Kinetic and CD/MCD spectroscopic studies of the atypical, three-his-ligated, non-heme Fe2+ center in diketone dioxygenase: The role of hydrophilic outer shell residues in catalysis

Biochemistry

Volumn 49, Issue 5, 2010, Pages 996-1004

  Straganz, Grit D ^a,b   Diebold, Adrienne R ^b   Egger, Sigrid ^a   Nidetzky, Bernd ^a   Solomon, Edward I ^b  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE POCKET; COFACTORS; DIKETONES; DIOXYGENASES; ENERGY SPLITTINGS; ENZYME CATALYSIS; HYDROPHILIC RESIDUES; LIGAND FIELD; MUTATIONAL ANALYSIS; O2 REDUCTION; OUTER SHELLS; PH DEPENDENCE; PH TITRATION; PRE-STEADY STATE; SPECTROSCOPIC DATA; SPECTROSCOPIC STUDIES; STABILIZING EFFECTS; STEADY STATE; SUBSTRATE BINDING; WILD TYPES; WILD-TYPE ENZYMES;

CATALYSIS; ENZYMES; HEMOGLOBIN; HYDROPHILICITY; KETONES; PHOSPHATASES; PORPHYRINS; SPECTROSCOPIC ANALYSIS; SULFUR COMPOUNDS;

BINDING ENERGY;

DIKETONE; DIOXYGENASE; LIGAND; METAL; OXYGEN;

ARTICLE; AUTOOXIDATION; CATALYSIS; CIRCULAR DICHROISM; CONTROLLED STUDY; ENERGY; ENZYME ACTIVE SITE; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; GEOMETRY; HYDROPHILICITY; KINETICS; MUTATIONAL ANALYSIS; PH MEASUREMENT; PRIORITY JOURNAL; PROTON TRANSPORT; STEADY STATE; TITRIMETRY;

ACINETOBACTER; CATALYSIS; CIRCULAR DICHROISM; CYSTEINE DIOXYGENASE; DIOXYGENASES; ENZYME STABILITY; FERROUS COMPOUNDS; GLUTAMIC ACID; GLUTAMINE; HEMEPROTEINS; HISTIDINE; KINETICS; LIGANDS; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; WATER;

EID: 75749094338     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901339n     Document Type: Article

References (33)

1. Costas, M., Mehn, M. P., Jensen, M. P., and Que, L., Jr. (2004) Dioxygen activation at mononuclear nonheme iron active sites: Enzymes, models, and intermediates. Chem. Rev. 104, 939-986.
2. Hegg, E. L., and Que, L., Jr. (1997) The 2-His-1-carboxylate facial triad-an emerging structural motif in mononuclear non-heme iron(II) enzymes. Eur. J. Biochem. 250, 625-629.
3. 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, 235-350.
4. Groce, S. L., and Lipscomb, J. D. (2005) Aromatic ring cleavage by homoprotocatechuate 2,3-dioxygenase: Role of His200 in the kinetics of interconversion of reaction cycle intermediates. Biochemistry 44, 7175-7188.
5. Mendel, S., Arndt, A., and Bugg, T. D. (2004) Acid-base catalysis in the extradiol catechol dioxygenase reaction mechanism: Site-directed mutagenesis of His-115 and His-179 in Escherichia coli 2,3-dihydroxyphenylpropionate 1,2-dioxygenase (MhpB). Biochemistry 43, 13390-13396.
6. Siegbahn, P. E., and Haeffner, F. (2004) Mechanism for catechol ringcleavage by non-heme iron extradiol dioxygenases. J. Am. Chem. Soc. 126, 8919-8932.
7. Viggiani, A., Siani, L., Notomista, E., Birolo, L., Pucci, P., and Di Donato, A. (2004) The role of the conserved residues His-246, His-199, and Tyr-255 in the catalysis of catechol 2,3-dioxygenase from Pseudomonas stutzeri OX1. J. Biol. Chem. 279, 48630-48639.
8. Neidig, M. L., Brown, C. D., Light, K. M., Fujimori, D. G., Nolan, E. M., Price, J. C., Barr, E. W., Bollinger, J. M., Jr., Krebs, C., Walsh, C. T., and Solomon, E. I. (2007) CD and MCD of CytC3 and taurine dioxygenase: Role of the facial triad in α-KG-dependent oxygenases. J. Am. Chem. Soc. 129, 14224-14231.
9. Straganz, G. D., and Nidetzky, B. (2006) Variations of the 2-His-1-carboxylate theme in mononuclear non-heme Fe(II) oxygenases. ChemBioChem 7, 1536-1548.
10. Blasiak, L. C., Vaillancourt, F. H., Walsh, C. T., and Drennan, C. L. (2006) Crystal structure of the non-haem iron halogenase SyrB2 in syringomycin biosynthesis. Nature 440, 368-371.
11. Wong, C., Fujimori, D. G., Walsh, C. T., and Drennan, C. L. (2009) Structural analysis of an open active site conformation of nonheme iron halogenase CytC3. J. Am. Chem. Soc. 131, 4872-4879.
12. Gudrun, R. (2002) Stranzl, Strukturuntersuchungen an Enzymen im Kristall und in Loesung. Ph.D. Dissertation, Karl Franzens University, Graz, Austria, pp 1-113.
13. Straganz, G., Brecker, L., Weber, H. J., Steiner, W., and Ribbons, D. W. (2002)A novel β-diketone-cleaving enzyme from Acinetobacter johnsonii: Acetylacetone 2,3-oxygenase. Biochem. Biophys. Res. Commun. 297, 232-236.
14. Straganz, G. D., Glieder, A., Brecker, L., Ribbons, D.W., and Steiner, W. (2003) Acetylacetone-cleaving enzyme Dke1: A novel C-C-bondcleaving enzyme from Acinetobacter johnsonii. Biochem. J. 369, 573-581.
15. Diebold, A. R., et al. Manuscript in preparation.
16. 2+ site in Dke1, a cupin-type dioxygenase from Acinetobacter johnsonii. Biochem. J. 418, 403-411.
17. Straganz, G. D., Hofer, H., Steiner, W., and Nidetzky, B. (2004) Electronic substituent effects on the cleavage specificity of a nonheme Fe(II)-dependent β-diketone dioxygenase and their mechanistic implications. J. Am. Chem. Soc. 126, 12202-12203.
18. Straganz, G. D., and Nidetzky, B. (2005) Reaction coordinate analysis for β-diketone cleavage by the non-heme Fe(II)-dependent dioxygenase Dke1. J. Am. Chem. Soc. 127, 12306-12314.
19. Wang,W., andMalcolm,B.A. (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using Quik Change site-directed mutagenesis. Bio Techniques 26, 680-682.
20. Straganz, G., Slavica, A., Hofer, H., Mandl, U., Steiner, W., and Nidetzky, B. (2005) Integrated approach for production of recombinant acetylacetone dioxygenase from Acinetobacter johnsonii. Biocatal. Biotransform. 23, 261-269.
21. Skerra, A., and Schmidt, T. G. (2000) Use of the Strep-Tag and streptavidin for detection and purification of recombinant proteins. Methods Enzymol. 326, 271-304.
22. Higgins, T. (1981) Novel chromogen for serum iron determinations. Clin. Chem. 27, 1619-1620.
23. 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.
24. Pace, C. N., Vajdos, F., Fee, L., Grimsley, G., and Gray, T. (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 11, 2411-2423.
25. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6, 1948-1954.
26. Calculated using Advanced Chemistry Development (ACD/ Laboratories) version 8.14 for Solaris ( 1994-2007) ACD/Laboratories, Scifinder Scholar.
27. Solomon, E. I., Pavel, E. G., Loeb, K. E., and Campochiaro, C. (1995) Magnetic circular dichroism spectroscopy as a probe of the geometric and electronic structure of non-heme ferrous enzymes. Coord. Chem. Rev., 369-460.
28. Pavel, E. G., Kitajima, N., and Solomon, E. I. (1998) Magnetic Circular Dichroism Spectroscopic Studies of Mononuclear Non-Heme Ferrous Model Complexes. Correlation of Excited- and Ground-State Electronic Structure with Geometry. J. Am. Chem. Soc. 120, 3949-3962.
29. DiTusa, C. A., McCall, K. A., Christensen, T., Mahapatro, M., Fierke, C. A., and Toone, E. J. (2001) Thermodynamics of metal ion binding. 2. Metal ion binding by carbonic anhydrase variants. Biochemistry 40, 5345-5351.
30. Lachenmann, M. J., Ladbury, J. E., Dong, J., Huang, K., Carey, P., and Weiss, M. A. (2004) Why zinc fingers prefer zinc: Ligand-field symmetry and the hidden thermodynamics of metal ion selectivity. Biochemistry 43, 13910-13925.
31. Dudev, T., Lin, Y. L., Dudev, M., and Lim, C. (2003) First-second shell interactions in metal binding sites in proteins: A PDB survey and DFT/CDM calculations. J. Am. Chem. Soc. 125, 3168-3180.
32. Frison, G., and Ohanessian, G. (2009) Metal-histidine-glutamate as a regulator of enzymatic cycles: A case study of carbonic anhydrase. Phys. Chem. Chem. Phys. 11, 374-383.
33. Whiting, A. K., Boldt, Y. R., Hendrich, M. P., Wackett, L. P., and Que, L., Jr. (1996) Manganese(II)-dependent extradiol-cleaving catechol dioxygenase from Arthrobacter globiformis CM-2. Biochemistry 35, 160-170.