O2- and α-ketoglutarate-dependent tyrosyl radical formation in TauD, an α-keto acid-dependent non-heme iron dioxygenase

Biochemistry

Volumn 42, Issue 7, 2003, Pages 1854-1862

  Ryle, Matthew J ^a,b   Liu, Aimin ^c,d   Muthukumaran, Rajendra Bose ^e   Ho, Raymond Y N ^c   Koehntop, Kevin D ^c   McCracken, John ^e   Que Jr , Lawrence ^c   Hausinger, Robert P ^a,b  

^a Michigan State University ^*  (United States)

^b Michigan State University   (United States)

^c University of Minnesota   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOPHORES; DECOMPOSITION; HYDROXYLATION; IRON COMPOUNDS; MUTAGENESIS; RATE CONSTANTS; SOLVENTS;

OXIDATIVE DECARBOXYLATION;

ENZYMES;

2 OXOACID; 2 OXOGLUTARIC ACID; FERRIC HYDROXIDE; FERRIC ION; HEME OXYGENASE; TAURINE; TYROSINE; ALPHA-KETOGLUTARIC ACID; ENZYME INHIBITOR; FERROUS ION; FREE RADICAL; IRON; ISOLEUCINE; MIXED FUNCTION OXIDASE; OXYGEN; OXYGENASE; RECOMBINANT PROTEIN; SERINE; TAURINE ALPHA KETOGLUTARATE DIOXYGENASE; TAURINE-ALPHA-KETOGLUTARATE DIOXYGENASE; TYROSINE RADICAL;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CHROMATOPHORE; DECARBOXYLATION; HYDROXYLATION; PRIORITY JOURNAL; RADICAL REACTION; CHEMISTRY; COMPARATIVE STUDY; DRUG ANTAGONISM; ELECTRON SPIN RESONANCE; GENETICS; RAMAN SPECTROMETRY; SITE DIRECTED MUTAGENESIS; SPECTROPHOTOMETRY; TIME;

AMINO ACID SUBSTITUTION; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME INHIBITORS; FERROUS COMPOUNDS; FREE RADICALS; IRON; ISOLEUCINE; KETOGLUTARIC ACIDS; MIXED FUNCTION OXYGENASES; MUTAGENESIS, SITE-DIRECTED; OXYGEN; OXYGENASES; RECOMBINANT PROTEINS; SERINE; SPECTROPHOTOMETRY; SPECTRUM ANALYSIS, RAMAN; TIME FACTORS; TYROSINE;

EID: 0037465344     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi026832m     Document Type: Article

References (42)

1. Prescott, A. G., and Lloyd, M. D. (2000) The iron(II) and 2-oxoacid-dependent dioxygenases and their role in metabolism, Nat. Prod. Rep. 17, 367-383.
2. Schofield, C. J., and Zhang, Z. (1999) Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes, Curr. Opin. Struct. Biol. 9, 722-731.
3. Ryle, M. J., and Hausinger, R. P. (2002) Non-heme iron oxygenases, Curr. Opin. Chem. Biol. 6, 193-201.
4. Zhang, Z., Ren, J., Stammers, D. K., Baldwin, J. E., Harlos, K., and Schofield, C. J. (2000) Structural origins of the selectivity of the trifunctional oxygenase clavaminic acid synthase, Nat. Struct. Biol. 7, 127-133.
5. Prescott, A. G., and John, P. (1996) Dioxygenases: molecular structure and role in plant metabolism, Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 245-271.
6. Hanauske-Abel, H. M., and Gunzler, V. (1982) A stereochemical concept for the catalytic mechanism of prolylhydroxylase. Applicability to classification and design of inhibitors, J. Theor. Biol. 94, 421-455.
7. Que, L., Jr., and Ho, R. Y. N. (1996) Dioxygen activation by enzymes with mononuclear non-heme iron active site, Chem. Rev. 96, 2607-2624.
8. Solomon, E. I., Brunold, T. C., Davis, M. I., Kemsley, J. N., Lee, S.-K., Lehnert, N., Neese, F., Skulan, A. J., Yang, Y.-S., and Zhou, J. (2000) Geometric and electronic structure/function correlations in non-heme iron enzymes, Chem. Rev. 100, 235-349.
9. Eichhorn, E., van der Ploeg, J. R., Kertesz, M. A., and Leisinger, T. (1997) Characterization of α-ketoglutarate-dependent taurine dioxygenase from Escherichia coli, J. Biol. Chem. 272, 23031-23036.
10. Elkins, J. M., Ryle, M. J., Clifton, I. J., Dunning Hotopp, J. C., Lloyd, J. S., Burzlaff, N. I., Baldwin, J. E., Hausinger, R. P., and Roach, P. L. (2002) X-ray crystal structure of Escherichia coli taurine/α-ketoglutarate dioxygenase complexed to ferrous iron and substrates, Biochemistry 41, 5185-5192.
11. Hogan, D. A., Smith, S. R., Saari, E. A., McCracken, J., and Hausinger, R. P. (2000) Site-directed mutagenesis of 2,4-dichlorophenoxyacetic acid/α-ketoglutarate dioxygenase. Identification of residues involved in metallocenter formation and substrate binding, J. Biol. Chem. 275, 12400-12409.
12. Valegård, K., Terwisscha van Scheltinga, A. C., Lloyd, M. D., Hara, T., Ramaswamy, S., Perrakis, A., Thompson, A., Lee, W.-J., Baldwin, J. E., Schofield, C. J., Hajdu, J., and Andersson, I. (1998) Structure of a cephalosporin synthase, Nature (London) 394, 805-809.
13. Ryle, M. J., Padmakumar, R., and Hausinger, R. P. (1999) Stopped-flow kinetic analysis of Escherichia coli taurine/α-ketoglutarate dioxygenase: interactions with α-ketoglutarate, taurine, and oxygen, Biochemistry 38, 15278-15286.
14. Ho, R. Y. N., Mehn, M. P., Hegg, E. L., Liu, A., Ryle, M. A., Hausinger, R. P., and Que, L., Jr. (2001) Resonance Raman studies of the iron(II)-α-keto acid chromophore in model and enzyme complexes, J. Am. Chem. Soc. 123, 5022-5029.
15. Pavel, E. G., Zhou, J., Busby, R. W., Gunsior, M., Townsend, C. A., and Solomon, E. I. (1998) Circular dichroism and magnetic circular dichroism spectroscopic studies of the non-heme ferrous active site in clavaminate synthase and its interaction with α-ketoglutarate cosubstrate, J. Am. Chem. Soc. 120, 743-753.
16. Wilmouth, R. C., Turnbull, J. J., Welford, R. W. D., Clifton, I. J., and Schofield, C. J. (2002) Structure and mechanism of anthocyanadin synthase from Arabidopsis thaliana, Structure 10, 93-103.
17. Zhou, J., Gunsior, M., Bachmann, B. O., Townsend, C. A., and Solomon, E. I. (1998) Substrate binding to the α-ketoglutarate-dependent non-heme iron enzyme clavaminate synthase 2: coupling mechanism of oxidative decarboxylation and hydroxylation, J. Am. Chem. Soc. 120, 13539-13540.
18. Zhou, J., Kelly, W. L., Bachmann, B. O., Gunsior, M., Townsend, C. A., and Solomon, E. I. (2001) Spectroscopic studies of substrate interactions with clavaminate synthase 2, a multifunctional α-KG-dependent non-heme iron enzyme: correlation with mechanisms and reactivities, J. Am. Chem. Soc. 123, 7388-7398.
19. Saari, R. E., and Hausinger, R. P. (1998) Ascorbic acid-dependent turnover and reactivation of 2,4-dichlorophenoxyacetic acid/α-ketoglutarate dioxygenase using thiophenoxyacetic acid, Biochemistry 37, 3035-3042.
20. Liu, A., Ho, R. Y. N., Que, L., Jr., Ryle, M. J., Phinney, B. S., and Hausinger, R. P. (2001) Alternative reactivity of an α-ketoglutarate-dependent iron(II) oxygenase: enzyme self-hydroxylation, J. Am. Chem. Soc. 123, 5126-5127.
21. Andersson, K. K., Cox, D. D., Que, L., Jr., Flatmark, T., and Haavik, J. (1988) Resonance Raman studies on the blue-green-colored bovine adrenal tyrosine 3-monooxygenase (tyrosine hydroxylase). Evidence that the feedback inhibitors adrenaline and noradrenaline are coordinated to iron, J. Biol. Chem. 263, 18621-18626.
22. Michaud-Soret, I., Andersson, K. K., Que, L., Jr., and Haavik, J. (1995) Resonance Raman studies of catecholate and phenolate complexes of recombinant human tyrosine hydroxylase, Biochemistry 34, 5504-5510.
23. Ling, J., Sahlin, M., Sjöberg, B.-M., Loehr, T. M., and Sanders-Loehr, J. (1994) Dioxygen is the source of the μ-oxo bridge in iron ribonucleotide reductase, J. Biol. Chem. 269, 5595-5601.
24. Smith, J. J., Thomson, A. J., Proudfoot, A. E. I., and Wells, T. N. C. (1997) Identification of an Fe(III)-dihydroxyphenylalanine site in recombinant phosphomannose isomerase from Candida albicans, Eur. J. Biochem. 244, 325-333.
25. Siu, D. C.-T., Orville, A. M., Lipscomb, J. D., Ohlendorf, D. H., and Que, L., Jr. (1992) Resonance Raman studies of the protocatechuate 3,4-dioxygenase from Brevibacterium fuscum, Biochemistry 31, 10443-10448.
26. Gaber, B. P., Sheridan, J. P., Bazer, F. W., and Roberts, R. M. (1979) Resonance Raman scattering from uteroferrin, the purple glycoprotein of the porcine uterus, J. Biol. Chem. 254, 8340-8342.
27. Stubbe, J., and Van der Donk, W. A. (1998) Protein radicals in enzyme catalysis, Chem. Rev. 98, 705-762.
28. Pesavento, R. P., and van der Donk, W. A. (2001) Tyrosyl radical cofactors, Adv. Protein Chem. 58, 317-385.
29. Shi, W., Hoganson, C. W., Espe, M., Bender, C. J., Babcock, G. T., Palmer, G., Kulmacz, R. J., and Tsai, A.-I. (2000) Electron paramagnetic resonance and electron nuclear double resonance spectroscopic identification and characterization of the tyrosyl radicals in prostaglandin H synthase I. Biochemistry 39, 4112-4121.
30. Liu, A., Pötsch, S., Davydov, A., Barra, A.-L., Rubin, H., and Gräslund, A. (1998) The tyrosyl free radical of recombinant ribonucleotide reductase from Mycobacterium tuberculosis is located in a rigid hydrophobic pocket. Biochemistry 37, 16369-16377.
31. Evelo, R. G., Styring, S., Rutherford, A. W., and Hoff, A. J. (1989) EPR relaxation measurements of photosystem II. Influence of S-state oxidation and temperature, Biochim. Biophys. Acta 973. 428-442.
32. Zounl, A., Witt, H.-T., Kern, J., Fromme, P., Krauss, N., Saenger, W., and Orth, P. (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution, Nature 409. 739-743.
33. Dunning Hotopp, J. C., and Hausinger, R. P. (2002) Probing the 2,4-dichlorophenoxyacetate/α-ketoglutarate dioxygenase substrate binding site by site-directed mutagenesis and mechanism-based inactivation, Biochemistry 41, 9787-9794.
34. Ormö, M., deMaré, F., Regnström, K., Aberg, A., Sahlin, M., Ling, J., Loehr, T. M., Sanders-Loehr, J., and Sjöberg, B.-M. (1992) Engineering of the iron site in ribonucleotide reductase to a self-hydroxylating monooxygenase, J. Biol. Chem. 267, 8711-8714.
35. Sono, M., Roach, M. P., Coulter, E. D., and Dawson, J. H. (1996) Heme-containing oxygenases, Chem. Rev. 96, 2841-2887.
36. Wallar, B. J., and Lipscomb, J. D. (1996) Dioxygen activation by enzymes containing binuclear non-heme iron clusters, Chem. Rev. 96, 2625-2657.
37. Counts, D. F., Cardinale, G. J., and Udenfriend, S. (1978) Prolyl hydroxylase half reaction: peptidyl prolyl-independent decarboxylation of α-ketoglutarate. Proc. Natl. Acad. Sci. U.S.A. 75, 2145-2149.
38. n stimulates α-ketoglutarate decarboxylation without prolyl hydroxylase, J. Biol. Chem. 253, 6327-6330.
39. Holme, E., and Lindstedt, S. (1982) Studies on the partial reaction of thymine 7-hydroxylase in the presence of 5-fluorouracil, Biochim. Biophys. Acta 704, 278-283.
40. Myllylä, R., Majamaa, K., Günzler, V., Hanauske-Abel, H. N., and Kivirikko, K. I. (1984) Ascorbate is consumed stoichiometrically in the uncoupled reactions catalyzed by prolyl 4-hydroxylase and lysyl hydroxylase, J. Biol. Chem. 259, 5403-5405.
41. Zhang, Z., Barlow, J. N., Baldwin, J. E., and Schofield, C. J. (1997) Metal-catalyzed oxidation and mutagenesis studies on the iron(II) binding site of 1-aminocyclopropane-1-carboxylate oxidase, Biochemistry 36, 15999-16007.
42. Logan, D. T., deMaré, F., Persson, B. O., Slaby, A., Sjöberg, B.-M., and Nordlund, P. (1998) Crystal structures of two self-hydroxylating ribonucleotide reductase protein R2 mutants: structural basis for the oxygen-insertion step of hydroxylation reactions catalyzed by diiron proteins, Biochemistry 37, 10798-10807.