Impact of distal side water and residue 315 on ligand binding to ferric Mycobacterium tuberculosis catalase - Peroxidase (KatG)

Biochemistry

Volumn 47, Issue 47, 2008, Pages 12583-12592

  Ranguelova, Kalina ^a,d   Suarez, Javier ^a,b   Metlitsky, Leonid ^a   Yu, Shengwei ^a   Brejt, Shelly Zev ^a   Brejt, Sidney Zelig ^a   Zhao, Lin ^c   Schelvis, Johannes P M ^c,e   Magliozzo, Richard S ^a,b  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e MONTCLAIR STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CATALYSTS; CYANIDES; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEMOGLOBIN; LIGANDS; OXIDATION; PARAMAGNETIC RESONANCE; PLANTS (BOTANY); PORPHYRINS; POTASSIUM; PROTEINS; VOLUMETRIC ANALYSIS;

ASSOCIATED WATERS; COMPLEX BEHAVIORS; EPR SPECTROSCOPIES; EQUILIBRIUM TITRATIONS; FUNCTIONAL PROPERTIES; HETEROGENEOUS POPULATIONS; LIGAND BINDINGS; MYCOBACTERIUM TUBERCULOSIS; OPTICAL-; POTASSIUM CYANIDES; REACTION MECHANISMS; RESONANCE RAMAN; SPECTROSCOPIC PROPERTIES; STOPPED FLOWS; TIME SCALES; TUBERCULOSIS INFECTIONS; WATER MOLECULES;

ENZYMES;

CYANIDE; FERRIC ION; HEMOPROTEIN; KATG PROTEIN; PEROXIDE; POTASSIUM CYANIDE; WATER;

ARTICLE; COMPLEX FORMATION; ELECTRON SPIN RESONANCE; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STABILITY; LIGAND BINDING; LOW TEMPERATURE; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; TITRIMETRY;

BACTERIAL PROTEINS; CYANIDES; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERRIC COMPOUNDS; ISOMERISM; LIGANDS; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PEROXIDASES; PROTONS; SPECTRUM ANALYSIS, RAMAN; TITRIMETRY; WATER;

MYCOBACTERIUM TUBERCULOSIS;

EID: 56749109668     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801511u     Document Type: Article

References (44)

1. Rouse, D. A., DeVito, J. A., Li, Z., Byer, H., and Morris, S. L. (1996) Site-directed mutagenesis of the katG gene of Mycobacterium tuberculosis: effects on catalase-peroxidase activities and isoniazid resistance. Mol. Microbiol. 22, 583-592.
2. Musser, J. M. (1996) Molecular population genetic analysis of emerged bacterial pathogens: selected insights. Emerg. Infect. Dis. 2, 1-17.
3. Marttila, H. J., Soini, H., Huovinen, P., and Viljanen, M. K. (1996) katG mutations in isoniazid-resistant Mycobacterium tuberculosis isolates recovered from Finnish patients. Antimicrob. Agents Chemother. 40, 2187-2189.
4. Bertrand, T., Eady, N. A. J., Jones, J. N., Jesmin, Nagy, J. M., Jamart-Gregoire, B., Raven, E. L., and Brown, K. A. (2004) Crystal structure of Mycobacterium tuberculosis catalase-peroxidase. J. Biol. Chem. 279, 38991-38999.
5. Zhao, X., Yu, H., Yu, S., Wang, F., Sacchettini, J. C., and Magliozzo, R. S. (2006) Hydrogen peroxide-mediated isoniazid activation catalyzed by Mycobacterium tuberculosis catalase-peroxidase (KatG) and its S315T mutant. Biochemistry 45, 4131-4140.
6. Yu, S., Girotto, S., Lee, C., and Magliozzo, R. S. (2003) Reduced affinity for isoniazid in the S315T mutant of Mycobacterium tuberculosis KatG is a key factor in antibiotic resistance. J. Biol. Chem. 278, 14769-14775.
7. Metcalfe, C., Macdonald, I. K., Murphy, E. J., Brown, K. A., Raven, E. L., and Moody, P. C. (2008) The tuberculosis prodrug isoniazid bound to activating peroxidases. J. Biol. Chem. 283, 6193-6200.
8. Pym, A. S., Saint-Joanis, B., and Cole, S. T. (2002) Effect of katG mutations on the virulence of Mycobacterium tuberculosis and the implication for transmission in humans. Infect. Immun. 70, 4955-4960.
9. Kapetanaki, S., Chouchane, S., Girotto, S., Yu, S., Magliozzo, R. S., and Schelvis, J. P. (2003) Conformational differences in Mycobacterium tuberculosis catalase-peroxidase KatG and its S315T mutant revealed by resonance Raman spectroscopy. Biochemistry 42, 3835-3845.
10. Jakopitsch, C., Auer, M., Ivancich, A., Ruker, F., FurtmuUer, P. G., and Obinger, C. (2003) Total conversion of bifunctional catalase-peroxidase (KatG) to monofunctional peroxidase by exchange of a conserved distal side tyrosine. J. Biol. Chem. 278, 20185-20191.
11. Jakopitsch, C., Ivancich, A., Schmuckenschlager, F., Wanasinghe, A., Poltl, G., Furtmuller, P. G., Ruker, F., and Obinger, C. (2004) Influence of the unusual covalent adduct on the kinetics and formation of radical intermediates in synechocystis catalase peroxidase: a stopped-flow and EPR characterization of the MET275, TYR249, and ARG439 variants. J. Biol. Chem. 279, 46082-46095.
12. Wengenack, N. L., Lane, B. D., Hill, P. J., Uhl, J. R., Lukat-Rodgers, G. S., Hall, L., Roberts, G. D., Cockerill, F. R., III, Brennan, P. J., Rodgers, K. R., Belisle, J. T., and Rusnak, F. (2004) Purification and characterization of Mycobacterium tuberculosis KatG, KatG(S315T), and Mycobacterium bovis KatG(R463L). Protein Expression Purif. 36, 232-243.
13. Cardoso, R. F., Cooksey, R. C., Morlock, G. P., Barco, P., Cecon, L., Forestiero, F., Leite, C. Q., Sato, D. N., Shikama Mde, L., Mamizuka, E. M., Hirata, R. D., and Hirata, M. H. (2004) Screening and characterization of mutations in isoniazid-resistant Mycobacterium tuberculosis isolates obtained in Brazil. Antimicrob. Agents Chemother. 48, 3373-3381.
14. Loewen, P. C., and Stauffer, G. V. (1990) Nucleotide sequence of katG of Salmonella typhimurium LT2 and characterization of its product, hydroperoxidase I. Mol. Gen. Genet. 224, 147-151.
15. Johnsson, K., Froland, W. A., and Schultz, P. G. (1997) Overexpression, purification, and characterization of the catalase-peroxidase KatG from Mycobacterium tuberculosis. J. Biol. Chem. 272, 2834-2840.
16. Chouchane, S., Lippai, I., and Magliozzo, R. S. (2000) Catalase-peroxidase (Mycobacterium tuberculosis KatG) catalysis and isoniazid activation. Biochemistry 39, 9975-9983.
17. Zhou, Y., Bowler, B. E., Lynch, K., Eaton, S. S., and Eaton, G. R. (2000) Interspin distances in spin-labeled metmyoglobin variants determined by saturation recovery EPR. Biophys. J. 79, 1039-1052.
18. Aasa, R., and Vanngard, T. (1975) EPR signal intensity and powder shapes: A reexamination. J. Magn. Reson. 19, 308-315.
19. Wengenack, N. L., Todorovic, S., Yu, L., and Rusnak, F. (1998) Evidence for differential binding of isoniazid by Mycobacterium tuberculosis KatG and the isoniazid-resistant mutant KatG(S315T). Biochemistry 37, 15825-15834.
20. 15N substituted derivatives. II. A normal coordinate analysis. J. Chem. Phys. 69, 4526-4534.
21. Choi, S., Lee, J. J., Wei, Y. H., and Spiro, T. G. (1983) J. Am. Chem. Soc. 105, 3692-3707.
22. Choi, S., and Spiro, T. G. (1983) J. Am. Chem. Soc. 105, 3683-3692.
23. Heering, H. A., Jansen, M. A., Thorneley, R. N., and Smulevich, G. (2001) Cationic ascorbate peroxidase isoenzyme II from tea: structural insights into the heme pocket of a unique hybrid peroxidase. Biochemistry 40, 10360-10370.
24. Chouchane, S., Girotto, S., Kapetanaki, S., Schelvis, J. P., Yu, S., and Magliozzo, R. S. (2003) Analysis of heme structural heterogeneity in Mycobacterium tuberculosis catalase-peroxidase (KatG). J. Biol. Chem. 278, 8154-8162.
25. Kapetanaki, S. M., Chouchane, S., Yu, S., Magliozzo, R. S., and Schelvis, J. P. (2005) Resonance Raman spectroscopy of Compound II and its decay in Mycobacterium tuberculosis catalase-peroxidase KatG and its isoniazid resistant mutant S315T. J. Inorg. Biochem. 99, 1401-1406.
26. Indiani, C., Feis, A., Howes, B. D., Marzocchi, M. P., and Smulevich, G. (2000) Benzohydroxamic acid-peroxidase complexes: spectroscopic characterization of a novel heme spin species. J. Am. Chem. Soc. 122, 7368-7376.
27. Howes, B. D., Schiodt, C. B., Welinder, K. G., Marzocchi, M. P., Ma, J. G., Zhang, J., Shelnutt, J. A., and Smulevich, G. (1999) The quantum mixed-spin heme state of barley peroxidase: A paradigm for class III peroxidases. Biophys. J. 77, 478-492.
28. 2O distance of 2.6 Å can correspond to hexa-coordinate high-spin heme. J. Biol. Inorg. Chem. 4, 39-47.
29. Jentzen, W., Ma, J. G., and Shelnutt, J. A. (1998) Conservation of the conformation of the porphyrin macrocycle in hemoproteins. Biophys. J. 74, 753-763.
30. Maltempo, M. M., Moss, T. H., and Cusanovich, M. A. (1974) Magnetic studies on the changes in the iron environment in chromatium ferricytochrome c′. Biochim. Biophys. Acta 342, 290-305.
31. Obinger, C., Regelsberger, G., Strasser, G., Burner, U., and Peschek, G. A. (1997) Purification and characterization of a homodimeric catalase-peroxidase from the cyanobacterium Anacystis nidulans. Biochem. Biophys. Res. Commun. 235, 545-552.
32. Engleder, M., Regelsberger, G., Jakopitsch, C., FurtmuUer, P. G., Ruker, F., Peschek, G. A., and Obinger, C. (2000) Nucleotide sequence analysis, overexpression in Escherichia coli and kinetic characterization of Anacystis nidulans catalase-peroxidase. Biochimie 82, 211-219.
33. Erman, J. E. (1974) Kinetic and equilibrium studies of cyanide binding by cytochrome c peroxidase. Biochemistry 13, 39-44.
34. Bidwai, A., Witt, M., Foshay, M., Vitello, L. B., Satterlee, J. D., and Erman, J. E. (2003) Cyanide binding to cytochrome c peroxidase (H52L). Biochemistry 42, 10764-10771.
35. Foshay, M. C., Vitello, L. B., and Erman, J. E. (2004) pH Dependence of heme iron coordination, hydrogen peroxide reactivity, and cyanide binding in cytochrome c peroxidase (H52K). Biochemistry 43, 5065-5072.
36. Jakopitsch, C., Auer, M., Regelsberger, G., Jantschko, W., Furtmuller, P. G., Ruker, F., and Obinger, C. (2003) Distal site aspartate is essential in the catalase activity of catalase-peroxidases. Biochemistry 42, 5292-5300.
37. Indiani, C., Feis, A., Howes, B. D., Marzocchi, M. P., and Smulevich, G. (2000) Effect of low temperature on soybean peroxidase: spectroscopic characterization of the quantum-mechanically admixed spin state. J. Inorg. Biochem. 79, 269-274.
38. Jakopitsch, C., Droghetti, E., Schmuckenschlager, F., Furtmuller, P. G., Smulevich, G., and Obinger, C. (2005) Role of the main access channel of catalase-peroxidase in catalysis. J. Biol. Chem. 280, 42411-42422.
39. Zhao, X., Yu, S., and Magliozzo, R. S. (2007) Characterization of the binding of isoniazid and analogues to Mycobacterium tuberculosis catalase-peroxidase. Biochemistry 46, 3161-3170.
40. Brancaccio, A., Cutruzzola, F., Allocatelli, C. T., Brunori, M., Smerdon, S. J., Wilkinson, A. J., Dou, Y., Keenan, D., Ikeda-Saito, M., Brantley, R. E., Jr., et al. (1994) Structural factors governing azide and cyanide binding to mammalian metmyoglobins. J. Biol. Chem. 269, 13843-13853.
41. Derat, E., Shaik, S., Rovira, C., Vidossich, P., and Alfonso-Prieto, M. (2007) The effect of a water molecule on the mechanism of formation of compound 0 in horseradish peroxidase. J. Am. Chem. Soc. 129, 6346-6347.
42. Jones, P., and Dunford, H. B. (2005) The mechanism of Compound I formation revisited. J. Inorg. Biochem. 99, 2292-2298.
43. Jones, P. (2001) Roles of water in heme peroxidase and catalase mechanisms. J. Biol. Chem. 276, 13791-13796.
44. Rao, P. K., Roxas, B. A., and Li, Q. (2008) Determination of global protein turnover in stressed mycobacterium cells using hybrid-linear ion trap-fourier transform mass spectrometry. Anal. Chem. 80, 396-406.