol. Chem. 255, 1339-1345.
14. 346 are essential for heme binding and catalytic function of human indoleamine 2,3-dioxygenase, J. Biol. Chem. 275, 29525-29531.
15. Littlejohn, T. K., Takikawa O., Skylas, D., Jamie, J. F., Walker, M. J., and Truscott, R. J. W. (2000) Expression and purification of recombinant human indoleamine 2,3-dioxygenase, Protein Expression Purif. 19, 22-29.
16. http://ca.expasy.org/tools/peptide-mass.html.
17. Dai, W., and Gupta, S. L. (1990) Molecular cloning, sequencing, and expression of human interferon-y-inducible indoleamine 2,3-dioxygenase cDNA, Biochem. Biophys. Res. Commun. 168, 1-8.
18. Antonini, M., and Brunori, E. (1971) Hemoglobin and Myoglobin and Their Reactions with Ligands, North-Holland Publishers, Amsterdam, The Netherlands.
19. Takikawa, O., Kuroiwa, T., Yamazaki, F., and Kido, R. (1988) Mechanism of interferon-γ action, J. Biol. Chem. 263, 2041-2048.
20. Shimizu, T., Nomiyama, S., Hirata, F., and Hayaishi, O. (1978) Indoleamine 2,3-dioxygenase-Purification and some properties, J. Biol. Chem. 253, 4700-4706.
21. Patel, N., Jones, D. K., and Raven, E. L. (2000) Investigation of the haem-nicotinate interaction in leghaemoglobin: Role of hydrogen bonding, Eur. J. Biochem. 267, 2581-2587.
22. Aasa, R., and Vanngard, T. (1975) J. Magn. Reson. 19, 308-315.
23. Munro A. W., Noble, M. A., Robledo, L., Daff, S. N., and Chapman, S. K. (2001) Determination of the redox properties of human NADPH-cytochrome P450 reductase, Biochemistry 40, 1956-1963.
24. Dutton, P. L. (1978) Redox potentiometry: Determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems, Methods Enzymol. 54, 411-435.
25. B3, Biochemistry 40, 13421-13429.
26. B3, Biochemistry 36, 13816-13823.
27. Southan M. D., Truscott, R. J. W., Jamie J. F., Pelosi L., Walker M. J., Maeda H., Iwamoto Y., and Tone S. (1996) Structural requirements of the competitive binding site of recombinant human indoleamine 2,3-dioxygenase, Med. Chem. Res. 343-352.
28. Seward, H. E. (1999) Magneto-optical spectroscopy of heme proteins, Ph.D. Thesis, University of East Anglia, Norwich, U.K.
29. Sono, M., and Dawson, J. H. (1984) Extensive studies of the heme coordination structure of indoleamine 2,3-dioxygenase and of tryptophan binding with magnetic and natural circular dichroism and electron paramagnetic resonance spectroscopy, Biochim. Biophys. Acta 789, 170-187.
30. Uchida, K., Shimizu, T., Makino, R., Sakaguchi, K., Iizuka, T., Ishimura, Y., Nozawa, T., and Hatano, M. (1983) Magnetic and natural circular dichroism of L-tryptophan 2,3-tryptophan dioxygenases and indoleamine 2,3-dioxygenase, J. Biol. Chem. 258, 2526-2533.
31. Cheesman, M. R., Greenwood, C, and Thomson, A. J. (1991) Adv. Inorg. Chem. 36, 201-255.
32. McKnight, J., Cheesman, M. R., Thomson, A. J., Miles, J. S., and Munro, A. W. (1993) Identification of charge-transfer transitions in the optical spectrum of low-spin ferric cytochrome P450 Bacillus megaterium, Eur. J. Biochem. 213, 683-687.
33. Gadsby, P. M. A., and Thomson, A. J. (1990) J. Am. Chem. Soc. 112, 5003.
34. 3 from Escherichia coli, J. Bioenerg. Biomembr. 30, 55-62.
35. Terentis, A. C., Thomas, S. R., Takikawa, O., Littlejohn, T. K., Truscott, R. J. W., Armstrong, R. S., Yeh, S., and 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.
36. Patel, N., Seward, H. E., Svensson, A., Gurman, S. J., Thomson, A. J., and Raven, E. L. (2003) Arch. Biochem. Biophys. 418, 197-204.
37. Eglinton, D. G., Gadsby, P. M. A., Sievers, G., Peterson, J., and Thomson, A. J. (1983) A comparative study of the low-temperature magnetic circular dichroism spectra of horse heart metmyoglobin and bovine liver catalase derivatives, Biochim. Biophys. Acta 742, 648-658.
38. Foote, N., Gadsby, P. M. A., Berry, M. J., Greenwood, C., and Thomson, A. J. (1987) Biochem. J. 246, 659-668.
39. Kobayashi, N., Nozawa, T., and Hatano, M. (1977) Magnetic circular dichroism studies on acid and alkaline forms of horseradish peroxidase, Biochim. Biophys. Acta 493, 340-351.
40. Bolard, J., and Gamier, A. (1972) Biochim. Biophys. Acta 263, 535-549.
41. Springall, J., Stillman, M. J., and Thomson, A. J. (1976) Biochim. Biophys. Acta 453, 494-501.
42. Nozawa, T., Kobayashi, N., and Hatano, M. (1976) Biochim. Biophys. Acta 427, 652-662.
43. Palmer, G. (1985) The electron paramagnetic resonance of metalloproteins, Biochem. Soc. Trans. 13, 548-560.
44. More, C, Belle, V., Asso, M., Fournel, A., Roger, G., Guigliarelli, B., and Bertrand, P. (1999) EPR spectroscopy: A powerful technique for the structural and functional investigation of metalloproteins, Biospectroscopy 5, S3-S18.
45. Yonetani, T., and Anni, H. (1987) Yeast cytochrome c peroxidase. Coordination and spin states of heme prosthetic group, J. Biol. Chem. 262, 9547-9554.
46. Suzuki, T., Kawamichi, H., and Imai, K. (1998) A myoglobin evolved from indoleamine 2,3-dioxygenase, a tryptophan-degrading enzyme, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 121, 117-128.
47. Newmyer, S. L., and Ortiz de Montellano, P. R. (1996) Rescue of the catalytic activity of an H42A mutant of horseradish peroxidase by exogenous imidazoles, J. Biol. Chem. 271, 14891-14896.
48. Yamazaki, F., Kuroiwa, T., Takikawa, O., and Kido, R. (1985) Human indoleamine 2,3-dioxygenase, Biochem. J. 230, 635-638.
49. Aitken, J. B., Thomas, S. E., Stocker, R., Thomas, S. R., Takikawa, O., Armstrong, R. S., and Lay, P. A. (2004) Determination of the nature of the heme environment in nitrosyl indoleamine 2,3-dioxygenase using mutiple-scattering analyses of X-ray absorption fime structure, Biochemistry 43, 4892-4898.
50. Jones, D. K., Patel, N. P., Cheesman, M. R., Thomson, A. J., and Raven, E. L. (2002) Leghaemoglobin: A model for the investigation of haem protein axial ligation, Inorg. Chim. Acta 331, 303-309.
51. Rosell, F. I., Ferrer, J. C., and Mauk, A. G. (1998) Proton-linked protein conformation swithcing: Definition of the alkaline conformation transition of yeast iso-1-ferricytochrome c, J. Am. Chem. Soc. 120, 11234-11245.
52. Makino, R., Sakaguchi, K., Iizuka, T., and Ishimura, Y. (1980) Acid-alkaline transition and thermal spin equilibirum of the heme in ferric L-tryptophan 2,3-dioxygenase, J. Biol. Chem. 255, 11883-11891.
53. Jones, D. K., Badii, R., Rosell, F. I., and Lloyd, E. (1998) Bacterial expression and spectroscopic characterization of soybean leghaemoglobin a, Biochem. J. 330, 983-988.
54. Foshay, M. C., Vitello, L. B., and Erman, J. E. (2004) pH dependence of heme iron coordination, hydrogen peroxide reactivity, and cyanide binding in cytochrome c peroxidase (H52K), Biochemistry 43, 5065-5072.
55. Turano, P., Ferrer, J. C., Cheesman, M. R., Thomson, A. J., Banci, L., Bertini, I., and Mauk, A. G. (1995) pH, electrolyte, and substrate-linked variations in active site structure of the Trp51Ala variant of cytochrome c peroxidase, Biochemistry 34, 13895-13905.
56. Raven, E. L., and Mauk, A. G. (2001) Chemical reactivity of the active site of myoglobin, Adv. Inorg. Chem. 51, 1-49.
57. Conroy, C. W., Tyma, P., Daum, P. H., and Erman, J. E. (1978) Oxidation-reduction potential measurements of cytochrome c peroxidase and pH dependent spectral transitions in the ferrous enzyme, Biochim. Biophys. Acta 537, 62-69.
58. Goodin, D. B., and McRee, D. E. (1993) The Asp-His-Fe triad of cytochrome c peroxidase controls the reduction potential, electronic structure, and coupling of the tryptophan free radical to the heme, Biochemistry 32, 3313-3324.
59. Harbury, H. A. (1957) Oxidation-reduction potentials of horseradish peroxidase, J. Biol. Chem. 225, 1009-1024.
60. Millis, C. D., Cai, D., Stankovich, M. T., and Tien, M. (1989) Oxidation-reduction potentials and ionization states of extracellular peroxidases from the lignin-degrading fungus Phanerochaete crysoporium, Biochemistry 28, 8484-8489.
61. Jones, D. K., Dalton, D. A., Rosell, F. I., and Raven, E. L. (1998) Class I heme peroxidases: Characterisation of soybean ascorbate peroxidase, Arch. Biochem. Biophys. 360, 173-178.
62. Tanaka, M., Ishimori, K., and Morishima, I. (1998) Structural roles of the highly conserved Glu residue in the heme distal site of peroxidases, Biochemistry 37, 2629-2638.
63. Yamada, H., Makino, R., and Yamazaki, I. (1975) Effrects of 2,4-substituents of deuteroheme upon redox potentials of horseradish peroxidases, Arch. Biochem. Biophys. 169, 344-353.
64. Sugar, S. G. (1976) Coupling of spin, substrate, and redox equilibria in cytochrome P450, Biochemistry 15, 5399-5406.
65. IV) forms of heme o, Eur. J. Biochem. 219, 595-602.
66. Yagil, G. (1967) The proton dissociation constant of pyrrole, indole, and related compounds, Tetrahedron 23, 2855-2861.
67. Andonovski, B. S. (1999) UV study of the protonation of indole-2-carboxylic acid, 3-methylindole, 3-acetylindole, and D-tryptophan in perchloric acid solutions, Croat. Chem. Acta 72, 711-726.