Transiently produced hypochlorite is responsible for the irreversible inhibition of chlorite dismutase

Biochemistry

Volumn 53, Issue 19, 2014, Pages 3145-3157

  Hofbauer, Stefan ^a   Gruber, Clemens ^a   Pirker, Katharina F ^a   Sündermann, Axel ^a   Schaffner, Irene ^a   Jakopitsch, Christa ^a   Oostenbrink, Chris ^a   Furtmüller, Paul G ^a   Obinger, Christian ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CHLORINE COMPOUNDS; ESCHERICHIA COLI; MASS SPECTROMETRY;

BOND FORMATION; DISMUTASE; IRREVERSIBLE INACTIVATION; IRREVERSIBLE INHIBITIONS; NITROSPIRA; OXIDATIVE MODIFICATION; OXIDO-REDUCTASES; REACTION MECHANISM;

PORPHYRINS;

BACTERIA; BACTERIAL PROTEINS; HYDROGEN-ION CONCENTRATION; HYPOCHLOROUS ACID; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN; RECOMBINANT PROTEINS;

EID: 84900993058     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi500401k     Document Type: Article

References (40)

1. Hagedoorn, P. L., de Geus, D. C., and Hagen, W. R. (2002) Spectroscopic characterization and ligand-binding properties of chlorite dismutase from the chlorate respiring bacterial strain GR-1 Eur. J. Biochem. 269, 4905-4911
2. Lee, A. Q., Streit, B. R., Zdilla, M. J., Abu-Omar, M. M., and Dubois, J. L. (2008) Mechanism of and exquisite selectivity for O-O bond formation by the heme dependent chlorite dismutase Proc. Natl. Acad. Sci. U.S.A. 105, 15654-15659
3. Keith, J. M., Abu-Omar, M. M., and Hall, M. B. (2011) Computational investigation of the concerted dismutation of chlorite ion by water-soluble iron porphyrins Inorg. Chem. 50, 7928-7930
4. Sun, S., Li, Z. S., and Chen, S. L. (2014) A dominant homolytic O-Cl bond cleavage with low-spin triplet-state Fe(IV) - O formed is revealed in the mechanism of heme-dependent chlorite dismutase Dalton Trans. 43, 973-981
5. de Geus, D. C., Thomassen, E. A. J., Hagedoorn, P.-L., Pannu, N. S., van Duijn, E., and Abrahams, J. P. (2009) Crystal structure of chlorite dismutase, a detoxifying enzyme producing molecular oxygen J. Mol. Biol. 387, 192-206
6. Goblirsch, B. R., Streit, B. R., DuBois, J. L., and Wilmot, C. M. (2010) Structural features promoting dioxygen production by Dechloromonas aromatica chlorite dismutase JBIC, J. Biol. Inorg. Chem. 15, 879-888
7. Kostan, J., Sjoeblom, B., Maixner, F., Mlynek, G., Furtmüller, P. G., Obinger, C., Wagner, M., Daims, H., and Djinovic-Carugo, K. (2010) Structural and functional analysis of the chlorite dismutase from the nitrite-oxidizing bacterium Candidatus "Nitrospira defluvii": Identification of a catalytically important amino acid residue J. Struct. Biol. 172, 331-342
8. Mlynek, G., Sjöblom, B., Kostan, J., Füreder, S., Maixner, F., Gysel, K., Furtmüller, P. G., Obinger, C., Wagner, M., Daims, H., and Djinovic-Carugo, K. (2011) Unexpected diversity of chlorite dismutases: A catalytically efficient dimeric enzyme from Nitrobacter winogradskyi J. Bacteriol. 193, 2408-2417
9. Blanc, B., Mayfield, J. A., McDonald, C. A., Lukat-Rodgers, G. S., Rodgers, K. R., and Dubois, J. L. (2012) Understanding how the distal environment directs reactivity in chlorite dismutase: Spectroscopy and reactivity of Arg183 mutants Biochemistry 51, 1895-1910
10. Hofbauer, S., Gysel, K., Bellei, M., Hagmüller, A., Schaffner, I., Mlynek, G., Kostan, J., Pirker, K. F., Daims, H., Furtmüller, P. G., Battistuzzi, G., Djinovic-Carugo, K., and Obinger, C. (2014) Manipulating conserved heme cavity residues of Chlorite dismutase: Effect on structure, redox chemistry and reactivity Biochemistry 53, 77-89
11. Stenklo, K., Thorell, D., Bergius, H., Aasa, R., and Nilsson, T. (2001) Chlorite dismutase from Ideonella dechloratans JBIC, J. Biol. Inorg. Chem. 6, 601-607
12. Mehboob, F., Wolterink, A. F., Vermeulen, A. J., Jiang, B., Hagedoorn, P. L., Stams, A. J., and Kengen, S. W. (2009) Purifcation and characterization of a chlorite dismutase from Pseudomonas chloritidismutans FEMS Microbiol. Lett. 293, 115-121
13. Streit, B. R. and DuBois, J. L. (2008) Chemical and steady-state analysis of a heterologously expressed heme dependent chlorite dismutase Biochemistry 47, 5271-5280
14. Streit, B. R., Blanc, B., Lukat-Rodgers, B. S., Rodgers, K. R., and DuBois, J. L. (2010) How active-site protonation state influences the reactivity and ligation of the heme in chlorite dismutase J. Am. Chem. Soc. 132, 5711-5724
15. Hofbauer, S., Bellei, M., Sündermann, A., Pirker, K. F., Hagmüller, A., Mlynek, G., Kostan, J., Daims, H., Furtmüller, P. G., Djinovic-Carugo, K., Oostenbrink, C., Battistuzzi, G., and Obinger, C. (2012) Redox thermodynamics of high-spin and low-spin forms of chlorite dismutases with diverse subunit and oligomeric structures Biochemistry 51, 9501-9512
16. 2 producing chlorite dismutases Dalton Trans. 42, 3156-3131
17. Hofbauer, S., Gysel, K., Mlynek, G., Kostan, J., Hagmüller, A., Daims, H., Furtmüller, P. G., Djinovic-Carugo, K., and Obinger, C. (2012) Impact of subunit and oligomeric structure on the thermal and conformational stability of chlorite dismutases Biochim. Biophys. Acta 1824, 1031-1038
18. Philippi, M., dos Santos, H. S., Martins, A. O., Azevedo, C. M., and Pires, M. (2007) Alternative spectrophotometric method for standardization of chlorite aqueous solutions Anal. Chim. Acta 585, 361-365
19. Armesto, X. L., Canle, M. L., Fernandez, M. I., Garcia, M. V., and Santaballa, J. A. (2000) First steps in the oxidation of sulfur-containing amino acids by hypohalogenation: Very fast generation of intermediate sulfenyl halides and halosulfonium cations Tetrahedron 56, 1103-1109
20. Peskin, A. V., Turner, R., Maghzal, G. J., Winterbourn, C. C., and Kettle, A. J. (2009) Oxidation of methionine to dehydromethionine by reactive halogen species generated by neutrophils Biochemistry 48, 10175-10182
21. Tachikawa, M., Sayama, C., Saita, K., Tezuka, M., and Sawamura, R. (2002) Effects of isocyanuric acid on the monochlorodimedone chlorinating rates with free chlorine and ammonia chloramine in water Water Res. 10, 2547-2554
22. Kettle, A. J. and Winterbourn, C. C. (1988) The mechanism of myeloperoxidase-dependent chlorination of monochlorodimedon Biochim. Biophys. Acta 957, 185-191
23. Flemmig, J., Zschaler, J., Remmler, J., and Arnhold, J. (2012) The fluorescein-derived dye aminophenyl fluorescein is a suitable tool to detect hypobromous acid (HOBr)-producing activity in eosinophils J. Biol. Chem. 287, 27913-27923
24. Jakopitsch, C., Pirker, K. F., Flemmig, J., Hofbauer, S., Schlorke, D., Furtmüller, P. G., Arnhold, J., and Obinger, C. (2014) Mechanism of reaction of chlorite with mammalian heme peroxidases J. Inorg. Biochem. 135, 10-19
25. Stoll, S. and Schweiger, A. (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR J. Magn. Reson. 178, 42-55
26. Peisach, J., Blumberg, W. E., Ogawa, S., Rachmilewitz, E. A., and Oltzik, R. (1971) The effects of protein conformation on the heme symmetry in high spin and ferric heme proteins as studied by electron paramagnetic resonance J. Biol. Chem. 246, 3342-3355
27. Schmid, N., Christ, C. D., Christen, M., Eichenberger, A. P., and van Gunsteren, W. F. (2012) Architecture, implementation and parallelisation of the GROMOS software for biomolecular simulation Comput. Phys. Commun. 183, 890-903
28. Schmid, N., Eichenberger, A. P., Choutko, A., Riniker, S., Winger, M., Mark, A. E., and van Gunsteren, W. F. (2011) Definition and testing of the GROMOS force-field versions 54A7 and 54B7 Eur. Biophys. J. 40, 846-856
29. Hofbauer, S., Schaffner, I., Furtmüller, P. G., and Obinger, C. (2014) Chlorite dismutases: A heme enzyme family for use in bioremediation and generation of molecular oxygen Biotechnol. J. 9, 461-473
30. Setsukinai, K., Urano, Y., Kakinuma, K., Majima, H. J., and Nagano, T. (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species J. Biol. Chem. 278, 3170-3175
31. Delporte, C., Zouaoui Boudjeltia, K., Noyon, C., Furtmüller, P. G., Slomianny, M.-C., Dufour, D., Vanhamme, L., Reyé, F., Rousseau, A., Vanhaeverbeek, M., Ducobu, J., Michalski, J.-C., Neve, J., Obinger, C., Malle, E., and Van Antwerpen, P. (2014) Impact of interaction between low-density lipoproteins and myeloperoxidase on specific enzymatic activity and post-translational oxidative modifications of apoB100 J. Lipid Res. 55, 747-757
32. Hazen, S. L. and Heinecke, J. W. (1997) 3-Chlorotyrosine, a specific marker of myeloperoxidase-catalyzed oxidation, is markedly elevated in low density lipoprotein isolated from human artherosclerotic intima J. Clin. Invest. 99, 2075-2081
33. Hazen, S. L., Crowley, J. R., Mueller, M. D., and Heinecke, J. W. (1997) Mass spectrometric quantification of 3-chlorotyrosine in human tissues with attomole sensitivity: A sensitive and specific marker for myeloperoxidase- catalyzed chlorination at sites of inflammation Free Radical Biol. Med. 23, 909-916
34. Petrek, M., Otyepka, M., Banás, P., Kosinová, P., Koca, J., and Damborsky, J. (2006) CAVER: A new tool to explore routes from protein clefts, pockets and cavities BMC Bioinf. 7, 316
35. French, C. L., Yaun, S. S., Baldwin, L. A., Leonhard, D. A., Zhao, X. Q., and Calabrese, E. J. (1995) Potency ranking of methemoglobin-forming agents J. Appl. Toxicol. 15, 167-174
36. Hrycay, E. G., Gustafsson, J. A., Ingelman-Sundberg, M., and Ernster, L. (1975) Sodium periodate, sodium chloride, and organic hydroperoxides as hydroxylating agents in hepatic microsomal steroid hydroxylation reactions catalyzed by cytochrome P450 FEBS Lett. 56, 161-165
37. Jakopitsch, C., Spalteholz, H., Furtmüller, P. G., Arnhold, J., and Obinger, C. (2008) Mechanism of reaction of horseradish peroxidase with chlorite and chlorine dioxide J. Inorg. Biochem. 102, 293-302
38. Zamocky, M., Jakopitsch, C., Furtmüller, P. G., Dunand, C., and Obinger, C. (2008) The peroxidase-cyclooxygenase superfamily. Reconstructed evolution of critical enzymes of the innate immune system Proteins 71, 589-605
39. van Ginkel, C. G., Rikken, G. B., Kroon, A. G. M., and Kengen, S. W. M. (1996) Purification and characterization of chlorite dismutase: A novel oxygen-generating enzyme Arch. Microbiol. 166, 321-326
40. Mayfield, J. A., Blanc, B., Rodgers, K. R., Lukat-Rodgers, G. S., and DuBois, J. L. (2013) Peroxidase-type reactions suggest a heterolytic/ nucleophilic O-O joining mechanism in the heme-dependent chlorite dismutase Biochemistry 52, 6982-6994