Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Alkyl hydroperoxide reductase E (AhpE), a novel subgroup of the peroxiredoxin family, comprises Mycobacterium tuberculosis AhpE (MtAhpE) and AhpE-like proteins present in many bacteria and archaea, for which functional characterization is scarce. We previously reported that MtAhpE reacted ~ 10 3 times faster with peroxynitrite than with hydrogen peroxide, but the molecular reasons for that remained unknown. Herein, we investigated the oxidizing substrate specificity and the oxidative inactivation of the enzyme. In most cases, both peroxidatic thiol oxidation and sulfenic acid overoxidation followed a trend in which those peroxides with the lower leaving-group pK a reacted faster than others. These data are in agreement with the accepted mechanisms of thiol oxidation and support that overoxidation occurs through sulfenate anion reaction with the protonated peroxide. However, MtAhpE oxidation and overoxidation by fatty acid-derived hydroperoxides (~ 10 8 and 10 5 M - 1 s - 1, respectively, at pH 7.4 and 25 °C) were much faster than expected according to the Brønsted relationship with leaving-group pK a. A stoichiometric reduction of the arachidonic acid hydroperoxide 15-HpETE to its corresponding alcohol was confirmed. Interactions of fatty acid hydroperoxides with a hydrophobic groove present on the reduced MtAhpE surface could be the basis of their surprisingly fast reactivity. © 2011 Elsevier Inc.

Registro:

Documento: Artículo
Título:Oxidizing substrate specificity of Mycobacterium tuberculosis alkyl hydroperoxide reductase E: Kinetics and mechanisms of oxidation and overoxidation
Autor:Reyes, A.M.; Hugo, M.; Trostchansky, A.; Capece, L.; Radi, R.; Trujillo, M.
Filiación:Departamento de Bioquímica, Universidad de la República, 11800 Montevideo, Uruguay
Center for Free Radical and Biomedical Research, Universidad de la República, 11800 Montevideo, Uruguay
Departamento de Química Inorgánica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Bioquímica and Center for Free Radical and Biomedical Research, Universidad de la República, General Flores 2125, 11800 Montevideo, Uruguay
Palabras clave:Alkyl hydroperoxide reductase E; Arachidonic acid; Free radicals; Hydroperoxide; Mycobacterium tuberculosis; Peroxidase; Peroxiredoxin; alcohol; alkyl hydroperoxide reductase E; arachidonic acid; hydroperoxide; peroxiredoxin; sulfenic acid derivative; thiol; unclassified drug; article; enzyme inactivation; enzyme specificity; hydrophobicity; kinetics; Mycobacterium tuberculosis; nonhuman; oxidation; priority journal; proton transport; stoichiometry; Chromatography, Liquid; Kinetics; Mycobacterium tuberculosis; Oxidation-Reduction; Peroxiredoxins; Substrate Specificity; Tandem Mass Spectrometry; Mycobacterium tuberculosis
Año:2011
Volumen:51
Número:2
Página de inicio:464
Página de fin:473
DOI: http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.023
Título revista:Free Radical Biology and Medicine
Título revista abreviado:Free Radic. Biol. Med.
ISSN:08915849
CODEN:FRBME
CAS:alcohol, 64-17-5; arachidonic acid, 506-32-1, 6610-25-9, 7771-44-0; peroxiredoxin, 207137-51-7; Peroxiredoxins, 1.11.1.15
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_08915849_v51_n2_p464_Reyes

Referencias:

  • Andersen, P., Vaccine strategies against latent tuberculosis infection (2007) Trends in Microbiology, 15 (1), pp. 7-13. , DOI 10.1016/j.tim.2006.11.008, PII S0966842X06002733
  • Brandt, L., Cunha, J.F., Olsen, A.W., Chilima, B., Hirsch, P., Appelberg, R., Andersen, P., Failure of the Mycobacterium bovis BCG vaccine: Some species of environmental mycobacteria block multiplication of BCG and induction of protective immunity to tuberculosis (2002) Infection and Immunity, 70 (2), pp. 672-678. , DOI 10.1128/IAI.70.2.672-678.2002
  • Harries, A.D., Zachariah, R., Corbett, E.L., Lawn, S.D., Santos-Filho, E.T., Chimzizi, R., Harrington, M., De Cock, K.M., The HIV-associated tuberculosis epidemic-when will we act? (2010) Lancet, 375, pp. 1906-1919
  • Kaye, K., Frieden, T.R., Tuberculosis control: The relevance of classic principles in an era of acquired immunodeficiency syndrome and multidrug resistance (1996) Epidemiologic Reviews, 18 (1), pp. 52-63
  • Meena, L.S., Rajni, Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv (2010) FEBS J., 277, pp. 2416-2427
  • Yoshida, A., Inagawa, H., Kohchi, C., Nishizawa, T., Soma, G., The role of toll-like receptor 2 in survival strategies of Mycobacterium tuberculosis in macrophage phagosomes (2009) Anticancer Res., 29, pp. 907-910
  • Rajavelu, P., Das, S.D., A correlation between phagocytosis and apoptosis in THP-1 cells infected with prevalent strains of Mycobacterium tuberculosis (2007) Microbiology and Immunology, 51 (2), pp. 201-210. , http://www.jstage.jst.go.jp/article/mandi/51/2/201/_pdf
  • Fang, F.C., Antimicrobial reactive oxygen and nitrogen species: Concepts and controversies (2004) Nature Reviews Microbiology, 2 (10), pp. 820-832. , DOI 10.1038/nrmicro1004
  • Nathan, C., Shiloh, M.U., Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens (2000) Proceedings of the National Academy of Sciences of the United States of America, 97 (16), pp. 8841-8848. , DOI 10.1073/pnas.97.16.8841
  • Alvarez, M.N., Peluffo, G., Piacenza, L., Radi, R., Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: Consequences for oxidative killing and role of microbial peroxiredoxins in infectivity (2011) J. Biol. Chem., 286, pp. 6627-6640
  • Radi, R., Beckman, J.S., Bush, K.M., Freeman, B.A., Peroxynitrite-induced membrane lipid peroxidation: The cytotoxic potential of superoxide and nitric oxide (1991) Arch. Biochem. Biophys., 288, pp. 481-487
  • Porter, N.A., Caldwell, S.E., Mills, K.A., Mechanisms of free radical oxidation of unsaturated lipids (1995) Lipids, 30, pp. 277-290
  • Lewis, J.G., Hamilton, T., Adams, D.O., The effect of macrophage development on the release of reactive oxygen intermediates and lipid oxidation products, and their ability to induce oxidative DNA damage in mammalian cells (1986) Carcinogenesis, 7 (5), pp. 813-818
  • Bonney, R.J., Opas, E.E., Humes, J.L., Lipoxygenase pathways of macrophages (1985) Federation Proceedings, 44 (14), pp. 2933-2936
  • Sevanian, A., Wratten, M.L., McLeod, L.L., Kim, E., Lipid peroxidation and phospholipase A2 activity in liposomes composed of unsaturated phospholipids: A structural basis for enzyme activation (1988) Biochim. Biophys. Acta, 961, pp. 316-327
  • Evans, M.V., Turton, H.E., Grant, C.M., Dawes, I.W., Toxicity of linoleic acid hydroperoxide to Saccharomyces cerevisiae: Involvement of a respiration-related process for maximal sensitivity and adaptive response (1998) Journal of Bacteriology, 180 (3), pp. 483-490
  • Wang, G., Hong, Y., Johnson, M.K., Maier, R.J., Lipid peroxidation as a source of oxidative damage in Helicobacter pylori: Protective roles of peroxiredoxins (2006) Biochimica et Biophysica Acta - General Subjects, 1760 (11), pp. 1596-1603. , DOI 10.1016/j.bbagen.2006.05.005, PII S0304416506001383
  • Jaeger, T., Budde, H., Flohe, L., Menge, U., Singh, M., Trujillo, M., Radi, R., Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis (2004) Archives of Biochemistry and Biophysics, 423 (1), pp. 182-191. , DOI 10.1016/j.abb.2003.11.021
  • Hu, Y., Coates, A.R., Acute and persistent Mycobacterium tuberculosis infections depend on the thiol peroxidase TpX (2009) PLoS One, 4, p. 5150
  • Master, S.S., Springer, B., Sander, P., Boettger, E.C., Deretic, V., Timmins, G.S., Oxidative stress response genes in Mycobacterium tuberculosis: Role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages (2002) Microbiology, 148 (10), pp. 3139-3144
  • Manca, C., Paul, S., Barry III, C.E., Freedman, V.H., Kaplan, G., Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro (1999) Infection and Immunity, 67 (1), pp. 74-79
  • Zhang, Y., Heym, B., Allen, B., Young, D., Cole, S., The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis (1992) Nature, 358, pp. 591-593
  • Sherman, D.R., Mdluli, K., Hickey, M.J., Arain, T.M., Morris, S.L., Barry III, C.E., Stover, C.K., Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis (1996) Science, 272 (5268), pp. 1641-1643
  • Jaeger, T., Peroxiredoxin systems in mycobacteria (2007) Subcell. Biochem., 44, pp. 207-217
  • Gu, S., Chen, J., Dobos, K.M., Bradbury, E.M., Belisle, J.T., Chen, X., Comprehensive proteomic profiling of the membrane constituents of a Mycobacterium tuberculosis strain (2003) Mol. Cell. Proteomics, 2, pp. 1284-1296
  • Oliva, M., Theiler, G., Zamocky, M., Koua, D., Margis-Pinheiro, M., Passardi, F., Dunand, C., PeroxiBase: A powerful tool to collect and analyse peroxidase sequences from Viridiplantae (2009) J. Exp. Bot., 60, pp. 453-459
  • Soito, L., Williamson, C., Knutson, S.T., Fetrow, J.S., Poole, L.B., Nelson, K.J., PREX: PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family (2010) Nucleic Acids Res., 39, pp. 332-D337
  • Murphy, D.J., Brown, J.R., Identification of gene targets against dormant phase Mycobacterium tuberculosis infections (2007) BMC Infect. Dis., 7, p. 84
  • Li, S., Peterson, N.A., Kim, M.-Y., Kim, C.-Y., Hung, L.-W., Yu, M., Lekin, T., Baker, E.N., Crystal structure of AhpE from Mycobacterium tuberculosis, a 1-Cys peroxiredoxin (2005) Journal of Molecular Biology, 346 (4), pp. 1035-1046. , DOI 10.1016/j.jmb.2004.12.046
  • Hugo, M., Turell, L., Manta, B., Botti, H., Monteiro, G., Netto, L.E., Alvarez, B., Trujillo, M., Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: Kinetics, acidity constants, and conformational dynamics (2009) Biochemistry, 48, pp. 9416-9426
  • Trujillo, M., Clippe, A., Manta, B., Ferrer-Sueta, G., Smeets, A., Declercq, J.-P., Knoops, B., Radi, R., Pre-steady state kinetic characterization of human peroxiredoxin 5: Taking advantage of Trp84 fluorescence increase upon oxidation (2007) Archives of Biochemistry and Biophysics, 467 (1), pp. 95-106. , DOI 10.1016/j.abb.2007.08.008, PII S000398610700402X
  • Manta, B., Hugo, M., Ortiz, C., Ferrer-Sueta, G., Trujillo, M., Denicola, A., The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2 (2009) Arch. Biochem. Biophys., 484, pp. 146-154
  • Ogusucu, R., Rettori, D., Munhoz, D.C., Soares Netto, L.E., Augusto, O., Reactions of yeast thioredoxin peroxidases I and II with hydrogen peroxide and peroxynitrite: Rate constants by competitive kinetics (2007) Free Radical Biology and Medicine, 42 (3), pp. 326-334. , DOI 10.1016/j.freeradbiomed.2006.10.042, PII S0891584906006733
  • Parsonage, D., Karplus, P.A., Poole, L.B., Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin (2008) Proceedings of the National Academy of Sciences of the United States of America, 105 (24), pp. 8209-8214. , http://www.pnas.org/cgi/reprint/105/24/8209, DOI 10.1073/pnas.0708308105
  • Trindade, D.F., Cerchiaro, G., Augusto, O., A role for peroxymonocarbonate in the stimulation of biothiol peroxidation by the bicarbonate/carbon dioxide pair (2006) Chemical Research in Toxicology, 19 (11), pp. 1475-1482. , DOI 10.1021/tx060146x
  • Maskrey, B.H., Bermudez-Fajardo, A., Morgan, A.H., Stewart-Jones, E., Dioszeghy, V., Taylor, G.W., Baker, P.R.S., O'Donnell, V.B., Activated platelets and monocytes generate four hydroxyphosphatidylethanolamines via lipoxygenase (2007) Journal of Biological Chemistry, 282 (28), pp. 20151-20163. , http://www.jbc.org/cgi/reprint/282/28/20151, DOI 10.1074/jbc.M611776200
  • Pryor, W.A., Castle, L., Chemical methods for the detection of lipid hydroperoxides (1984) Methods in Enzymology, 105, pp. 293-299
  • Ellman, G.L., Tissue sulfhydryl groups (1959) Arch. Biochem. Biophys., 82, pp. 70-77
  • Trujillo, M., Radi, R., Peroxynitrite reaction with the reduced and the oxidized forms of lipoic acid: New insights into the reaction of peroxynitrite with thiols (2002) Archives of Biochemistry and Biophysics, 397 (1), pp. 91-98. , DOI 10.1006/abbi.2001.2619
  • Jiang, Z.Y., Hunt, J.V., Wolff, S.P., Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein (1992) Anal. Biochem., 202, pp. 384-389
  • Jiang, Z.Y., Woollard, A.C., Wolff, S.P., Lipid hydroperoxide measurement by oxidation of Fe 2+ in the presence of xylenol orange: Comparison with the TBA assay and an iodometric method (1991) Lipids, 26, pp. 853-856
  • Humphrey, W., Dalke, A., Schulten, K., VMD: Visual molecular dynamics (1996) Journal of Molecular Graphics, 14 (1), pp. 33-38. , DOI 10.1016/0263-7855(96)00018-5
  • Richardson, W.H., Hodge, V.F., Acidities of tertiary alkyl hydroperoxides (1970) J. Org. Chem., 35, pp. 4012-4016
  • Richardson, D.E., Yao, H., Frank, K.M., Bennett, D.A., Equilibria, kinetics, and mechanism in the bicarbonate activation of hydrogen peroxide: Oxidation of sulfides by peroxymonocarbonate (2000) Journal of the American Chemical Society, 122 (8), pp. 1729-1739. , DOI 10.1021/ja9927467
  • Davies, D.M., Jones, P., Mantle, D., The kinetics of formation of horseradish peroxidase compound i by reaction with peroxobenzoic acids: PH and peroxo acid substituent effects (1976) Biochem. J., 157, pp. 247-253
  • Winterbourn, C.C., Metodiewa, D., Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide (1999) Free Radical Biology and Medicine, 27 (3-4), pp. 322-328. , DOI 10.1016/S0891-5849(99)00051-9, PII S0891584999000519
  • Hall, A., Parsonage, D., Poole, L.B., Karplus, P.A., Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization (2010) J. Mol. Biol., 402, pp. 194-209
  • Perrin, D., Ionisation constants of inorganic acids and bases in aqueous solution (1984) IUPAC Chemical Data Series, , Pergamon Press Oxford
  • Ali, S.T., Karamat, S., Kona, J., Fabian, W.M., Theoretical prediction of pK(a) values of seleninic, selenenic, sulfinic, and carboxylic acids by quantum-chemical methods (2010) J. Phys. Chem. A, 114, pp. 12470-12478
  • Ursini, F., Maiorino, M., Gregolin, C., The selenoenzyme phospholipid hydroperoxide glutathione peroxidase (1985) Biochimica et Biophysica Acta - General Subjects, 839 (1), pp. 62-70. , DOI 10.1016/0304-4165(85)90182-5
  • Soonsanga, S., Lee, J.-W., Helmann, J.D., Oxidant-dependent switching between reversible and sacrificial oxidation pathways for Bacillus subtilis OhrR (2008) Molecular Microbiology, 68 (4), pp. 978-986. , DOI 10.1111/j.1365-2958.2008.06200.x
  • Declercq, J.-P., Evrard, C., Clippe, A., Stricht, D.V., Bernard, A., Knoops, B., Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 A resolution (2001) Journal of Molecular Biology, 311 (4), pp. 751-759. , DOI 10.1006/jmbi.2001.4853
  • Piñeyro, M.D., Arcari, T., Robello, C., Radi, R., Trujillo, M., Tryparedoxin peroxidases from Trypanosoma cruzi: High efficiency in the catalytic elimination of hydrogen peroxide and peroxynitrite (2011) Arch. Biochem. Biophys., 507, pp. 287-295
  • Bryk, R., Griffin, P., Nathan, C., Peroxynitrite reductase activity of bacterial peroxiredoxins (2000) Nature, 407, pp. 211-215
  • Akaki, T., Tomioka, H., Shimizu, T., Dekio, S., Sato, K., Comparative roles of free fatty acids with reactive nitrogen intermediates and reactive oxygen intermediates in expression of the anti-microbial activity of macrophages against Mycobacterium tuberculosis (2000) Clinical and Experimental Immunology, 121 (2), pp. 302-310. , DOI 10.1046/j.1365-2249.2000.01298.x

Citas:

---------- APA ----------
Reyes, A.M., Hugo, M., Trostchansky, A., Capece, L., Radi, R. & Trujillo, M. (2011) . Oxidizing substrate specificity of Mycobacterium tuberculosis alkyl hydroperoxide reductase E: Kinetics and mechanisms of oxidation and overoxidation. Free Radical Biology and Medicine, 51(2), 464-473.
http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.023
---------- CHICAGO ----------
Reyes, A.M., Hugo, M., Trostchansky, A., Capece, L., Radi, R., Trujillo, M. "Oxidizing substrate specificity of Mycobacterium tuberculosis alkyl hydroperoxide reductase E: Kinetics and mechanisms of oxidation and overoxidation" . Free Radical Biology and Medicine 51, no. 2 (2011) : 464-473.
http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.023
---------- MLA ----------
Reyes, A.M., Hugo, M., Trostchansky, A., Capece, L., Radi, R., Trujillo, M. "Oxidizing substrate specificity of Mycobacterium tuberculosis alkyl hydroperoxide reductase E: Kinetics and mechanisms of oxidation and overoxidation" . Free Radical Biology and Medicine, vol. 51, no. 2, 2011, pp. 464-473.
http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.023
---------- VANCOUVER ----------
Reyes, A.M., Hugo, M., Trostchansky, A., Capece, L., Radi, R., Trujillo, M. Oxidizing substrate specificity of Mycobacterium tuberculosis alkyl hydroperoxide reductase E: Kinetics and mechanisms of oxidation and overoxidation. Free Radic. Biol. Med. 2011;51(2):464-473.
http://dx.doi.org/10.1016/j.freeradbiomed.2011.04.023