Spectroscopic and computational characterization of the NO adduct of substrate-bound Fe(II) cysteine dioxygenase: Insights into the mechanism of O2 activation

Biochemistry

Volumn 52, Issue 35, 2013, Pages 6040-6051

  Blaesi, Elizabeth J ^a   Gardner, Jessica D ^a,b   Fox, Brian G ^a   Brunold, Thomas C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b American Journal Experts   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE DIOXYGENASE; DIFFERENT GEOMETRY; ELECTRONIC ABSORPTION SPECTROSCOPY; MAGNETIC CIRCULAR DICHROISMS; REACTION PATHWAYS; SELENOCYSTEINE; SEMI-EMPIRICAL CALCULATION; SUBSTRATE-BOUND;

ELECTRONIC PROPERTIES; ELECTRONIC STRUCTURE; GEOMETRY; MAGNETIC RESONANCE;

AMINO ACIDS;

CYSTEINE DIOXYGENASE; FERROUS ION; NITRIC OXIDE; OXYGEN; SELENOCYSTEINE;

ABSORPTION SPECTROSCOPY; ARTICLE; CHEMICAL STRUCTURE; CIRCULAR DICHROISM; DENSITY FUNCTIONAL THEORY; ELECTRON SPIN RESONANCE; ELECTRONICS; ENERGY; GENE EXPRESSION; GEOMETRY; OXIDATION; PRIORITY JOURNAL; PROTEIN PURIFICATION; REACTION ANALYSIS; SPECTROSCOPY;

CIRCULAR DICHROISM; CYSTEINE DIOXYGENASE; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERROUS COMPOUNDS; GENE EXPRESSION; MODELS, MOLECULAR; NITRIC OXIDE; OXYGEN;

EID: 84883481558     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400825c     Document Type: Article

References (67)

1. Yamaguchi, K. and Hosokawa, Y. (1987) Cysteine dioxygenase Methods Enzymol. 143, 395-403
2. 18oxygen J. Biol. Chem. 244, 1172-1175
3. Cooper, A. J. (1983) Biochemistry of sulfur-containing amino-acids Annu. Rev. Biochem. 52, 187-222
4. Stipanuk, M. H. (2004) Sulfur amino acid metabolism: Pathways for production and removal of homocysteine and cysteine Annu. Rev. Nutr. 24, 539-577
5. Slivka, A. and Cohen, G. (1993) Brain ischemia markedly elevates levels of the neurotoxic amino-acid, cysteine Brain Res. 608, 33-37
6. Pean, A. R., Parsons, R. B., Waring, R. H., Williams, A. C., and Ramsden, D. B. (1995) Toxicity of sulfur-containing-compounds to neuronal cell-lines J. Neurol. Sci. 129, 107-108
7. Heafield, M. T., Fearn, S., Steventon, G. B., Waring, R. H., Williams, A. C., and Sturman, S. G. (1990) Plasma cysteine and sulfate levels in patients with motor-neuron, Parkinson's and Alzheimer's disease Neurosci. Lett. 110, 216-220
8. Gordon, C., Bradley, H., Waring, R. H., and Emery, P. (1992) Abnormal sulfur oxidation in systemic Lupus-Erythematosus Lancet 339, 25-26
9. Emery, P., Bradley, H., Gough, A., Arthur, V., Jubb, R., and Waring, R. (1992) Increased prevalence of poor sulphoxidation in patients with rheumatoid arthritis: Effect of changes in the acute phase response and second line drug treatment Ann. Rheum. Dis. 51, 318-320
10. McCoy, J. G., Bailey, L. J., Bitto, E., Bingman, C. A., Aceti, D. J., Fox, B. G., and Phillips, G. N. (2006) Structure and mechanism of mouse cysteine dioxygenase Proc. Natl. Acad. Sci. U.S.A. 103, 3084-3089
11. Ye, S., Wu, X., Wei, L., Tang, D., Sun, P., Bartlam, M., and Rao, Z. (2007) An insight into the mechanism of human cysteine dioxygenase. Key roles of the thioether-bonded tyrosine-cysteine cofactor J. Biol. Chem. 282, 3391-3402
12. Straganz, G. D. and Nidetzky, B. (2006) Variations of the 2-His-1-carboxylate theme in mononudear non-heme Fe-III oxygenases ChemBioChem 7, 1536-1548
13. Straganz, G. D., Glieder, A., Brecker, L., Ribbons, D. W., and Steiner, W. (2003) Acetylacetone-cleaving enzyme Dke1: A novel C-C-bond-cleaving enzyme from Acinetobacter johnsonii Biochem. J. 369, 573-581
14. Straganz, G. D., Diebold, A. R., Egger, S., Nidetzky, B., and Solomon, E. I. (2010) 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 49, 996-1004
15. Leitgeb, S. and Nidetzky, B. (2008) Structural and functional comparison of 2-His-1-carboxylate and 3-His metallocentres in non-haem iron(II)-dependent enzymes Biochem. Soc. Trans. 36, 1180-1186
16. Hegg, E. L. and Que, L. (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
17. Koehntop, K. D., Emerson, J. P., and Que, L. (2005) The 2-His-1-carboxylate facial triad: A versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymes J. Biol. Inorg. Chem. 10, 87-93
18. Wachter, R. M. and Branchaud, B. P. (1998) Construction and analysis of a semi-quantitative energy profile for the reaction catalyzed by the radical enzyme galactose oxidase Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1384, 43-54
19. Whittaker, M. M., Ekberg, C. A., Peterson, J., Sendova, M. S., Day, E. P., and Whittaker, J. W. (2000) Spectroscopic and magnetochemical studies on the active site copper complex in galactose oxidase J. Mol. Catal. B: Enzym. 8, 3-15
20. Schnell, R., Sandalova, T., Hellman, U., Lindqvist, Y., and Schneider, G. (2005) Siroheme- and Fe-4-S-4 -dependent NirA from Mycobacterium tuberculosis is a sulfite reductase with a covalent Cys-Tyr bond in the active site J. Biol. Chem. 280, 27319-27328
21. Ito, N., Phillips, S. E. V., Stevens, C., Ogel, Z. B., McPherson, M. J., Keen, J. N., Yadav, K. D. S., and Knowles, P. F. (1991) Novel thioether bond revealed by a 1.7-A crystal-structure of galactose-oxidase Nature 350, 87-90
22. Whittaker, M. M. and Whittaker, J. W. (2003) Cu(I)-dependent biogenesis of the galactose oxidase redox cofactor J. Biol. Chem. 278, 22090-22101
23. Siakkou, E., Rutledge, M. T., Wilbanks, S. M., and Jameson, G. N. L. (2011) Correlating crosslink formation with enzymatic activity in cysteine dioxygenase Biochim. Biophys. Acta, Proteins Proteomics 1814, 2003-2009
24. Dominy, J. E., Simmons, C. R., Karplus, P. A., Gehring, A. M., and Stipanuk, M. H. (2006) Identification and characterization of bacterial cysteine dioxygenases: A new route of cysteine degradation for eubacteria J. Bacteriol. 188, 5561-5569
25. Aluri, S. and de Visser, S. P. (2007) The mechanism of cysteine oxygenation by cysteine dioxygenase enzymes J. Am. Chem. Soc. 129, 14846-14847
26. Kumar, D., Thiel, W., and de Visser, S. P. (2011) Theoretical study on the mechanism of the oxygen activation process in cysteine dioxygenase enzymes J. Am. Chem. Soc. 133, 3869-3882
27. Pierce, B. S., Gardner, J. D., Bailey, L. J., Brunold, T. C., and Fox, B. G. (2007) Characterization of the nitrosyl adduct of substrate-bound mouse cysteine dioxygenase by electron paramagnetic resonance: Electronic structure of the active site and mechanistic implications Biochemistry 46, 8569-8578
28. Tchesnokov, E. P., Wilbanks, S. M., and Jameson, G. N. L. (2012) A strongly bound high-spin iron(II) coordinates cysteine and homocysteine in cysteine dioxygenase Biochemistry 51, 257-264
29. Gardner, J. D., Pierce, B. S., Fox, B. G., and Brunold, T. C. (2010) Spectroscopic and computational characterization of substrate-bound mouse cysteine dioxygenase: Nature of the ferrous and ferric cysteine adducts and mechanistic implications Biochemistry 49, 6033-6041
30. Brown, C. A., Pavlosky, M. A., Westre, T. E., Zhang, Y., Hedman, B., Hodgson, K. O., and Solomon, E. I. (1995) Spectroscopic and theoretical description of the electronic-structure of S = 3/2 iron-nitrosyl complexes and their relation to O2 activation by non-heme tron enzyme active-sites J. Am. Chem. Soc. 117, 715-732
31. Nauser, T., Dockheer, S., Kissner, R., and Koppenol, W. H. (2006) Catalysis of electron transfer by selenocysteine Biochemistry 45, 6038-6043
32. Kleffmann, T., Jongkees, S. A. K., Fairweather, G., Wilbanks, S. M., and Jameson, G. N. L. (2009) Mass-spectrometric characterization of two posttranslational modifications of cysteine dioxygenase J. Biol. Inorg. Chem. 14, 913-921
33. Hondal, R. J., Nilsson, B. L., and Raines, R. T. (2001) Selenocysteine in native chemical ligation and expressed protein ligation J. Am. Chem. Soc. 123, 5140-5141
34. Smith, A. T., Majtan, T., Freeman, K. M., Su, Y., Kraus, J. P., and Burstyn, J. N. (2011) Cobalt cystathionine beta-synthase: A cobalt-substituted heme protein with a unique thiolate ligation motif Inorg. Chem. 50, 4417-4427
35. (2011) IGOR Pro, Version 6.22A, WaveMetrics, Lake Oswego, OR.
36. Neese, F. (1995) The EPR program QCPE Bull. 15, 5
37. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., Nakatsuji, H., Caricato, M., Li, X., Hratchian, H. P., Izmaylov, A. F., Bloino, J., Zheng, G., Sonnenberg, J. L., J. L., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Montgomery, J., J. A., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Keith, T., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Rega, N., Millam, J. M., Klene, M., Knox, J. E., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Martin, R. L., Morokuma, K., Zakrzewski, V. G., Voth, G. A., Salvador, P., Dannenberg, J. J., Dapprich, S., Daniels, A. D., Farkas, O., Foresman, J. B., Ortiz, J. V., Cioslowski, J., and Fox, D. J. (2010) Gaussian 09, Revision C.01, Gaussian, Inc., Wallingford, CT.
38. Lee, C. T., Yang, W. T., and Parr, R. G. (1988) Development of the colle-salvetti correlation-energy formula into a functional of the electron-density Phys. Rev. B 37, 785-789
39. Becke, A. D. (1993) Density-functional thermochemistry III. The role of exact exchange J. Chem. Phys. 98, 5648-5652
40. Hehre, W. J., Ditchfie., R., and Pople, J. A. (1972) Self-consistent molecular-orbital methods XII. Further extensions of Gaussian-type basis sets for use in molecular-orbital studies of organic-molecules J. Chem. Phys. 56, 2257-2261
41. Schafer, A., Horn, H., and Ahlrichs, R. (1992) Fully optimized contracted gaussian-basis sets for atoms Li to Kr J. Chem. Phys. 97, 2571-2577
42. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules J. Am. Chem. Soc. 117, 5179-5197
43. Simmons, C. R., Krishnamoorthy, K., Granett, S. L., Schuller, D. J., Dominy, J. E., Begley, T. P., Stipanuk, M. H., and Karplus, P. A. (2008) A putative Fe2+-bound persulfenate intermediate in cysteine dioxygenase Biochemistry 47, 11390-11392
44. Word, J. M., Lovell, S. C., Richardson, J. S., and Richardson, D. C. (1999) Asparagine and glutamine: Using hydrogen atom contacts in the choice of side-chain amide orientation J. Mol. Biol. 285, 1735-1747
45. Becke, A. D. (1988) Density-functional exchange-energy approximation with correct asymptotic-behavior Phys. Rev. A 38, 3098-3100
46. Perdew, J. P. and Yue, W. (1986) Accurate and simple density functional for the electronic exchange energy: Generalized gradient approximation Phys. Rev. B 33, 8800-8802
47. Neese, F. (2012) Orca 2.9.1, An Ab Initio, DFT and Semiempirical Electronic Structure Package.
48. The PyMOL Molecular Graphics System, Version 1.5.0.4, Schrodinger, LLC.
49. Neese, F. (2001) Prediction of electron paramagnetic resonance g values using coupled perturbed Hartree-Fock and Kohn-Sham theory J. Chem. Phys. 115, 11080-11096
50. Neese, F. (2003) Metal and ligand hyperfine couplings in transition metal complexes: The effect of spin-orbit coupling as studied by coupled perturbed Kohn-Sham theory J. Chem. Phys. 118, 3939-3948
51. Neese, F. (2002) Prediction and interpretation of the Fe-57 isomer shift in Mossbauer spectra by density functional theory Inorg. Chim. Acta 337, 181-192
52. Wachters, A. J. H. (1970) Gaussian basis set for molecular wavefunctions containing third-row atoms J. Chem. Phys. 52, 1033-1036
53. (1990) The IGLO method: Ab initio calculation and interpretation of NMR chemical shifts and magnetic susceptibilities in NMR Basic Principles and Progress (Kutzelnigg, W., Fleischer, U., and Schindler, M., Eds.) Vol. 23, pp 165-262, Springer-Verlag, Heidelberg, Germany.
54. Enemark, J. H. and Feltham, R. D. (1974) Principles of structure, bonding, and reactivity for metal nitrosyl complexes Coord. Chem. Rev. 13, 339-406
55. Sellmann, D., Blum, N., Heinemann, F. W., and Hess, B. A. (2001) Synthesis, reactivity, and structure of strictly homologous 18 and 19 valence electron iron nitrosyl complexes Chem.-Eur. J. 7, 1874-1880
56. Pr(NO)] Inorg. Chem. 41, 3444-3456
57. 8 complexes of isopenicillin N synthase: Substrate determination of oxidase versus oxygenase activity in nonheme Fe enzymes J. Am. Chem. Soc. 129, 7427-7438
58. 2+/+/O J. Am. Chem. Soc. 126, 5138-5153
59. Patra, A. K., Rowland, J. M., Marlin, D. S., Bill, E., Olmstead, M. M., and Mascharak, P. K. (2003) Iron nitrosyls of a pentadentate ligand containing a single carboxamide group: Syntheses, structures, electronic properties, and photolability of NO Inorg. Chem. 42, 6812-6823
60. Stipanuk, M. H., Fieselmann, K., Hirschberger, L. L., Ueki, I., Lam, J., Peters, R., Roman, H. B., and Valli, A. (2011) Sulfur metabolism in the cysteine dioxygenase knockout mouse: Impairment in taurine synthesis and increased formation of acid labile sulfur Amino Acids 41, S78
61. Brait, M., Ling, S., Nagpal, J. K., Chang, X., Park, H. L., Lee, J., Okamura, J., Yamashita, K., Sidransky, D., and Kim, M. S. (2012) Cysteine dioxygenase 1 is a tumor suppressor gene silenced by promoter methylation in multiple human cancers PLoS One e44951-1-e44951-19
62. Crawford, J. A., Li, W., and Pierce, B. S. (2011) Single turnover of substrate-bound ferric cysteine dioxygenase with superoxide anion: Enzymatic reactivation, product formation, and a transient intermediate Biochemistry 50, 10241-10253
63. Ghosh, P., Stobie, K., Bill, E., Bothe, E., Weyhermuller, T., Ward, M. D., McCleverty, J. A., and Wieghardt, K. (2007) Electronic structure of nitric oxide adducts of bis(diaryl-1,2-dithiolene)iron compounds: Four-membered electron-transfer series Fe(NO)(L)(2) (z) (z = 1+, 0, 1-, 2-) Inorg. Chem. 46, 522-532
64. Bartberger, M. D., Liu, W., Ford, E., Miranda, K. M., Switzer, C., Fukuto, J. M., Farmer, P. J., Wink, D. A., and Houk, K. N. (2002) The reduction potential of nitric oxide (NO) and its importance to NO biochemistry Proc. Natl. Acad. Sci. U.S.A. 99, 10958-10963
65. Wood, P. M. (1987) The two redox potentials for oxygen reduction to superoxide Trends Biochem. Sci. 12, 250-251
66. Ghosh, A. (2006) Transition metal spin state energetics and noninnocent systems: challenges for DFT in the bioinorganic arena J. Biol. Inorg. Chem. 11, 712-724
67. Che, X., Gao, J., Liu, Y., and Liu, C. (2013) Metal vs. chalcogen competition in the catalytic mechanism of cysteine dioxygenase J. Inorg. Biochem. 122, 1-7