Artículo

Hannibal, L.; Tomasina, F.; Capdevila, D.A.; Demicheli, V.; Tórtora, V.; Alvarez-Paggi, D.; Jemmerson, R.; Murgida, D.H.; Radi, R. "Alternative Conformations of Cytochrome c: Structure, Function, and Detection" (2016) Biochemistry. 55(3):407-428
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Abstract:

Cytochrome c (cyt c) is a cationic hemoprotein of ∼100 amino acid residues that exhibits exceptional functional versatility. While its primary function is electron transfer in the respiratory chain, cyt c is also recognized as a key component of the intrinsic apoptotic pathway, the mitochondrial oxidative protein folding machinery, and presumably as a redox sensor in the cytosol, along with other reported functions. Transition to alternative conformations and gain-of-peroxidase activity are thought to further enable the multiple functions of cyt c and its translocation across cellular compartments. In vitro, direct interactions of cyt c with cardiolipin, post-translational modifications such as tyrosine nitration, phosphorylation, methionine sulfoxidation, mutations, and even fine changes in electrical fields lead to a variety of conformational states that may be of biological relevance. The identification of these alternative conformations and the elucidation of their functions in vivo continue to be a major challenge. Here, we unify the knowledge of the structural flexibility of cyt c that supports functional moonlighting and review biochemical and immunochemical evidence confirming that cyt c undergoes conformational changes during normal and altered cellular homeostasis. © 2015 American Chemical Society.

Registro:

Documento: Artículo
Título:Alternative Conformations of Cytochrome c: Structure, Function, and Detection
Autor:Hannibal, L.; Tomasina, F.; Capdevila, D.A.; Demicheli, V.; Tórtora, V.; Alvarez-Paggi, D.; Jemmerson, R.; Murgida, D.H.; Radi, R.
Filiación:Departamento de Bioquímica, Facultad de Medicina, Universidad de la República, Avda. General Flores 2125, Montevideo, 11800, Uruguay
Centro de Investigaciones Biomédicas (CEINBIO), Facultad de Medicina, Universidad de la República, Avda. General Flores 2125, Montevideo, 11800, Uruguay
Center for Pediatrics and Adolescent Medicine, Medical Center, University of Freiburg, Mathildenstrasse 1, Freiburg, D-79106, Germany
Departamento de Química Inorgánica, Analítica y Química Física, INQUIMAE, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón 2, Ciudad Universitaria, Buenos Aires, C1428EHA, Argentina
Department of Microbiology and Immunology, University of Minnesota, MMC 196, 420 Delaware Street, Southeast, Minneapolis, MN 55455, United States
Palabras clave:Machinery; Phospholipids; Amino acid residues; Cellular compartments; Cellular homeostasis; Conformational change; Conformational state; Peroxidase activities; Post-translational modifications; Structural flexibilities; Amino acids; cardiolipin; cytochrome c; methionine; peroxidase; tyrosine; cytochrome c; fungal protein; phospholipid; vegetable protein; antigenicity; apoptosis; cell respiration; circular dichroism; complex formation; conformational transition; crystal structure; electron transport; enzyme activity; genetic conservation; hydrogen bond; immunochemistry; in vitro study; membrane potential; nitration; oxidation reduction potential; phosphorylation; physical chemistry; priority journal; protein analysis; protein conformation; protein folding; protein function; protein phosphorylation; protein processing; protein secondary structure; protein stability; protein structure; respiratory chain; Review; static electricity; sulfoxidation; animal; chemistry; electricity; human; intracellular space; metabolism; protein conformation; protein transport; Animals; Cardiolipins; Cytochromes c; Electricity; Fungal Proteins; Humans; Intracellular Space; Phospholipids; Plant Proteins; Protein Conformation; Protein Folding; Protein Processing, Post-Translational; Protein Transport
Año:2016
Volumen:55
Número:3
Página de inicio:407
Página de fin:428
DOI: http://dx.doi.org/10.1021/acs.biochem.5b01385
Título revista:Biochemistry
Título revista abreviado:Biochemistry
ISSN:00062960
CODEN:BICHA
CAS:cytochrome c, 9007-43-6, 9064-84-0; methionine, 59-51-8, 63-68-3, 7005-18-7; peroxidase, 9003-99-0; tyrosine, 16870-43-2, 55520-40-6, 60-18-4; Cardiolipins; Cytochromes c; Fungal Proteins; Phospholipids; Plant Proteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00062960_v55_n3_p407_Hannibal

Referencias:

  • Margoliash, E., Functional evolution of cytochrome c (1972) The Harvey Lectures, pp. 177-247. , Series 66, Academic Press, London
  • Bushnell, G.W., Louie, G.V., Brayer, G.D., High-resolution three-dimensional structure of horse heart cytochrome c (1990) J. Mol. Biol., 214, pp. 585-595
  • Zaidi, S., Hassan, M.I., Islam, A., Ahmad, F., The role of key residues in structure, function, and stability of cytochrome-c (2014) Cell. Mol. Life Sci., 71, pp. 229-255
  • Schmidt, T.R., Wildman, D.E., Uddin, M., Opazo, J.C., Goodman, M., Grossman, L.I., Rapid electrostatic evolution at the binding site for cytochrome c on cytochrome c oxidase in anthropoid primates (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 6379-6384
  • Bertini, I., Grassi, E., Luchinat, C., Quattrone, A., Saccenti, E., Monomorphism of human cytochrome c (2006) Genomics, 88, pp. 669-672
  • Fumo, G., Spitzer, J.S., Fetrow, J.S., A method of directed random mutagenesis of the yeast chromosome shows that the iso-1-cytochrome c heme ligand His18 is essential (1995) Gene, 164, pp. 33-39
  • Roder, H., Elove, G.A., Englander, S.W., Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR (1988) Nature, 335, pp. 700-704
  • Sosnick, T.R., Mayne, L., Hiller, R., Englander, S.W., The barriers in protein folding (1994) Nat. Struct. Biol., 1, pp. 149-156
  • Wu, L.C., Laub, P.B., Elove, G.A., Carey, J., Roder, H., A noncovalent peptide complex as a model for an early folding intermediate of cytochrome c (1993) Biochemistry, 32, pp. 10271-10276
  • San Francisco, B., Bretsnyder, E.C., Kranz, R.G., Human mitochondrial holocytochrome c synthase's heme binding, maturation determinants, and complex formation with cytochrome c (2013) Proc. Natl. Acad. Sci. U. S. A., 110, pp. E788-E797
  • Kapralov, A.A., Yanamala, N., Tyurina, Y.Y., Castro, L., Samhan-Arias, A., Vladimirov, Y.A., Maeda, A., Kagan, V.E., Topography of tyrosine residues and their involvement in peroxidation of polyunsaturated cardiolipin in cytochrome c/cardiolipin peroxidase complexes (2011) Biochim. Biophys. Acta, Biomembr., 1808, pp. 2147-2155
  • Barker, P.D., Ferguson, S.J., Still a puzzle: why is haem covalently attached in c-type cytochromes? (1999) Structure, 7, pp. R281-R290
  • Heineman, W.R., Norris, B.J., Goelz, J.F., Measurement of enzyme E'values by optically transparent thin layer electrochemical cells (1975) Anal. Chem., 47, pp. 79-84
  • Luntz, T.L., Schejter, A., Garber, E.A., Margoliash, E., Structural significance of an internal water molecule studied by site-directed mutagenesis of tyrosine-67 in rat cytochrome c (1989) Proc. Natl. Acad. Sci. U. S. A., 86, pp. 3524-3528
  • Kawai, C., Prado, F.M., Nunes, G.L., Di Mascio, P., Carmona-Ribeiro, A.M., Nantes, I.L., PH-Dependent interaction of cytochrome c with mitochondrial mimetic membranes: the role of an array of positively charged amino acids (2005) J. Biol. Chem., 280, pp. 34709-34717
  • Koppenol, W.H., Margoliash, E., The asymmetric distribution of charges on the surface of horse cytochrome c. Functional implications (1982) J. Biol. Chem., 257, pp. 4426-4437
  • Huttemann, M., Pecina, P., Rainbolt, M., Sanderson, T.H., Kagan, V.E., Samavati, L., Doan, J.W., Lee, I., The multiple functions of cytochrome c and their regulation in life and death decisions of the mammalian cell: from respiration to apoptosis (2011) Mitochondrion, 11, pp. 369-381
  • Mordas, A., Tokatlidis, K., The MIA Pathway: A Key Regulator of Mitochondrial Oxidative Protein Folding and Biogenesis (2015) Acc. Chem. Res., 48, pp. 2191-2199
  • Greenwood, C., Palmer, G., Evidence for the existence of two functionally distinct forms cytochrome c manomer at alkaline pH (1965) J. Biol. Chem., 240, pp. 3660-3663
  • Wilson, M.T., Greenwood, C., The alkaline transition in ferrycytochrome c (1996) Cytochrome C: A Multidisciplinary Approach, pp. 611-634. , (Scott, R. A. and Mauk, A. G. Eds.), University Science Books, Sausalito, CA
  • Theorell, H., Åkesson, A., Studies on cytochrome c. II. the optical properties of pure cytochrome c and some of its derivatives (1941) J. Am. Chem. Soc., 63, pp. 1812-1818
  • Kagan, V.E., Tyurin, V.A., Jiang, J., Tyurina, Y.Y., Ritov, V.B., Amoscato, A.A., Osipov, A.N., Borisenko, G.G., Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors (2005) Nat. Chem. Biol., 1, pp. 223-232
  • Capdevila, D.A., Oviedo Rouco, S., Tomasina, F., Tortora, V., Demicheli, V., Radi, R., Murgida, D.H., Active Site Structure and Peroxidase Activity of Oxidatively Modified Cytochrome c Species in Complexes with Cardiolipin (2015) Biochemistry, 54, pp. 7491-7504
  • Godoy, L.C., Munoz-Pinedo, C., Castro, L., Cardaci, S., Schonhoff, C.M., King, M., Tortora, V., Mannick, J.B., Disruption of the M80-Fe ligation stimulates the translocation of cytochrome c to the cytoplasm and nucleus in nonapoptotic cells (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 2653-2658
  • Tuominen, E.K., Wallace, C.J., Kinnunen, P.K., Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage (2002) J. Biol. Chem., 277, pp. 8822-8826
  • Santucci, R., Sinibaldi, F., Patriarca, A., Santucci, D., Fiorucci, L., Misfolded proteins and neurodegeneration: role of non-native cytochrome c in cell death (2010) Expert Rev. Proteomics, 7, pp. 507-517
  • Hoye, A.T., Davoren, J.E., Wipf, P., Fink, M.P., Kagan, V.E., Targeting mitochondria (2008) Acc. Chem. Res., 41, pp. 87-97
  • Josephs, T.M., Liptak, M.D., Hughes, G., Lo, A., Smith, R.M., Wilbanks, S.M., Bren, K.L., Ledgerwood, E.C., Conformational change and human cytochrome c function: mutation of residue 41 modulates caspase activation and destabilizes Met-80 coordination (2013) JBIC, J. Biol. Inorg. Chem., 18, pp. 289-297
  • Cassina, A.M., Hodara, R., Souza, J.M., Thomson, L., Castro, L., Ischiropoulos, H., Freeman, B.A., Radi, R., Cytochrome c nitration by peroxynitrite (2000) J. Biol. Chem., 275, pp. 21409-21415
  • Abriata, L.A., Cassina, A., Tortora, V., Marin, M., Souza, J.M., Castro, L., Vila, A.J., Radi, R., Nitration of solvent-exposed tyrosine 74 on cytochrome c triggers heme iron-methionine 80 bond disruption. Nuclear magnetic resonance and optical spectroscopy studies (2009) J. Biol. Chem., 284, pp. 17-26
  • Josephs, T.M., Morison, I.M., Day, C.L., Wilbanks, S.M., Ledgerwood, E.C., Enhancing the peroxidase activity of cytochrome c by mutation of residue 41: implications for the peroxidase mechanism and cytochrome c release (2014) Biochem. J., 458, pp. 259-265
  • De Rocco, D., Cerqua, C., Goffrini, P., Russo, G., Pastore, A., Meloni, F., Nicchia, E., Savoia, A., Mutations of cytochrome c identified in patients with thrombocytopenia THC4 affect both apoptosis and cellular bioenergetics (2014) Biochim. Biophys. Acta, Mol. Basis Dis., 1842, pp. 269-274
  • Lett, C.M., Guillemette, J.G., Increasing the redox potential of isoform 1 of yeast cytochrome c through the modification of select haem interactions (2002) Biochem. J., 362, pp. 281-287
  • Ascenzi, P., Coletta, M., Wilson, M.T., Fiorucci, L., Marino, M., Polticelli, F., Sinibaldi, F., Santucci, R., Cardiolipin-cytochrome c complex: Switching cytochrome c from an electron-transfer shuttle to a myoglobin- and a peroxidase-like heme-protein (2015) IUBMB Life, 67, pp. 98-109
  • Schonhoff, C.M., Gaston, B., Mannick, J.B., Nitrosylation of cytochrome c during apoptosis (2003) J. Biol. Chem., 278, pp. 18265-18270
  • Jemmerson, R., Liu, J., Hausauer, D., Lam, K.P., Mondino, A., Nelson, R.D., A conformational change in cytochrome c of apoptotic and necrotic cells is detected by monoclonal antibody binding and mimicked by association of the native antigen with synthetic phospholipid vesicles (1999) Biochemistry, 38, pp. 3599-3609
  • Yu, X., Acehan, D., Menetret, J.F., Booth, C.R., Ludtke, S.J., Riedl, S.J., Shi, Y., Akey, C.W., A structure of the human apoptosome at 12.8 A resolution provides insights into this cell death platform (2005) Structure, 13, pp. 1725-1735
  • Zhou, M., Li, Y., Hu, Q., Bai, X.C., Huang, W., Yan, C., Scheres, S.H., Shi, Y., Atomic structure of the apoptosome: mechanism of cytochrome c- and dATP-mediated activation of Apaf-1 (2015) Genes Dev., 29, pp. 2349-2361
  • Boehning, D., Patterson, R.L., Sedaghat, L., Glebova, N.O., Kurosaki, T., Snyder, S.H., Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis (2003) Nat. Cell Biol., 5, pp. 1051-1061
  • Bruey, J.M., Ducasse, C., Bonniaud, P., Ravagnan, L., Susin, S.A., Diaz-Latoud, C., Gurbuxani, S., Garrido, C., Hsp27 negatively regulates cell death by interacting with cytochrome c (2000) Nat. Cell Biol., 2, pp. 645-652
  • Codina, R., Vanasse, A., Kelekar, A., Vezys, V., Jemmerson, R., Cytochrome c-induced lymphocyte death from the outside in: inhibition by serum leucine-rich alpha-2-glycoprotein-1 (2010) Apoptosis, 15, pp. 139-152
  • Feng, Y., Roder, H., Englander, S.W., Wand, A.J., Di Stefano, D.L., Proton resonance assignments of horse ferricytochrome c (1989) Biochemistry, 28, pp. 195-203
  • Feng, Y., Englander, S.W., Salt-dependent structure change and ion binding in cytochrome c studied by two-dimensional proton NMR (1990) Biochemistry, 29, pp. 3505-3509
  • Feng, Y., Roder, H., Englander, S.W., Redox-dependent structure change and hyperfine nuclear magnetic resonance shifts in cytochrome c (1990) Biochemistry, 29, pp. 3494-3504
  • Feng, Y.Q., Roder, H., Englander, S.W., Assignment of paramagnetically shifted resonances in the 1H NMR spectrum of horse ferricytochrome c (1990) Biophys. J., 57, pp. 15-22
  • Leszczynski, J.F., Rose, G.D., Loops in globular proteins: a novel category of secondary structure (1986) Science, 234, pp. 849-855
  • Louie, G.V., Brayer, G.D., High-resolution refinement of yeast iso-1-cytochrome c and comparisons with other eukaryotic cytochromes c (1990) J. Mol. Biol., 214, pp. 527-555
  • Liptak, M.D., Fagerlund, R.D., Ledgerwood, E.C., Wilbanks, S.M., Bren, K.L., The proapoptotic G41S mutation to human cytochrome c alters the heme electronic structure and increases the electron self-exchange rate (2011) J. Am. Chem. Soc., 133, pp. 1153-1155
  • McClelland, L.J., Mou, T.C., Jeakins-Cooley, M.E., Sprang, S.R., Bowler, B.E., Structure of a mitochondrial cytochrome c conformer competent for peroxidase activity (2014) Proc. Natl. Acad. Sci. U. S. A., 111, pp. 6648-6653
  • Poulos, T.L., Kraut, J., A hypothetical model of the cytochrome c peroxidase. cytochrome c electron transfer complex (1980) J. Biol. Chem., 255, pp. 10322-10330
  • Poulos, T.L., Finzel, B.C., Heme enzyme structure and function (1984) Pept. Prot. Rev., 4, pp. 115-171
  • Gu, J., Yang, S., Rajic, A.J., Kurnikov, I.V., Prytkova, T.R., Pletneva, E.V., Control of cytochrome c redox reactivity through off-pathway modifications in the protein hydrogen-bonding network (2014) Chem. Commun. (Cambridge, U. K.), 50, pp. 5355-5357
  • Bowman, S.E., Bren, K.L., The chemistry and biochemistry of heme c: functional bases for covalent attachment (2008) Nat. Prod. Rep., 25, pp. 1118-1130
  • Haldar, S., Mitra, S., Chattopadhyay, K., Role of protein stabilizers on the conformation of the unfolded state of cytochrome c and its early folding kinetics: investigation at single molecular resolution (2010) J. Biol. Chem., 285, pp. 25314-25323
  • Paul, S.S., Sil, P., Haldar, S., Mitra, S., Chattopadhyay, K., Subtle Change in the Charge Distribution of Surface Residues May Affect the Secondary Functions of Cytochrome c (2015) J. Biol. Chem., 290, pp. 14476-14490
  • Weinkam, P., Pletneva, E.V., Gray, H.B., Winkler, J.R., Wolynes, P.G., Electrostatic effects on funneled landscapes and structural diversity in denatured protein ensembles (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 1796-1801
  • Weinkam, P., Zimmermann, J., Romesberg, F.E., Wolynes, P.G., The folding energy landscape and free energy excitations of cytochrome c (2010) Acc. Chem. Res., 43, pp. 652-660
  • Bryngelson, J.D., Onuchic, J.N., Socci, N.D., Wolynes, P.G., Funnels, pathways, and the energy landscape of protein folding: a synthesis (1995) Proteins: Struct., Funct., Genet., 21, pp. 167-195
  • Maity, H., Rumbley, J.N., Englander, S.W., Functional role of a protein foldon - An Omega-loop foldon controls the alkaline transition in ferricytochrome c (2006) Proteins: Struct., Funct., Genet., 63, pp. 349-355
  • Perroud, T.D., Bokoch, M.P., Zare, R.N., Cytochrome c conformations resolved by the photon counting histogram: watching the alkaline transition with single-molecule sensitivity (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 17570-17575
  • Hong, X.L., Dixon, D.W., NMR study of the alkaline isomerization of ferricytochrome c (1989) FEBS Lett., 246, pp. 105-108
  • Ferrer, J.C., Guillemette, J.G., Bogumil, R., Inglis, S.C., Smith, M., Mauk, A.G., Identification of Lys79 as an iron ligand in one form of alkaline yeast iso-1-ferricytochrome c (1993) J. Am. Chem. Soc., 115, pp. 7507-7508
  • Bai, Y., Sosnick, T.R., Mayne, L., Englander, S.W., Protein folding intermediates: native-state hydrogen exchange (1995) Science, 269, pp. 192-197
  • Krishna, M.M., Maity, H., Rumbley, J.N., Englander, S.W., Branching in the sequential folding pathway of cytochrome c (2007) Protein Sci., 16, pp. 1946-1956
  • Maity, H., Maity, M., Englander, S.W., How cytochrome c folds, and why: submolecular foldon units and their stepwise sequential stabilization (2004) J. Mol. Biol., 343, pp. 223-233
  • Maity, H., Maity, M., Krishna, M.M., Mayne, L., Englander, S.W., Protein folding: the stepwise assembly of foldon units (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 4741-4746
  • Panchenko, A.R., Luthey-Schulten, Z., Wolynes, P.G., Foldons, protein structural modules, and exons (1996) Proc. Natl. Acad. Sci. U. S. A., 93, pp. 2008-2013
  • Krishna, M.M., Lin, Y., Mayne, L., Englander, S.W., Intimate view of a kinetic protein folding intermediate: residue-resolved structure, interactions, stability, folding and unfolding rates, homogeneity (2003) J. Mol. Biol., 334, pp. 501-513
  • Fazelinia, H., Xu, M., Cheng, H., Roder, H., Ultrafast hydrogen exchange reveals specific structural events during the initial stages of folding of cytochrome c (2014) J. Am. Chem. Soc., 136, pp. 733-740
  • Ziv, G., Thirumalai, D., Haran, G., Collapse transition in proteins (2009) Phys. Chem. Chem. Phys., 11, pp. 83-93
  • Klein-Seetharaman, J., Oikawa, M., Grimshaw, S.B., Wirmer, J., Duchardt, E., Ueda, T., Imoto, T., Schwalbe, H., Long-range interactions within a nonnative protein (2002) Science, 295, pp. 1719-1722
  • Lapidus, L.J., Yao, S., McGarrity, K.S., Hertzog, D.E., Tubman, E., Bakajin, O., Protein hydrophobic collapse and early folding steps observed in a microfluidic mixer (2007) Biophys. J., 93, pp. 218-224
  • Russell, B.S., Melenkivitz, R., Bren, K.L., NMR investigation of ferricytochrome c unfolding: detection of an equilibrium unfolding intermediate and residual structure in the denatured state (2000) Proc. Natl. Acad. Sci. U. S. A., 97, pp. 8312-8317
  • Colon, W., Wakem, L.P., Sherman, F., Roder, H., Identification of the predominant non-native histidine ligand in unfolded cytochrome c (1997) Biochemistry, 36, pp. 12535-12541
  • Elove, G.A., Bhuyan, A.K., Roder, H., Kinetic mechanism of cytochrome c folding: involvement of the heme and its ligands (1994) Biochemistry, 33, pp. 6925-6935
  • Takahashi, S., Yeh, S.R., Das, T.K., Chan, C.K., Gottfried, D.S., Rousseau, D.L., Folding of cytochrome c initiated by submillisecond mixing (1997) Nat. Struct. Biol., 4, pp. 44-50
  • Tezcan, F.A., Winkler, J.R., Gray, H.B., Probing Protein Folding with Substitution-Inert Metal Ions. Folding Kinetics of Co(III)-cytochrome c (1999) J. Am. Chem. Soc., 121, pp. 11918-11919
  • Gadsby, P.M., Peterson, J., Foote, N., Greenwood, C., Thomson, A.J., Identification of the ligand-exchange process in the alkaline transition of horse heart cytochrome c (1987) Biochem. J., 246, pp. 43-54
  • Brandt, K.G., Parks, P.C., Czerlinski, G.H., Hess, G.P., On the elucidation of the pH dependence of the oxidation-reduction potential of cytochrome c at alkaline pH (1966) J. Biol. Chem., 241, pp. 4180-4185
  • Hoang, L., Maity, H., Krishna, M.M., Lin, Y., Englander, S.W., Folding units govern the cytochrome c alkaline transition (2003) J. Mol. Biol., 331, pp. 37-43
  • Assfalg, M., Bertini, I., Dolfi, A., Turano, P., Mauk, A.G., Rosell, F.I., Gray, H.B., Structural model for an alkaline form of ferricytochrome C (2003) J. Am. Chem. Soc., 125, pp. 2913-2922
  • Döpner, S., Hildebrandt, P., Rosell, F.I., Mauk, A.G., Alkaline Conformational Transitions of Ferricytochrome c Studied by Resonance Raman Spectroscopy (1998) J. Am. Chem. Soc., 120, pp. 11246-11255
  • Bradley, J.M., Silkstone, G., Wilson, M.T., Cheesman, M.R., Butt, J.N., Probing a complex of cytochrome c and cardiolipin by magnetic circular dichroism spectroscopy: implications for the initial events in apoptosis (2011) J. Am. Chem. Soc., 133, pp. 19676-19679
  • Amacher, J.F., Zhong, F., Lisi, G.P., Zhu, M.Q., Alden, S.L., Hoke, K.R., Madden, D.R., Pletneva, E.V., A Compact Structure of Cytochrome c Trapped in a Lysine-Ligated State: Loop Refolding and Functional Implications of a Conformational Switch (2015) J. Am. Chem. Soc., 137, pp. 8435-8449
  • McClelland, L.J., Seagraves, S.M., Khan, M.K., Cherney, M.M., Bandi, S., Culbertson, J.E., Bowler, B.E., The response of Omega-loop D dynamics to truncation of trimethyllysine 72 of yeast iso-1-cytochrome c depends on the nature of loop deformation (2015) JBIC, J. Biol. Inorg. Chem., 20, pp. 805-819
  • Bandi, S., Bowler, B.E., Effect of an Ala81His Mutation on the Met80 Loop Dynamics of Iso-1-cytochrome c (2015) Biochemistry, 54, p. 1729
  • Kinnunen, P.K., Koiv, A., Lehtonen, J.Y., Rytomaa, M., Mustonen, P., Lipid dynamics and peripheral interactions of proteins with membrane surfaces (1994) Chem. Phys. Lipids, 73, pp. 181-207
  • Kawai, C., Pessoto, F.S., Rodrigues, T., Mugnol, K.C., Tortora, V., Castro, L., Milicchio, V.A., Nantes, I.L., PH-sensitive binding of cytochrome c to the inner mitochondrial membrane. Implications for the participation of the protein in cell respiration and apoptosis (2009) Biochemistry, 48, pp. 8335-8342
  • Rytomaa, M., Mustonen, P., Kinnunen, P.K., Reversible, nonionic, and pH-dependent association of cytochrome c with cardiolipin-phosphatidylcholine liposomes (1992) J. Biol. Chem., 267, pp. 22243-22248
  • Rytomaa, M., Kinnunen, P.K., Evidence for two distinct acidic phospholipid-binding sites in cytochrome c (1994) J. Biol. Chem., 269, pp. 1770-1774
  • Rytomaa, M., Kinnunen, P.K., Reversibility of the binding of cytochrome c to liposomes. Implications for lipid-protein interactions (1995) J. Biol. Chem., 270, pp. 3197-3202
  • Rytomaa, M., Kinnunen, P.K., Dissociation of cytochrome c from liposomes by histone H1. Comparison with basic peptides (1996) Biochemistry, 35, pp. 4529-4539
  • Kawai, C., Pessoto, F.S., Graves, C.V., Carmona-Ribeiro, A.M., Nantes, I.L., Effects of transmembrane potential and pH gradient on the cytochrome c-promoted fusion of mitochondrial mimetic membranes (2013) J. Bioenerg. Biomembr., 45, pp. 421-430
  • Kagan, V.E., Bayir, H.A., Belikova, N.A., Kapralov, O., Tyurina, Y.Y., Tyurin, V.A., Jiang, J., Borisenko, G., Cytochrome c/cardiolipin relations in mitochondria: a kiss of death (2009) Free Radical Biol. Med., 46, pp. 1439-1453
  • Kapralov, A.A., Kurnikov, I.V., Vlasova, I.I., Belikova, N.A., Tyurin, V.A., Basova, L.V., Zhao, Q., Kagan, V.E., The hierarchy of structural transitions induced in cytochrome c by anionic phospholipids determines its peroxidase activation and selective peroxidation during apoptosis in cells (2007) Biochemistry, 46, pp. 14232-14244
  • Jutila, A., Rytomaa, M., Kinnunen, P.K., Detachment of cytochrome c by cationic drugs from membranes containing acidic phospholipids: comparison of lidocaine, propranolol, and gentamycin (1998) Mol. Pharmacol., 54, pp. 722-732
  • Kagan, V.E., Chu, C.T., Tyurina, Y.Y., Cheikhi, A., Bayir, H., Cardiolipin asymmetry, oxidation and signaling (2014) Chem. Phys. Lipids, 179, pp. 64-69
  • Radi, R., Sims, S., Cassina, A., Turrens, J.F., Roles of catalase and cytochrome c in hydroperoxide-dependent lipid peroxidation and chemiluminescence in rat heart and kidney mitochondria (1993) Free Radical Biol. Med., 15, pp. 653-659
  • Radi, R., Turrens, J.F., Chang, L.Y., Bush, K.M., Crapo, J.D., Freeman, B.A., Detection of catalase in rat heart mitochondria (1991) J. Biol. Chem., 266, pp. 22028-22034
  • Radi, R., Turrens, J.F., Freeman, B.A., Cytochrome c-catalyzed membrane lipid peroxidation by hydrogen peroxide (1991) Arch. Biochem. Biophys., 288, pp. 118-125
  • Sinibaldi, F., Fiorucci, L., Patriarca, A., Lauceri, R., Ferri, T., Coletta, M., Santucci, R., Insights into cytochrome c-cardiolipin interaction. Role played by ionic strength (2008) Biochemistry, 47, pp. 6928-6935
  • Abe, M., Niibayashi, R., Koubori, S., Moriyama, I., Miyoshi, H., Molecular mechanisms for the induction of peroxidase activity of the cytochrome c-cardiolipin complex (2011) Biochemistry, 50, pp. 8383-8391
  • Vladimirov, Y.A., Proskurnina, E.V., Izmailov, D.Y., Novikov, A.A., Brusnichkin, A.V., Osipov, A.N., Kagan, V.E., Cardiolipin activates cytochrome c peroxidase activity since it facilitates H(2)O(2) access to heme (2006) Biochemistry (Moscow), 71, pp. 998-1005
  • Vladimirov, Y.A., Proskurnina, E.V., Izmailov, D.Y., Novikov, A.A., Brusnichkin, A.V., Osipov, A.N., Kagan, V.E., Mechanism of activation of cytochrome C peroxidase activity by cardiolipin (2006) Biochemistry (Moscow), 71, pp. 989-997
  • Huang, Z., Jiang, J., Tyurin, V.A., Zhao, Q., Mnuskin, A., Ren, J., Belikova, N.A., Kagan, V.E., Cardiolipin deficiency leads to decreased cardiolipin peroxidation and increased resistance of cells to apoptosis (2008) Free Radical Biol. Med., 44, pp. 1935-1944
  • Belikova, N.A., Vladimirov, Y.A., Osipov, A.N., Kapralov, A.A., Tyurin, V.A., Potapovich, M.V., Basova, L.V., Kagan, V.E., Peroxidase activity and structural transitions of cytochrome c bound to cardiolipin-containing membranes (2006) Biochemistry, 45, pp. 4998-5009
  • Patriarca, A., Polticelli, F., Piro, M.C., Sinibaldi, F., Mei, G., Bari, M., Santucci, R., Fiorucci, L., Conversion of cytochrome c into a peroxidase: inhibitory mechanisms and implication for neurodegenerative diseases (2012) Arch. Biochem. Biophys., 522, pp. 62-69
  • Bartesaghi, S., Wenzel, J., Trujillo, M., Lopez, M., Joseph, J., Kalyanaraman, B., Radi, R., Lipid peroxyl radicals mediate tyrosine dimerization and nitration in membranes (2010) Chem. Res. Toxicol., 23, pp. 821-835
  • Folkes, L.K., Bartesaghi, S., Trujillo, M., Radi, R., Wardman, P., Kinetics of oxidation of tyrosine by a model alkoxyl radical (2012) Free Radical Res., 46, pp. 1150-1156
  • Kapetanaki, S.M., Silkstone, G., Husu, I., Liebl, U., Wilson, M.T., Vos, M.H., Interaction of carbon monoxide with the apoptosis-inducing cytochrome c-cardiolipin complex (2009) Biochemistry, 48, pp. 1613-1619
  • Spooner, P.J., Watts, A., Cytochrome c interactions with cardiolipin in bilayers: a multinuclear magic-angle spinning NMR study (1992) Biochemistry, 31, pp. 10129-10138
  • Hanske, J., Toffey, J.R., Morenz, A.M., Bonilla, A.J., Schiavoni, K.H., Pletneva, E.V., Conformational properties of cardiolipin-bound cytochrome c (2012) Proc. Natl. Acad. Sci. U. S. A., 109, pp. 125-130
  • Balakrishnan, G., Hu, Y., Oyerinde, O.F., Su, J., Groves, J.T., Spiro, T.G., A conformational switch to beta-sheet structure in cytochrome c leads to heme exposure. Implications for cardiolipin peroxidation and apoptosis (2007) J. Am. Chem. Soc., 129, pp. 504-505
  • Pandiscia, L.A., Schweitzer-Stenner, R., Coexistence of native-like and non-native partially unfolded ferricytochrome c on the surface of cardiolipin-containing liposomes (2015) J. Phys. Chem. B, 119, pp. 1334-1349
  • O'Brien, E.S., Nucci, N.V., Fuglestad, B., Tommos, C., Wand, A.J., Defining the apoptotic trigger: the interaction of cytochrome c and cardiolipin (2015) J. Biol. Chem., 290, p. 30879
  • Mandal, A., Hoop, C.L., Delucia, M., Kodali, R., Kagan, V.E., Ahn, J., Van Der Wel, P.C., Structural Changes and Proapoptotic Peroxidase Activity of Cardiolipin-Bound Mitochondrial Cytochrome c (2015) Biophys. J., 109, pp. 1873-1884
  • Oellerich, S., Lecomte, S., Paternostre, M., Heimburg, T., Hildebrandt, P., Peripheral and Integral Binding of Cytochrome c to Phospholipids Vesicles (2004) J. Phys. Chem. B, 108, pp. 3871-3878
  • Simon, M., Metzinger-Le Meuth, V., Chevance, S., Delalande, O., Bondon, A., Versatility of non-native forms of human cytochrome c: pH and micellar concentration dependence (2013) JBIC, J. Biol. Inorg. Chem., 18, pp. 27-38
  • Sinibaldi, F., Howes, B.D., Piro, M.C., Polticelli, F., Bombelli, C., Ferri, T., Coletta, M., Santucci, R., Extended cardiolipin anchorage to cytochrome c: a model for protein-mitochondrial membrane binding (2010) JBIC, J. Biol. Inorg. Chem., 15, pp. 689-700
  • Bergstrom, C.L., Beales, P.A., Lv, Y., Vanderlick, T.K., Groves, J.T., Cytochrome c causes pore formation in cardiolipin-containing membranes (2013) Proc. Natl. Acad. Sci. U. S. A., 110, pp. 6269-6274
  • Firsov, A.M., Kotova, E.A., Korepanova, E.A., Osipov, A.N., Antonenko, Y.N., Peroxidative permeabilization of liposomes induced by cytochrome c/cardiolipin complex (2015) Biochim. Biophys. Acta, Biomembr., 1848, pp. 767-774
  • Gonzalez-Arzola, K., Diaz-Moreno, I., Cano-Gonzalez, A., Diaz-Quintana, A., Velazquez-Campoy, A., Moreno-Beltran, B., Lopez-Rivas, A., De La Rosa, M.A., Structural basis for inhibition of the histone chaperone activity of SET/TAF-Ibeta by cytochrome c (2015) Proc. Natl. Acad. Sci. U. S. A., 112, pp. 9908-9913
  • Batthyany, C., Souza, J.M., Duran, R., Cassina, A., Cervenansky, C., Radi, R., Time course and site(s) of cytochrome c tyrosine nitration by peroxynitrite (2005) Biochemistry, 44, pp. 8038-8046
  • Souza, J.M., Castro, L., Cassina, A.M., Batthyany, C., Radi, R., Nitrocytochrome c: synthesis, purification, and functional studies (2008) Methods Enzymol., 441, pp. 197-215
  • Radi, R., Nitric oxide, oxidants, and protein tyrosine nitration (2004) Proc. Natl. Acad. Sci. U. S. A., 101, pp. 4003-4008
  • Souza, J.M., Peluffo, G., Radi, R., Protein tyrosine nitration - Functional alteration or just a biomarker? (2008) Free Radical Biol. Med., 45, pp. 357-366
  • Radi, R., Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects (2013) Acc. Chem. Res., 46, pp. 550-559
  • Alonso, D., Encinas, J.M., Uttenthal, L.O., Bosca, L., Serrano, J., Fernandez, A.P., Castro-Blanco, S., Rodrigo, J., Coexistence of translocated cytochrome c and nitrated protein in neurons of the rat cerebral cortex after oxygen and glucose deprivation (2002) Neuroscience, 111, pp. 47-56
  • Cruthirds, D.L., Novak, L., Akhi, K.M., Sanders, P.W., Thompson, J.A., Macmillan-Crow, L.A., Mitochondrial targets of oxidative stress during renal ischemia/reperfusion (2003) Arch. Biochem. Biophys., 412, pp. 27-33
  • Peluffo, G., Radi, R., Biochemistry of protein tyrosine nitration in cardiovascular pathology (2007) Cardiovasc. Res., 75, pp. 291-302
  • Oursler, M.J., Bradley, E.W., Elfering, S.L., Giulivi, C., Native, not nitrated, cytochrome c and mitochondria-derived hydrogen peroxide drive osteoclast apoptosis (2005) Am. J. Physiol. Cell. Physiol., 288, pp. C156-C168
  • Nakagawa, H., Komai, N., Takusagawa, M., Miura, Y., Toda, T., Miyata, N., Ozawa, T., Ikota, N., Nitration of specific tyrosine residues of cytochrome C is associated with caspase-cascade inactivation (2007) Biol. Pharm. Bull., 30, pp. 15-20
  • Jang, B., Han, S., Biochemical properties of cytochrome c nitrated by peroxynitrite (2006) Biochimie, 88, pp. 53-58
  • Rodriguez-Roldan, V., Garcia-Heredia, J.M., Navarro, J.A., De La Rosa, M.A., Hervas, M., Effect of nitration on the physicochemical and kinetic features of wild-type and monotyrosine mutants of human respiratory cytochrome c (2008) Biochemistry, 47, pp. 12371-12379
  • Ly, H.K., Utesch, T., Diaz-Moreno, I., Garcia-Heredia, J.M., De La Rosa, M.A., Hildebrandt, P., Perturbation of the redox site structure of cytochrome c variants upon tyrosine nitration (2012) J. Phys. Chem. B, 116, pp. 5694-5702
  • Tognaccini, L., Ciaccio, C., D'Oria, V., Cervelli, M., Howes, B.D., Coletta, M., Mariottini, P., Fiorucci, L., Structure-function relationships in human cytochrome c: the role of tyrosine 67 (2016) J. Inorg. Biochem., 155, pp. 56-66
  • Ying, T., Wang, Z.H., Lin, Y.W., Xie, J., Tan, X., Huang, Z.X., Tyrosine-67 in cytochrome c is a possible apoptotic trigger controlled by hydrogen bonds via a conformational transition (2009) Chem. Commun. (Cambridge, U. K.), pp. 4512-4514
  • Garcia-Heredia, J.M., Diaz-Moreno, I., Nieto, P.M., Orzáez, M., Kocanis, S., Teixeira, M., Perez-Paya, E., De La Rosa, M.A., Nitration of tyrosine 74 prevents human cytochrome c to play a key role in apoptosis signaling by blocking caspase-9 activation (2010) Biochim. Biophys. Acta, Bioenerg., 1797, pp. 981-993
  • Alvarez-Paggi, D., Castro, M.A., Tortora, V., Castro, L., Radi, R., Murgida, D.H., Electrostatically driven second-sphere ligand switch between high and low reorganization energy forms of native cytochrome c (2013) J. Am. Chem. Soc., 135, pp. 4389-4397
  • Diaz-Moreno, I., Garcia-Heredia, J.M., Diaz-Quintana, A., Teixeira, M., De La Rosa, M.A., Nitration of tyrosines 46 and 48 induces the specific degradation of cytochrome c upon change of the heme iron state to high-spin (2011) Biochim. Biophys. Acta, Bioenerg., 1807, pp. 1616-1623
  • Garcia-Heredia, J.M., Diaz-Quintana, A., Salzano, M., Orzáez, M., Perez-Paya, E., Teixeira, M., De La Rosa, M.A., Diaz-Moreno, I., Tyrosine phosphorylation turns alkaline transition into a biologically relevant process and makes human cytochrome c behave as an anti-apoptotic switch (2011) JBIC, J. Biol. Inorg. Chem., 16, pp. 1155-1168
  • Rajagopal, B.S., Edzuma, A.N., Hough, M.A., Blundell, K.L., Kagan, V.E., Kapralov, A.A., Fraser, L.A., Worrall, J.A., The hydrogen-peroxide-induced radical behaviour in human cytochrome c-phospholipid complexes: implications for the enhanced pro-apoptotic activity of the G41S mutant (2013) Biochem. J., 456, pp. 441-452
  • Morison, I.M., Cramer Borde, E.M., Cheesman, E.J., Cheong, P.L., Holyoake, A.J., Fichelson, S., Weeks, R.J., Ledgerwood, E.C., A mutation of human cytochrome c enhances the intrinsic apoptotic pathway but causes only thrombocytopenia (2008) Nat. Genet., 40, pp. 387-389
  • Capdevila, D.A., Marmisolle, W.A., Tomasina, F., Demicheli, V., Portela, M., Radi, R., Murgida, D.H., Specific methionine oxidation of cytochrome c in complexes with zwitterionic lipids by hydrogen peroxide: potential implications for apoptosis (2015) Chem. Sci., 6, pp. 705-713
  • Azzi, A., Montecucco, C., Richter, C., The use of acetylated ferricytochrome c for the detection of superoxide radicals produced in biological membranes (1975) Biochem. Biophys. Res. Commun., 65, pp. 597-603
  • Kim, S.C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Cheng, T., Zhao, Y., Substrate and functional diversity of lysine acetylation revealed by a proteomics survey (2006) Mol. Cell, 23, pp. 607-618
  • Osman, C., Voelker, D.R., Langer, T., Making heads or tails of phospholipids in mitochondria (2011) J. Cell Biol., 192, pp. 7-16
  • Salamon, Z., Tollin, G., Interaction of horse heart cytochrome c with lipid bilayer membranes: effects on redox potentials (1997) J. Bioenerg. Biomembr., 29, pp. 211-221
  • Trusova, V.M., Gorbenko, G.P., Molotkovsky, J.G., Kinnunen, P.K., Cytochrome c-lipid interactions: new insights from resonance energy transfer (2010) Biophys. J., 99, pp. 1754-1763
  • Capdevila, D.A., Marmisolle, W.A., Williams, F.J., Murgida, D.H., Phosphate mediated adsorption and electron transfer of cytochrome c. A time-resolved SERR spectroelectrochemical study (2013) Phys. Chem. Chem. Phys., 15, pp. 5386-5394
  • Marmisolle, W.A., Capdevila, D.A., De La Llave, E., Williams, F.J., Murgida, D.H., Self-assembled monolayers of NH2-terminated thiolates: order, pKa, and specific adsorption (2013) Langmuir, 29, pp. 5351-5359
  • Wang, B., Zhang, J.J., Pan, Z.Y., Tao, X.Q., Wang, H.S., A novel hydrogen peroxide sensor based on the direct electron transfer of horseradish peroxidase immobilized on silica-hydroxyapatite hybrid film (2009) Biosens. Bioelectron., 24, pp. 1141-1145
  • Sun, H., Hu, N., Ma, H., Direct Electrochemistry of Hemoglobin in Polyacrylamide Hydrogel Films on Pyrolytic Graphite Electrodes (2000) Electroanalysis, 12, pp. 1064-1070
  • Giorgio, M., Trinei, M., Migliaccio, E., Pelicci, P.G., Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? (2007) Nat. Rev. Mol. Cell Biol., 8, pp. 722-728
  • Radi, R., Thomson, L., Rubbo, H., Prodanov, E., Cytochrome c-catalyzed oxidation of organic molecules by hydrogen peroxide (1991) Arch. Biochem. Biophys., 288, pp. 112-117
  • De Biase, P.M., Paggi, D.A., Doctorovich, F., Hildebrandt, P., Estrin, D.A., Murgida, D.H., Marti, M.A., Molecular basis for the electric field modulation of cytochrome C structure and function (2009) J. Am. Chem. Soc., 131, pp. 16248-16256
  • Capdevila, D.A., Alvarez-Paggi, D., Castro, M.A., Tortora, V., Demicheli, V., Estrin, D.A., Radi, R., Murgida, D.H., Coupling of tyrosine deprotonation and axial ligand exchange in nitrocytochrome c (2014) Chem. Commun. (Cambridge, U. K.), 50, pp. 2592-2594
  • Diederix, R.E., Ubbink, M., Canters, G.W., Peroxidase activity as a tool for studying the folding of c-type cytochromes (2002) Biochemistry, 41, pp. 13067-13077
  • Clarke, R.J., The dipole potential of phospholipid membranes and methods for its detection (2001) Adv. Colloid Interface Sci., 89-90, pp. 263-281
  • Marcus, R.A., Chemical and Electrochemical Electron-Transfer Theory (1964) Annu. Rev. Phys. Chem., 15, pp. 155-196
  • Marcus, R.A., Electron Transfer Reactions in Chemistry: Theory and Experiment (Nobel Lecture) (1993) Angew. Chem., Int. Ed. Engl., 32, pp. 1111-1121
  • Murgida, D.H., Hildebrandt, P., Disentangling interfacial redox processes of proteins by SERR spectroscopy (2008) Chem. Soc. Rev., 37, pp. 937-945
  • Murgida, D.H., Hildebrandt, P., Electron-transfer processes of cytochrome C at interfaces. New insights by surface-enhanced resonance Raman spectroscopy (2004) Acc. Chem. Res., 37, pp. 854-861
  • Kranich, A., Ly, H.K., Hildebrandt, P., Murgida, D.H., Direct observation of the gating step in protein electron transfer: electric-field-controlled protein dynamics (2008) J. Am. Chem. Soc., 130, pp. 9844-9848
  • Murgida, D.H., Hildebrandt, P., Heterogeneous Electron Transfer of Cytochrome c on Coated Silver Electrodes. Electric Field Effects on Structure and Redox Potential (2001) J. Phys. Chem. B, 105, pp. 1578-1586
  • Koppenol, W.H., Rush, J.D., Mills, J.D., Margoliash, E., The dipole moment of cytochrome c (1991) Mol. Biol. Evol., 8, pp. 545-558
  • Alvarez-Paggi, D., Martin, D.F., Debiase, P.M., Hildebrandt, P., Marti, M.A., Murgida, D.H., Molecular basis of coupled protein and electron transfer dynamics of cytochrome c in biomimetic complexes (2010) J. Am. Chem. Soc., 132, pp. 5769-5778
  • Paggi, D.A., Martín, D.F., Kranich, A., Hildebrandt, P., Martí, M.A., Murgida, D.H., Computer simulation and SERR detection of cytochrome c dynamics at SAM-coated electrodes (2009) Electrochim. Acta, 54, pp. 4963-4970
  • Ly, H.K., Marti, M.A., Martin, D.F., Alvarez-Paggi, D., Meister, W., Kranich, A., Weidinger, I.M., Murgida, D.H., Thermal fluctuations determine the electron-transfer rates of cytochrome c in electrostatic and covalent complexes (2010) ChemPhysChem, 11, pp. 1225-1235
  • Alvarez-Paggi, D., Meister, W., Kuhlmann, U., Weidinger, I., Tenger, K., Zimanyi, L., Rakhely, G., Murgida, D.H., Disentangling electron tunneling and protein dynamics of cytochrome c through a rationally designed surface mutation (2013) J. Phys. Chem. B, 117, pp. 6061-6068
  • Battistuzzi, G., Bortolotti, C.A., Bellei, M., Di Rocco, G., Salewski, J., Hildebrandt, P., Sola, M., Role of Met80 and Tyr67 in the low-pH conformational equilibria of cytochrome c (2012) Biochemistry, 51, pp. 5967-5978
  • Berghuis, A.M., Guillemette, J.G., McLendon, G., Sherman, F., Smith, M., Brayer, G.D., The role of a conserved internal water molecule and its associated hydrogen bond network in cytochrome c (1994) J. Mol. Biol., 236, pp. 786-799
  • Feinberg, B.A., Petro, L., Hock, G., Qin, W., Margoliash, E., Using entropies of reaction to predict changes in protein stability: tyrosine-67-phenylalanine variants of rat cytochrome c and yeast Iso-1 cytochromes c (1999) J. Pharm. Biomed. Anal., 19, pp. 115-125
  • Zhou, P., Tian, F., Lv, F., Shang, Z., Geometric characteristics of hydrogen bonds involving sulfur atoms in proteins (2009) Proteins: Struct., Funct., Genet., 76, pp. 151-163
  • Lange, C., Hunte, C., Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 2800-2805
  • Pelletier, H., Kraut, J., Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c (1992) Science, 258, pp. 1748-1755
  • Roberts, V.A., Pique, M.E., Definition of the interaction domain for cytochrome c on cytochrome c oxidase. III. Prediction of the docked complex by a complete, systematic search (1999) J. Biol. Chem., 274, pp. 38051-38060
  • Khoa Ly, H.K., Sezer, M., Wisitruangsakul, N., Feng, J.J., Kranich, A., Millo, D., Weidinger, I.M., Hildebrandt, P., Surface-enhanced vibrational spectroscopy for probing transient interactions of proteins with biomimetic interfaces: electric field effects on structure, dynamics and function of cytochrome c (2011) FEBS J., 278, pp. 1382-1390
  • Weidinger, I.M., Murgida, D.H., Dong, W.F., Mohwald, H., Hildebrandt, P., Redox processes of cytochrome c immobilized on solid supported polyelectrolyte multilayers (2006) J. Phys. Chem. B, 110, pp. 522-529
  • Oellerich, S., Wackerbarth, H., Hildebrandt, P., Spectroscopic Characterization of Nonnative Conformational States of Cytochrome c (2002) J. Phys. Chem. B, 106, pp. 6566-6580
  • Dopner, S., Hildebrandt, P., Rosell, F.I., Mauk, A.G., Von Walter, M., Buse, G., Soulimane, T., The structural and functional role of lysine residues in the binding domain of cytochrome c in the electron transfer to cytochrome c oxidase (1999) Eur. J. Biochem., 261, pp. 379-391
  • De Biase, P.M., Doctorovich, F., Murgida, D.H., Estrin, D.A., Electric field effects on the reactivity of heme model systems (2007) Chem. Phys. Lett., 434, pp. 121-126
  • Sela, M., Schechter, B., Schechter, I., Borek, F., Antibodies to sequential and conformational determinants (1967) Cold Spring Harbor Symp. Quant. Biol., 32, pp. 537-545
  • Jemmerson, R., Antigenicity and native structure of globular proteins: low frequency of peptide reactive antibodies (1987) Proc. Natl. Acad. Sci. U. S. A., 84, pp. 9180-9184
  • Spangler, B.D., Binding to native proteins by antipeptide monoclonal antibodies (1991) J. Immunol., 146, pp. 1591-1595
  • Liu, X., Kim, C.N., Yang, J., Jemmerson, R., Wang, X., Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c (1996) Cell, 86, pp. 147-157
  • Jemmerson, R., Paterson, Y., Mapping epitopes on a protein antigen by the proteolysis of antigen-antibody complexes (1986) Science, 232, pp. 1001-1004
  • Bakan, A., Kapralov, A.A., Bayir, H., Hu, F., Kagan, V.E., Bahar, I., Inhibition of Peroxidase Activity of Cytochrome c: de Novo Compound Discovery and Validation (2015) Mol. Pharmacol., 88, p. 421
  • Koonin, E.V., Aravind, L., Origin and evolution of eukaryotic apoptosis: the bacterial connection (2002) Cell Death Differ., 9, pp. 394-404
  • Kluck, R.M., Ellerby, L.M., Ellerby, H.M., Naiem, S., Yaffe, M.P., Margoliash, E., Bredesen, D., Newmeyer, D.D., Determinants of cytochrome c pro-apoptotic activity. the role of lysine 72 trimethylation (2000) J. Biol. Chem., 275, pp. 16127-16133
  • Ascenzi, P., Marino, M., Ciaccio, C., Santucci, R., Coletta, M., Reductive nitrosylation of the cardiolipin-ferric cytochrome c complex (2014) IUBMB Life, 66, pp. 438-447
  • Ott, M., Robertson, J.D., Gogvadze, V., Zhivotovsky, B., Orrenius, S., Cytochrome c release from mitochondria proceeds by a two-step process (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 1259-1263
  • Tam, Z.Y., Cai, Y.H., Gunawan, R., Elucidating cytochrome C release from mitochondria: insights from an in silico three-dimensional model (2010) Biophys. J., 99, pp. 3155-3163
  • Garcia-Heredia, J.M., Diaz-Moreno, I., Diaz-Quintana, A., Orzáez, M., Navarro, J.A., Hervas, M., De La Rosa, M.A., Specific nitration of tyrosines 46 and 48 makes cytochrome c assemble a non-functional apoptosome (2012) FEBS Lett., 586, pp. 154-158
  • Battistuzzi, G., Borsari, M., Sola, M., Redox properties of cytochrome c (2001) Antioxid. Redox Signaling, 3, pp. 279-291

Citas:

---------- APA ----------
Hannibal, L., Tomasina, F., Capdevila, D.A., Demicheli, V., Tórtora, V., Alvarez-Paggi, D., Jemmerson, R.,..., Radi, R. (2016) . Alternative Conformations of Cytochrome c: Structure, Function, and Detection. Biochemistry, 55(3), 407-428.
http://dx.doi.org/10.1021/acs.biochem.5b01385
---------- CHICAGO ----------
Hannibal, L., Tomasina, F., Capdevila, D.A., Demicheli, V., Tórtora, V., Alvarez-Paggi, D., et al. "Alternative Conformations of Cytochrome c: Structure, Function, and Detection" . Biochemistry 55, no. 3 (2016) : 407-428.
http://dx.doi.org/10.1021/acs.biochem.5b01385
---------- MLA ----------
Hannibal, L., Tomasina, F., Capdevila, D.A., Demicheli, V., Tórtora, V., Alvarez-Paggi, D., et al. "Alternative Conformations of Cytochrome c: Structure, Function, and Detection" . Biochemistry, vol. 55, no. 3, 2016, pp. 407-428.
http://dx.doi.org/10.1021/acs.biochem.5b01385
---------- VANCOUVER ----------
Hannibal, L., Tomasina, F., Capdevila, D.A., Demicheli, V., Tórtora, V., Alvarez-Paggi, D., et al. Alternative Conformations of Cytochrome c: Structure, Function, and Detection. Biochemistry. 2016;55(3):407-428.
http://dx.doi.org/10.1021/acs.biochem.5b01385