Abstract:
Cytochrome c (Cyt-c) has been previously shown to participate in cardiolipin (CL) oxidation and, therefore, in mitochondrial membrane permeabilization during the early events of apoptosis. The gain in this function has been ascribed to specific CL/Cyt-c interactions. Here we report that the cationic protein Cyt-c is also able to interact electrostatically with the main lipid components of the mitochondrial membranes, the zwitterionic lipids phosphatidylcholine (PC) and phosphatidylethanolamine (PE), through the mediation of phosphate anions that bind specifically to amino groups in the surfaces of protein and model membranes. In these complexes, Cyt-c reacts efficiently with H 2 O 2 at submillimolar levels, which oxidizes the sulfur atom of the axial ligand Met80. The modified protein is stable and presents significantly enhanced peroxidatic activity. Based on these results, we postulate that the rise of H 2 O 2 concentrations to the submillimolar levels registered during initiation of the apoptotic program may represent one signaling event that triggers the gain in peroxidatic function of the Cyt-c molecules bound to the abundant PE and PC membrane components. As the activated protein is a chemically stable species, it can potentially bind and oxidize important targets, such as CL. This journal is © The Royal Society of Chemistry.
Registro:
Documento: |
Artículo
|
Título: | Specific methionine oxidation of cytochrome c in complexes with zwitterionic lipids by hydrogen peroxide: Potential implications for apoptosis |
Autor: | Capdevila, D.A.; Marmisollé, W.A.; Tomasina, F.; Demicheli, V.; Portela, M.; Radi, R.; Murgida, D.H. |
Filiación: | Departamento de Química Inorgánica, Analítica y Química Física, Facultad de Ciencias Exactas y Naturales, Ciudad Universitaria, Pab. 2, piso 1, Buenos Aires, C1428EHA, Argentina Departamento de Bioquímica, Center for Free Radical and Biomedical Research, Universidad de la República, Montevideo, Uruguay Unidad de Bioquímica y Proteómica Analíticas, Institut Pasteur de Montevideo, Montevideo, Uruguay
|
Palabras clave: | Amino acids; Bins; Cell death; Cell membranes; Lipids; Mitochondria; Oxidation; Phospholipids; Proteins; Activated proteins; Cationic proteins; Membrane components; Methionine oxidation; Mitochondrial membranes; Phosphatidylcholine; Phosphatidylethanolamine; Zwitterionic lipids; C (programming language) |
Año: | 2015
|
Volumen: | 6
|
Número: | 1
|
Página de inicio: | 705
|
Página de fin: | 713
|
DOI: |
http://dx.doi.org/10.1039/c4sc02181a |
Título revista: | Chemical Science
|
Título revista abreviado: | Chem. Sci.
|
ISSN: | 20416520
|
CODEN: | CSHCC
|
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20416520_v6_n1_p705_Capdevila |
Referencias:
- Scott, R.A., Mauk, A.G., Cytochrome c: A multidisciplinary approach (1995) Univ Science Books, , Sausalito, California
- Hüttemann, M., Pecina, P., Rainbolt, M., Sanderson, T.H., Kagan, V.E., Samavati, L., Doan, J.W., Lee, I., (2011) Mitochondrion, 11, p. 369
- Liu, X., Kim, C.N., Yang, J., Jemmerson, R., Wang, X., (1996) Cell, 86, p. 147
- Kushnareva, Y., Newmeyer, D., (2010) Ann. N. Y. Acad. Sci., 50, p. 1201
- Caroppi, R., Sinibaldi, P., Fiorucci, F., Santucci, L., (2009) Curr. Med. Chem., 16, p. 4058
- Jiang, X., Wang, X., (2004) Annu. Rev. Biochem., 73, p. 87
- Kulikov, A.V., Shilov, E.S., Mufazalov, I.A., Gogvadze, V., Nedospasov, S.A., Zhivotovsky, B., (2012) Cell. Mol. Life Sci., 69, p. 1787
- Garrido, C., Galluzzi, L., Brunet, M., Puig, P.E., Didelot, C., Kroemer, G., (2006) Cell Death Differ., 13, p. 1423
- Gogvadze, V., Orrenius, S., Zhivotovsky, B., (2006) Biochim. Biophys. Acta, 1757, p. 639
- Kagan, V.E., Tyurin, V.A., Jiang, J., Tyurina, Y.Y., Ritov, V.B., Amoscato, A.A., Osipov, A.N., Borisenko, G.G., (2005) Nat. Chem. Biol., 1, p. 223
- Kagan, V.E., Bayir, H.A., Belikova, N.A., Kapralov, O., Tyurina, Y.Y., Tyurin, V.A., Jiang, J., Borisenko, G., (2009) Free Radicals Biol. Med., 46, p. 1439
- Ascenzi, P., Ciaccio, C., Sinibaldi, F., Santucci, R., Coletta, M., (2011) Biochem. Biophys. Res. Commun., 404, p. 190
- Ascenzi, P., Santucci, R., Coletta, M., Polticelli, F., (2010) Biophys. Chem., 152, p. 21
- Trusova, V.M., Gorbenko, G.P., Molotkovsky, J.G., Kinnunen, P.K.J., (2010) Biophys. J., 99, p. 1754
- Macchioni, L., Corazzi, T., Davidescu, M., Francescangeli, E., Roberti, R., Corazzi, L., (2010) Mol. Cell. Biochem., 341, p. 149
- Sinibaldi, F., Howes, B.D., Piro, M.C., Polticelli, F., Bombelli, C., Ferri, T., Coletta, M., Santucci, R., (2010) JBIC, J. Biol. Inorg. Chem., 15, p. 689
- Hanske, J., Toffey, J.R., Morenz, A.M., Bonilla, A.J., Schiavoni, K.H., Pletneva, E.V., (2012) Proc. Natl. Acad. Sci. U. S. A., 109, p. 125
- Bergstrom, C.L., Beales, P.A., Lv, Y., Vanderlick, T.K., Groves, J.T., (2013) Proc. Natl. Acad. Sci. U. S. A., 110, p. 6269
- Vladimirov, Y.A., Proskurnina, E.V., Alekseev, A.V., (2013) Biokhim., Biochem., 78, p. 1086
- Bradley, J.M., Silkstone, G., Wilson, M.T., Cheesman, M.R., Butt, J.N., (2011) J. Am. Chem. Soc., 133, p. 19676
- Iverson, S.L., Orrenius, S., (2004) Arch. Biochem. Biophys., 423, p. 37
- Ow, Y.-L.P., Green, D.R., Hao, Z., Mak, T.W., (2008) Nat. Rev. Mol. Cell Biol., 9, p. 532
- Belikova, N., Vladimirov, Y., (2006) Biochemistry, 45, p. 4998
- Kalanxhi, E., Wallace, C.J.A., (2007) Biochem. J., 407, p. 179
- Osman, C., Voelker, D.R., Langer, T., (2011) J. Cell Biol., 192, p. 7
- Ardail, D., Privat, J., Egret-Charlier, M., (1990) J. Biol. Chem., 265, p. 18797
- Gebert, N., Joshi, A.S., Kutik, S., Becker, T., McKenzie, M., Guan, X.L., Mooga, V.P., Pfanner, N., (2009) Curr. Biol., 19, p. 2133
- Garcia Fernandez, M., Troiano, L., Moretti, L., Nasi, M., Pinti, M., Salvioli, S., Dobrucki, J., Cossarizza, A., (2002) Cell Growth Differ., 13, p. 449
- Schug, Z.T., Gottlieb, E., (2009) Biochim. Biophys. Acta, 1788, p. 2022
- Montero, J., Mari, M., Colell, A., Morales, A., Basañez, G., Garcia-Ruiz, C., Fernández-Checa, J.C., (2010) Biochim. Biophys. Acta, 1797, p. 1217
- Schlame, M., Rua, D., Greenberg, M.L., (2000) Prog. Lipid Res., 39, p. 257
- Kagan, V.E., Borisenko, G.G., Tyurina, Y.Y., Tyurin, V.A., Jiang, J., Potapovich, A.I., Kini, V., Fujii, Y., (2004) Free Radicals Biol. Med., 37, p. 1963
- Salamon, Z., Tollin, G., (1996) Biophys. J., 71, p. 848
- Ahn, T., Oh, D.B., Lee, B.C., Yun, C.H., (2000) Biochemistry, 39, p. 10147
- Capdevila, D.A., Marmisollé, W.A., Williams, F.J., Murgida, D.H., (2013) Phys. Chem. Chem. Phys., 15, p. 5386
- Marmisollé, W.A., Capdevila, D.A., De La Llave, E., Williams, F.J., Murgida, D.H., (2013) Langmuir, 29, p. 5351
- Giorgio, M., Trinei, M., Migliaccio, E., Pelicci, P.G., (2007) Nat. Rev. Mol. Cell Biol., 8, p. 722
- Cerella, C., Coppola, S., Maresca, V., De Nicola, M., Radogna, F., Ghibelli, L., (2009) Ann. N. Y. Acad. Sci., 1171, p. 559
- Godoy, L.C., Muñoz-Pinedo, C., Castro, L., Cardaci, S., Schonhoff, C.M., King, M., Tórtora, V., Mannick, J.B., (2009) Proc. Natl. Acad. Sci. U. S. A., 106, p. 2653
- Murgida, D.H., Hildebrandt, P., (2001) J. Phys. Chem. B, 105, p. 1578
- Lee, S.-H., Lin, W.-C., Kuo, C.-H., Karakachian, M., Lin, Y.-C., Yu, B.-Y., Shyue, J.-J., (2010) J. Phys. Chem. C, 114, p. 10512
- Chen, Y.-R., Deterding, L.J., Sturgeon, B.E., Tomer, K.B., Mason, R.P., (2002) J. Biol. Chem., 277, p. 29781
- Pande, J., Kinnally, K., Thallum, K.K., Verma, B., Myer, Y., Rechsteiner, L., Bosshard, H., (1987) J. Protein Chem., 6, p. 295
- Valderrama, B., Ayala, M., Vazquez-Duhalt, R., (2002) Chem. Biol., 9, p. 555
- Wang, L., Waldeck, D.H., (2008) J. Phys. Chem. C, 112, p. 1351
- Alvarez-Paggi, D., Martín, D.F., Debiase, P.M., Hildebrandt, P., Martí, M.A., Murgida, D.H., (2010) J. Am. Chem. Soc., 132, p. 5769
- Chen, X., Ferrigno, R., Yang, J., Whitesides, G.M., (2002) Langmuir, 18, p. 7009
- Murgida, D.H., Hildebrandt, P., (2004) Acc. Chem. Res., 37, p. 854
- Battistuzzi, G., Borsari, M., Cowan, J.A., Ranieri, A., Sola, M., (2002) J. Am. Chem. Soc., 124, p. 5315
- Murgida, D.H., Hildebrandt, P., (2008) Chem. Soc. Rev., 37, p. 937
- Battistuzzi, G., Bortolotti, C.A., Bellei, M., Di Rocco, G., Salewski, J., Hildebrandt, P., Sola, M., (2012) Biochemistry, 51, p. 5967
- Cohen, G., Heikkila, R., (1974) J. Biol. Chem., 249, p. 2447
- Scaduto, R.C., (1995) Free Radicals Biol. Med., 18, p. 271
- Steiner, M.G., Babbs, C.F., (1990) Arch. Biochem. Biophys., 278, p. 478
- Tai, C., Peng, J.-F., Liu, J.-F., Jiang, G.-B., Zou, H., (2004) Anal. Chim. Acta, 527, p. 73
- Wang, B., Zhang, J.-J., Pan, Z.-Y., Tao, X.-Q., Wang, H.-S., (2009) Biosens. Bioelectron., 24, p. 1141
- Vogt, W., (1995) Free Radicals Biol. Med., 18, pp. 93-105
- Valderrama, B., Vazquez-Duhalt, R., (2005) J. Mol. Catal. B: Enzym., 35, p. 41
- Thariat, J., Collin, F., Marchetti, C., Ahmed-Adrar, N.S., Vitrac, H., Jore, D., Gardes-Albert, M., (2008) Biochimie, 90, p. 1442
- Casalini, S., Battistuzzi, G., Borsari, M., Bortolotti, C.A., Di Rocco, G., Ranieri, A., Sola, M., (2010) J. Phys. Chem. B, 114, p. 1698
- Águila, S., Vidal-Limón, A.M., Alderete, J.B., Sosa-Torres, M., Vázquez-Duhalt, R., (2013) J. Mol. Catal. B: Enzym., 85-86, p. 187
- Battistuzzi, G., Bellei, M., Bortolotti, C.A., Sola, M., (2010) Arch. Biochem. Biophys., 500, p. 21
- Radi, R., Thomson, L., Rubbo, H., Prodanov, E., (1991) Arch. Biochem. Biophys., 288, p. 112
- Chen, X., Ferrigno, R., Yang, J., Whitesides, G., (2002) Langmuir, p. 7009
- Ranieri, A., Bernini, F., Bortolotti, C.A., Castellini, E., (2012) Catal. Sci. Technol., 2, p. 2206
Citas:
---------- APA ----------
Capdevila, D.A., Marmisollé, W.A., Tomasina, F., Demicheli, V., Portela, M., Radi, R. & Murgida, D.H.
(2015)
. Specific methionine oxidation of cytochrome c in complexes with zwitterionic lipids by hydrogen peroxide: Potential implications for apoptosis. Chemical Science, 6(1), 705-713.
http://dx.doi.org/10.1039/c4sc02181a---------- CHICAGO ----------
Capdevila, D.A., Marmisollé, W.A., Tomasina, F., Demicheli, V., Portela, M., Radi, R., et al.
"Specific methionine oxidation of cytochrome c in complexes with zwitterionic lipids by hydrogen peroxide: Potential implications for apoptosis"
. Chemical Science 6, no. 1
(2015) : 705-713.
http://dx.doi.org/10.1039/c4sc02181a---------- MLA ----------
Capdevila, D.A., Marmisollé, W.A., Tomasina, F., Demicheli, V., Portela, M., Radi, R., et al.
"Specific methionine oxidation of cytochrome c in complexes with zwitterionic lipids by hydrogen peroxide: Potential implications for apoptosis"
. Chemical Science, vol. 6, no. 1, 2015, pp. 705-713.
http://dx.doi.org/10.1039/c4sc02181a---------- VANCOUVER ----------
Capdevila, D.A., Marmisollé, W.A., Tomasina, F., Demicheli, V., Portela, M., Radi, R., et al. Specific methionine oxidation of cytochrome c in complexes with zwitterionic lipids by hydrogen peroxide: Potential implications for apoptosis. Chem. Sci. 2015;6(1):705-713.
http://dx.doi.org/10.1039/c4sc02181a