Steady-state and transient kinetic analyses of taurine/α- ketoglutarate dioxygenase: Effects of Oxygen concentration, alternative sulfonates, and active-site variants on the FeIV-oxo intermediate

Biochemistry

Volumn 44, Issue 10, 2005, Pages 3845-3855

  Grzyska, Piotr K ^a   Ryle, Matthew J ^a,c   Monterosso, Greta R ^a   Liu, Jian ^a   Ballou, David P ^b   Hausinger, Robert P ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c IDEXX LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGON; CARBOXYLATION; CHEMICAL BONDS; CRYSTAL STRUCTURE; HYDROPHOBICITY; KINETIC THEORY; PROTONS; REACTION KINETICS; SPECTROSCOPIC ANALYSIS;

AMINOACETALDEHYDE; OXIDATIVE DECARBOXYLATION; SULFITES; TRANSIENT KINETICS;

ENZYMES;

2 OXOGLUTARIC ACID; 3 N MORPHOLINOPROPANESULFONIC ACID; ALPHA KETOGLUTARATE DIOXYGENASE; HEMOPROTEIN; IRON; OXYGENASE; PENTANESULFONIC ACID; PROTON; SULFONIC ACID DERIVATIVE; TAU PROTEIN; TAURINE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHELATION; DECARBOXYLATION; ENZYME KINETICS; HYDROPHOBICITY; HYDROXYLATION; OXYGEN CONCENTRATION; PRIORITY JOURNAL; PROTEIN BINDING; STEADY STATE; ULTRAVIOLET SPECTROSCOPY; WILD TYPE;

ALKANESULFONATES; BINDING SITES; CATALYSIS; ELECTRON TRANSPORT COMPLEX IV; ESCHERICHIA COLI PROTEINS; FERROUS COMPOUNDS; IRON; KETOGLUTARIC ACIDS; KINETICS; MIXED FUNCTION OXYGENASES; MUTAGENESIS, SITE-DIRECTED; OXYGEN; SPECTROPHOTOMETRY, ULTRAVIOLET; SUBSTRATE SPECIFICITY; TAURINE;

EID: 14844358869     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048746n     Document Type: Article

References (56)

1. II/α-ketoglutarate-dependent hydroxylases and related enzymes, Crit. Rev. Biochem. Mol. Biol. 39, 21-68.
2. 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.
3. Trewick, S. C., Henshaw, T. F., Hausinger, R. P., Lindahl, T., and Sedgwick, B. (2002) Oxidative demethylatton by Escherichia coli AlkB directly reverts DNA base damage, Nature 419, 174-178.
4. Aas, P. A., Otterlei, M., Falnes, P. O., Vagbe, C. B., Skorpen, F., Akbari, M., Sundheim, O., Bjoras, M., Slupphaug, G., Seeberg, E., and Krokan, H. E. (2003) Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA, Nature 421, 859-863.
5. Kivirikko, K. I., and Pihlajaniemi, T. (1998) Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylase, Adv. Enzymol. Relat. Areas Mol. Biol. 72, 325-398.
6. 2 sensing, Science 292, 464-467.
7. 2-regulated prolyl hydroxylation, Science 292, 468-472.
8. Dann, C. E., III, Bruick, R. K., and Deisenhofer, J. (2002) Structure of a factor-inhibiting hypoxia-inducible factor 1: An essential asparaginyl hydroxylase involved in the hypoxic response pathway, Proc. Natl. Acad. Sci. U.S.A. 99, 15351-15356.
9. 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.
10. Clifton, I. J., Hsueh, L.-C., Baldwin, J. E., Harlos, K., and Schofield, C. J. (2001) Structure of proline 3-hydroxylase. Evolution of the family of 2-oxoglutarate dependent dioxygenases, Eur. J. Biochem. 268, 6625-6636.
11. Lukacin, R., Groning, I., Pieper, U., and Matern, U. (2000) Site-directed mutagenesis of the active site serine290 in flavanone 3β-hydroxylase from Petunia hybrida, Eur. J. Biochem. 267, 853-860.
12. Hedden, P., and Phillips, A. L. (2000) Gibberellin metabolism: New insights revealed by the genes, Trend Plant Sci. 5, 523-528.
13. De Carolis, E., Chan, F., Balsevich, J., and De Luca, V. (1990) Isolation and characterization of a 2-oxoglutarate dependent dioxygenase involved in the second-to-last step in vindoline biosynthesis, Plant Physiol. 94, 1323-1329.
14. Hashimoto, T., and Yamada, Y. (1987) Purification and characterization of hyoscyamine 6β-hydroxylase from root cultures of Hyoscyamus niger L. Hydroxylase and epoxidase activities of enzyme preparations, Eur. J. Biochem. 164, 277-285.
15. Jansen, G. A., Mihalik, S. J., Watkins, P. A., Jakobs, C., Moser, H. W., and Wanders, R. J. A. (1998) Characterization of phytanoyl-coenzyme A hydroxylase in human liver and activity measurements in patients with peroxisomal disorders, Clin. Chim. Acta 271, 203-211.
16. Fukumori, F., and Hausinger, R. P. (1993) Purification and characterization of 2,4-dichlorophenoxyacetate/α-ketoglutarate dioxygenase, J. Biol. Chem. 268, 24311-24317.
17. 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 394, 805-809.
18. Wilmouth, R. C., Turnbull, J. J., Welford, R. W. D., Clifton, I. J., Prescott, A. G., and Schofield, C. J. (2002) Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure 10, 93-103.
19. Roach, P. L., Clifton, I. J., Hensgens, C. M. H., Shibata, N., Schofield, C. J., Hajdu, J., and Baldwin, J. E. (1997) Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation, Nature 387, 827-830.
20. 2 activation in the biosynthesis of ethylene, J. Am. Chem. Soc. 124, 4602-4609.
21. Clifton, I. J., Doan, L. X., Sleeman, M. C., Topf, M., Suzuki, H., Wilmouth, R. C., and Schofield, C. J. (2003) Crystal structure of carbapenem synthase (CarC), J. Biol. Chem. 278, 20843-20850.
22. 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.
23. 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.
24. Hanauske-Abel, H. M., and Günzler, V. (1982) A stereochemical concept for the catalytic mechanism of prolylhydroxylase. Applicability to classification and design of inhibitors, J. Theor. Biol. 94, 421-455.
25. Sono, M., Roach, M. P., Coulter, E. D., and Dawson, J. H. (1996) Heme-containing oxygenases, Chem. Rev. 96, 2841-2887.
26. 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.
27. O'Brien, J. R., Schuller, D. J., Yang, V. S., Dillard, B. D., and Lanzilotta, W. N. (2003) Substrate-induced conformational changes in Escherichia coli taurine/α-ketoglutarate dioxygenase and insight into the oligomeric structure, Biochemistry 42, 5547-5554.
28. Lee, H. J., Lloyde, M. D., Clifton, I. J., Baldwin, J. E., and Schofield, C. J. (2001) Kinetic and crystallographic studies on deacetoxycephalosporin C synthase (DAOCS), J. Mol. Biol. 308, 937-948.
29. II-2-oxoglutarate-substrate-NO complex: Evidence for metal centred rearrangements, FEBS Lett. 517, 7-12.
30. Elkins, J. M., Hewitson, K. S., McNeill, L. A., Seibel, J. F., Schlemminger, I., Pugh, C. W., Ratcliffe, P. J., and Schofield, C. J. (2003) Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1α, J. Biol. Chem. 278, 1802-1806.
31. II α-ketoglutarate-dependent dioxygenase superfamily, Biochemistry 43, 3075-3088.
32. 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.
33. 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.
34. 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.
35. II-α-keto acid chromophore in model and enzyme complexes, J. Am. Chem. Soc. 123, 5022-5029.
36. IV complex in taurine/α-ketoglutarate dioxygenase (TauD) from Escherichia coli, Biochemistry 42, 7497-7508.
37. IV intermediate detected during oxygen activation by taurine:α-ketoglutarate dioxygenase (TauD), J. Am. Chem. Soc. 125, 13008-13009.
38. Proshlyakov, D. A., Henshaw, T. F., Monterosso, G. R., Ryle, M. J., and Hausinger, R. P. (2004) Direct detection of oxygen intermediates in the non-heme Fe enzyme taurine/α-ketoglutarate dioxygenase, J. Am. Chem. Soc. 126, 1022-1023.
39. IV intermediate observed during oxygen activation by taurine:α-ketoglutarate dioxygenase, J. Am. Chem. Soc. 126, 8108-8109.
40. Borowski, T., Bassan, A., and Siegbahn, P. E. M. (2004) Mechanism of dioxygen activation in 2-oxoglutarate-dependent enzymes: A hybrid DFT study, Chem. Eur. J. 10, 1031-1041.
41. IV=O complex, Science 299, 1037-1039.
42. IV=O complex of a tetradentate tripodal nonheme ligand, Proc. Natl. Acad. Sci. U.S.A. 100, 3665-3670.
43. IV=O complex, J. Am. Chem. Soc. 126, 5378-5379.
44. 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.
45. Henshaw, T. F., Feig, M., and Hausinger, R. P. (2004) Aberrant activity of the DNA repair enzyme AlkB, J. Inorg. Biochem. 98, 856-861.
46. 2- and α-ketoglutarate-dependent tyrosyl radical formation in TauD, an α-keto acid-dependent non-heme iron dioxygenase, Biochemistry 42, 1854-1862.
47. Ryle, M. J., Koehntop, K. D., Liu, A., Que, L., Jr., and Hausinger, R. P. (2003) Interconversion of two oxidized forms of TauD, a non-heme iron hydroxylase: Evidence for bicarbonate binding, Proc. Natl. Acad. Sci. U.S.A. 100, 3790-3795.
48. Johnson-Winters, K., Purpero, V. M., Kavana, M., Nelson, T., and Moran, G. R. (2003) (4-Hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis: The basis for ordered substrate addition, Biochemistry 42, 2072-2080.
49. Brownlee, J. M., Johnson-Winters, K., Harrison, D. H. T., and Moran, G. R. (2004) Structure of the ferrous form of (4-hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis in complex with the therapeutic herbicide, NTBC, Biochemistry 43, 6370-6377.
50. Borowski, T., Bassan, A., and Siegbahn, P. E. M. (2004) 4-Hydroxyphenylpyruvate dioxygenase: A hybrid density functional study of the catalytic reaction mechanism, Biochemistry 43, 12331-12342.
51. Moran, G. R. (2005) 4-Hydroxyphenylpyruvate dioxygenase, Arch. Biochem. Biophys. 433, 117-128.
52. 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.
53. Patil, P. V., and Ballou, D. P. (2000) The use of protocatechuate dioxygenase for maintaining anaerobic conditions in biochemical experiments, Anal. Biochem. 286, 187-192.
54. Matheson, I. B. C., and De Sa, R. J. (1990) Robust multivariate analysis applied to separation of components in absorption spectra, Comput. Chem. 14, 157-164.
55. Schowen, K. B., and Schowen, R. L. (1982) Solvent isotope effects of enzyme systems, Methods Enzymol. 87, 551-606.
56. Bevington, P. R. (1969) in Data Reduction and Error Analysis for the Physical Sciences, pp 235-242, McGraw-Hill, Inc., New York.