Nitric oxide binding to the cardiolipin complex of ferric cytochrome

Biochemistry

Volumn 51, Issue 34, 2012, Pages 6760-6766

  Silkstone, G ^a   Kapetanaki, S M ^b   Husu, I ^a   Vos, M H ^b   Wilson, M T ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b LABORATOIRE D OPTIQUE ET BIOSCIENCES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; HYDROPHOBICITY; LIGANDS; PHOSPHOLIPIDS; PHOTOLYSIS; PORPHYRINS; PROTEINS;

APOPTOTIC ACTIVITY; CARDIOLIPINS; CONFORMATIONAL CHANGE; CYTOCHROME C; ELECTRON TRANSFER; HEME POCKETS; HEME-PROTEINS; HYDROPHOBIC INTERACTIONS; MITOCHONDRIAS; PROTEIN CYTOCHROME C;

NITRIC OXIDE;

CARDIOLIPIN; CYTOCHROME C; HEME; LIGAND; METHIONINE; NITRIC OXIDE; NITRO DERIVATIVE; SULFUR;

APOPTOSIS; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CHEMICAL BOND; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; HYDROPHOBICITY; PEROXIDATION; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION;

ANIMALS; CARDIOLIPINS; CYTOCHROMES C; HORSES; IRON; KINETICS; NITRIC OXIDE; PROTEIN BINDING;

EID: 84867550132     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300582u     Document Type: Article

References (34)

1. Iverson, S. L., and Orrenius, S. (2004) The cardiolipincytochrome c interaction and the mitochondrial regulation of apoptosis. Arch. Biochem. Biophys. 423, 37-46.
2. Basova, L. V., Kurnikov, I. V., Wang, L., Ritov, V. B., Belikova, N. A., Vlasova, I. I., Pacheco, A. A., Winnica, D. E., Peterson, J., Bayir, H., Waldeck, D. H., and Kagan, V. E. (2007) Cardiolipin Switch in Mitochondria: Shutting off the Reduction of Cytochrome c and Turning on the Peroxidase Activity. Biochemistry 46, 3423-3434.
3. Kagan, V. E., Bayir, H. A., Belikova, N. A., Kapralov, O., Tyurina, Y. Y., Tyurin, V. A., Jiang, J., Stoyanovsky, D. A., Wipf, P., Kochanek, P. M., Greenberger, J. S., Pitt, B., Shvedova, A. A., and Borisenko, G. (2009) Cytochrome c/cardiolipin relations in mitochondria: A kiss of death. Free Radical Biol. Med. 46, 1439-1453.
4. Twiddy, D., Brown, D. G., Adrain, C., Jukes, R., Martin, S. J., Cohen, G. M., MacFarlane, M., and Cain, K. (2004) Proapoptoticproteins released from the mitochondria regulate the protein composition and caspase-processing activity of the native Apaf1/ caspase-9 apoptosome complex. J. Biol. Chem. 279, 19665-19682.
5. Martin, M. C., Allan, L. A., Lickrish, M., Sampson, C., Morrice, N., and Clarke, P. R. (2005) Protein Kinase A Regulates Caspase-9 Activation by Apaf-1 Downstream of Cytochrome c. J. Biol. Chem. 280, 15449-15455.
6. Hancock, J. T., Desikan, R., and Neill, S. J. (2001) Does the redox status of cytochrome c act as a fail-safe mechanism in the regulation of programmed cell death? Free Radical Biol. Med. 31, 697-703.
7. Brown, G. C., and Borutaite, V. (2008) Regulation of apoptosis by the redox state of cytochrome c. Biochim. Biophys. Acta 1777, 877-881.
8. Chung, H. T., Pae, H. O., Choi, B. M., Billiar, T. R., and Kim, Y. M. (2001) Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 282, 1075-1079.
9. Bilban, M., Haschemi, A., Wegiel, B., Chin, B. Y., Wagner, O., and Otterbein, L. E. (2008) Heme oxygenase and carbon monoxide initiate homeostatic signaling. J. Mol. Med. 86, 267-279.
10. Kapetanaki, S. M., Silkstone, G., Husu, I., Liebl, U., Wilson, M. T., and Vos, M. H. (2009) Interaction of Carbon Monoxide with the Apoptosis-Inducing Cytochrome c-Cardiolpin Complex. Biochemistry 48, 1613-1619.
11. Lawson, D. M., Stevenson, C. E. M., Andrew, C. R., and Eady, R. R. (2000) Unprecedented proximal binding of nitric oxide to heme: Implications for guanylate cyclase. EMBO J. 19, 5661-5671.
12. Silkstone, G., Kapetanaki, S. M., Husu, I., Vos, M. H., and Wilson, M. T. (2010) Nitric Oxide Binds to the Proximal Heme Coordination Site of the Ferrocytochrome c/Cardiolipin Complex: Formation Mechanism and Dynamics. J. Biol. Chem. 285, 19785-19792.
13. Stone, J. R., and Marletta, M. A. (1994) Soluble Guanylate Cyclase from Bovine Lung: Activation with Nitric Oxide and Carbon Monoxide and Spectral Characterization of the Ferrous and Ferric States. Biochemistry 33, 5636-5640.
14. Yoshimura, T., Suzuki, S., Nakahara, A., Iwasaki, H., Masuko, M., and Matsubara, T. (1986) Spectral Properties of Nitric-Oxide Complexes of Cytochrome-c′ from Alcaligenes sp. Ncib 11015. Biochemistry 25, 2436-2442.
15. Vos, M. H. (2008) Ultrafast dynamics of ligands within heme proteins. Biochim. Biophys. Acta 1777, 15-31.
16. Dupre, S., Brunori, M., Wilson, M. T., and Greenwood, C. (1974) Kinetics of Carbon-Monoxide Binding and Electron-Transfer by Cytochrome-c Polymers. Biochem. J. 141, 299-304.
17. Martin, J.-L., and Vos, M. H. (1994) Femtosecond spectroscopy of ligand rebinding in heme proteins. Methods Enzymol. 232, 416-430.
18. Liebl, U., Lambry, J.-C., Leibl, W., Breton, J., Martin, J.-L., and Vos, M. H. (1996) Energy and electron transfer upon selective femtosecond excitation of pigments in membranes of Heliobacillus mobilis. Biochemistry 35, 9925-9934.
19. Yoshimura, T., and Suzuki, S. (1988) The pH-Dependence of the Stereochemistry around the Heme Group in No Cytochrome-C (Horse Heart). Inorg. Chim. Acta 152, 241-249.
20. Vlasova, I. I., Tyurin, V. A., Kapralov, A. A., Kurnikov, I. V., Osipov, A. N., Potapovich, M. V., Stoyanovsky, D. A., and Kagan, V. E. (2006) Nitric Oxide Inhibits Peroxidase Activity of Cytochrome c. Cardiolipin Complex and Blocks Cardiolipin Oxidation. J. Biol. Chem. 281, 14554-14562.
21. Cianetti, S. M. (2005) Ph.D. Thesis, University of Florence and University of Paris 6.
22. Silkstone, G., Stanway, G., Brzezinski, P., and Wilson, M. T. (2002) Production and characterisation of Met80X mutants of yeast iso-1-cytochrome c: Spectral, photochemical and binding studies on the ferrous derivatives. Biophys. Chem. 98, 65-77.
23. Petrich, J. W., Poyart, C., and Martin, J.-L. (1988) Photophysics and reactivity of heme proteins: A femtosecond absorption study of hemoglobin, myoglobin and protoheme. Biochemistry 27, 4049-4060.
24. Franzen, S., Kiger, L., Poyart, C., and Martin, J. L. (2001) Heme photolysis occurs by ultrafast excited state metal-To-ring charge transfer. Biophys. J. 80, 2372-2385.
25. Kapetanaki, S. M., Field, S. J., Hughes, R. J. L., Watmough, N. J., Liebl, U., and Vos, M. H. (2008) Ultrafast ligand binding dynamics in the active site of native bacterial nitric oxide reductase. Biochim. Biophys. Acta 1777, 919-924.
26. Hanske, J., Toffey, J. R., Morenz, A. M., Bonilla, J., Schiavoni, H., and Pletneva, E. V. (2012) Conformational properties of cardiolipinbound cytochrome c. Proc. Natl. Acad. Sci. U.S.A. 109, 125-130.
27. Hoshino, M., Ozawa, K., Seki, H., and Ford, P. C. (1993) Photochemistry of nitric oxide adducts of water-soluble iron(III) porphyrin and ferrihemoproteins studied by nanosecond laser photolysis. J. Am. Chem. Soc. 115, 9568-9575.
28. Vladimirov, Y. A., Proskurnina, E. V., Izmailov, D. Y., Novikov, A. A., Brusnichkin, A. V., Osipov, A. N., and Kagan, V. E. (2006) Mechanism of activation of cytochrome c peroxidase activity by cardiolipin. Biochemistry (Moscow, Russ. Fed.) 71, 989-997.
29. Bradley, J. M., Silkstone, G., Wilson, M. T., Cheesman, M. R., and Butt, J. N. (2011) Probing a complex of cytochrome c and cardiolipin by magnetic circular dichroism spectroscopy: Implications for the initial events in apoptosis. J. Am. Chem. Soc. 133, 19676-19679.
30. Davis, D. J., Frame, M. K., and Johnson, D. A. (1988) Resonance Raman spectroscopy indicates a lysine as the sixth iron ligand in cytochrome f . Biochim. Biophys. Acta 936, 61-66.
31. Schonhoff, C. M., Gaston, B., and Mannick, J. B. (2003) Nitrosylation of Cytochrome c during Apoptosis. J. Biol. Chem. 278, 18265-18270.
32. Chung, H. T., Pae, H. O., Choi, B. M., Billiar, T. R., and Kim, Y. M. (2001) Nitric oxide as a bioregulator of apoptosis. Biochem. Biophys. Res. Commun. 282, 1075-1079.
33. 2 access to heme. Biochemistry (Moscow, Russ. Fed.) 71, 998-1005.
34. Kapralov, A. A., Kurnikov, I. V., Vlasova, I. I., Belikova, N. A., Tyurin, V. A., Basova, L. V., Zhao, Q., Tyurina, Y. Y., Jiang, J., Bayir, H., Vladimirov, Y. A., and Kagan, V. E. (2007) The hierarchy of structural transitions induced in cytochrome c by anionic phospholipids determines its peroxidase activation and selective peroxidation during apoptosis in cells. Biochemistry 46, 14232-14244.