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Abstract:

In this overview we present recent combined electrochemical, spectroelectrochemical, spectroscopic and computational studies from our group on the electron transfer reactions of cytochrome c and of the primary electron acceptor of cytochrome c oxidase, the CuA site, in biomimetic complexes. Based on these results, we discuss how protein dynamics and thermal fluctuations may impact on protein ET reactions, comment on the possible physiological relevance of these results, and finally propose a regulatory mechanism that may operate in the Cyt/CcO electron transfer reaction in vivo. This article is part of a Special Issue entitled: 18th European Bioenergetic Conference. © 2014 Elsevier B.V.

Registro:

Documento: Artículo
Título:The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer
Autor:Alvarez-Paggi, D.; Zitare, U.; Murgida, D.H.
Filiación:INQUIMAE-CONICET, Departamento de Química Inorgánica, Analítica y Química Física, Universidad de Buenos Aires, pab. 2, piso 3, C1428EHA Buenos Aires, Argentina
Palabras clave:Bioelectrochemistry; CuA; Cytochrome c; Electron transfer; Raman spectroelectrochemistry; azurin; copper ion; cytochrome c; cytochrome c oxidase; cytochrome c peroxidase; hemoprotein; histidine; methionine; plastocyanin; porphyrin; self assembled monolayer; ubiquinol cytochrome c reductase; algorithm; biomimetics; complex formation; conceptual framework; conference paper; conformational transition; crystal structure; dipole; electrochemistry; electrode; electron spin resonance; electron transport; energy transfer; Escherichia coli; ionic strength; lipid bilayer; molecular dynamics; nonhuman; nuclear magnetic resonance spectroscopy; oxidation reduction potential; oxidation reduction reaction; oxidation reduction state; pH; photosystem I; priority journal; protein protein interaction; protein secondary structure; proton transport; Raman spectrometry; static electricity; Thermus thermophilus; Bioelectrochemistry; CuA; Cytochrome c; Electron transfer; Raman spectroelectrochemistry; Amino Acid Sequence; Animals; Cytochromes c; Electron Transport; Electron Transport Complex IV; Humans; Molecular Docking Simulation; Molecular Dynamics Simulation; Molecular Sequence Data
Año:2014
Volumen:1837
Número:7
Página de inicio:1196
Página de fin:1207
DOI: http://dx.doi.org/10.1016/j.bbabio.2014.01.019
Título revista:Biochimica et Biophysica Acta - Bioenergetics
Título revista abreviado:Biochim. Biophys. Acta Bioenerg.
ISSN:00052728
CODEN:BBBEB
CAS:azurin, 12284-43-4; cytochrome c, 9007-43-6, 9064-84-0; cytochrome c oxidase, 72841-18-0, 9001-16-5; cytochrome c peroxidase, 9029-53-2; histidine, 645-35-2, 7006-35-1, 71-00-1; methionine, 59-51-8, 63-68-3, 7005-18-7; plastocyanin, 9014-09-9; porphyrin, 24869-67-8; ubiquinol cytochrome c reductase, 9027-03-6
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00052728_v1837_n7_p1196_AlvarezPaggi

Referencias:

  • Zhuang, X., Kim, H., Pereira, M.J.B., Babcock, H.P., Walter, N.G., Chu, S., Correlating structural dynamics and function in single ribozyme molecules (2002) Science, 296 (5572), pp. 1473-1476. , DOI 10.1126/science.1069013
  • Shaw, D.E., Atomic-level characterization of the structural dynamics of proteins (2010) Science, 330 (6002), pp. 341-346
  • Frauenfelder, H., A unified model of protein dynamics (2009) Proc. Natl. Acad. Sci. U. S. A., 106 (13), pp. 5129-5134
  • Bashir, Q., Scanu, S., Ubbink, M., Dynamics in electron transfer protein complexes (2011) FEBS J., 278 (9), pp. 1391-1400
  • Chohan, K.K., Protein dynamics enhance electronic coupling in electron transfer complexes (2001) J. Biol. Chem., 276 (36), pp. 34142-34147
  • Gehlen, J.N., Marchi, M., Chandler, D., Dynamics affecting the primary charge transfer in photosynthesis (1994) Science, 263 (5146), pp. 499-501
  • Kundu, P., Dua, A., Protein dynamics modulated electron transfer kinetics in early stage photosynthesis (2013) J. Chem. Phys., 138 (4), p. 045104
  • Prytkova, T.R., Kurnikov, I.V., Beratan, D.N., Coupling coherence distinguishes structure sensitivity in protein electron transfer (2007) Science, 315 (5812), pp. 622-625. , DOI 10.1126/science.1134862
  • Skourtis, S.S., Balabin, I.A., Kawatsu, T., Beratan, D.N., Protein dynamics and electron transfer: Electronic decoherence and non-Condon effects (2005) Proceedings of the National Academy of Sciences of the United States of America, 102 (10), pp. 3552-3557. , DOI 10.1073/pnas.0409047102
  • Sumi, H., Marcus, R.A., Dynamical effects in electron transfer reactions (1986) J. Chem. Phys., 84, p. 4894
  • Tan, M.-L., Balabin, I., Onuchic, J.N., Dynamics of Electron Transfer Pathways in Cytochrome c Oxidase (2004) Biophysical Journal, 86 (3), pp. 1813-1819
  • Wang, H., Lin, S., Allen, J.P., Williams, J.C., Blankert, S., Laser, C., Woodbury, N.W., Protein dynamics control the kinetics of initial electron transfer in photosynthesis (2007) Science, 316 (5825), pp. 747-750. , DOI 10.1126/science.1140030
  • Wang, H., Hao, Y., Jiang, Y., Lin, S., Woodbury, N.W., Role of protein dynamics in guiding electron-transfer pathways in reaction centers from Rhodobacter sphaeroides (2011) J. Phys. Chem. B, 116 (1), pp. 711-717
  • Wheeler, K.E., Nocek, J.M., Cull, D.A., Yatsunyk, L.A., Rosenzweig, A.C., Hoffman, B.M., Dynamic docking of cytochrome b5 with myoglobin and α-hemoglobin: Heme-neutralization "squares" and the binding of electron-transfer-reactive configurations (2007) Journal of the American Chemical Society, 129 (13), pp. 3906-3917. , DOI 10.1021/ja067598g
  • Zhuravleva, A.V., Korzhnev, D.M., Kupce, E., Arseniev, A.S., Billeter, M., Orekhov, V.Yu., Gated electron transfers and electron pathways in azurin: A NMR dynamic study at multiple fields and temperatures (2004) Journal of Molecular Biology, 342 (5), pp. 1599-1611. , DOI 10.1016/j.jmb.2004.08.001, PII S0022283604009556
  • 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 (30), pp. 9844-9848
  • Bushnell, G.W., Louie, G.V., Brayer, G.D., High-resolution three-dimensional structure of horse heart cytochrome c (1990) Journal of Molecular Biology, 214 (2), pp. 585-595. , DOI 10.1016/0022-2836(90)90200-6
  • Williams, P.A., Blackburn, N.J., Sanders, D., Bellamy, H., Stura, E.A., Fee, J.A., McRee, D.E., The Cu(A) domain of Thermus thermophilus ba3-type cytochrome C oxidase at 1.6 Å resolution (1999) Nature Structural Biology, 6 (6), pp. 509-516. , DOI 10.1038/9274
  • Marcus, R.A., Chemical and electrochemical electron-transfer theory (1964) Annu. Rev. Phys. Chem., 15 (1), pp. 155-196
  • Marcus, R.A., Electron transfer reactions in chemistry: Theory and experiment (Nobel lecture) (1993) Angew. Chem. Int. Edit., 32 (8), pp. 1111-1121
  • Dogonadze, R.R., Kuznetsov, A.M., Chernenko, A.A., Theory of homogeneous and heterogeneous electronic processes in liquids (1965) Russ. Chem. Rev., 34, pp. 759-775
  • Fawcett, W.R., Opallo, M., The kinetics of heterogeneous electron transfer reactions in polar solvents (1994) Angewandte Chemie (International Edition in English), 33 (21), pp. 2131-2143
  • Sen, R.K., Yeager, E., O'Grady, W.E., Theory of charge transfer at electrochemical interfaces (1975) Annu. Rev. Phys. Chem., 26 (1), pp. 287-314
  • Kuznetsov, A.M., Ulstrup, J., Theory of electron transfer at electrified interfaces (2000) Electrochim. Acta, 45 (1516), pp. 2339-2361
  • Ulstrup, J., Jortner, J., The effect of intramolecular quantum modes on free energy relationships for electron transfer reactions (1975) J. Chem. Phys., 63 (10), pp. 4358-4368
  • Hush, N.S., Adiabatic theory of outer sphere electron-transfer reactions in solution (1961) Trans. Faraday Soc., 57, pp. 557-580
  • Hopfield, J.J., Electron transfer between biological molecules by thermally activated tunneling (1974) Proc. Natl. Acad. Sci. U. S. A., 71 (9), p. 3640
  • Betts, J.N., Beratan, D.N., Onuchic, J.N., Mapping electron tunneling pathways: An algorithm that finds the "minimum length"/maximum coupling pathway between electron donors and acceptors in proteins (1992) J. Am. Chem. Soc., 114 (11), pp. 4043-4046
  • Skourtis, S.S., Waldeck, D.H., Beratan, D.N., Fluctuations in biological and bioinspired electron-transfer reactions (2010) Annu. Rev. Phys. Chem., 61, pp. 461-485
  • Balabin, I.A., Beratan, D.N., Skourtis, S.S., Persistence of structure over fluctuations in biological electron-transfer reactions (2008) Phys. Rev. Lett., 101 (15), pp. 158102-158106
  • Beratan, D.N., Betts, J.N., Onuchic, J.N., Protein electron transfer rates set by the bridging secondary and tertiary structure (1991) Science, 252 (5010), pp. 1285-1288
  • Hervás, M., Rosa, M.A., Tollin, G., A comparative laser-flash absorption spectroscopy study of algal plastocyanin and cytochrome c552 photooxidation by photosystem i particles from spinach (1992) Eur. J. Biochem., 203 (12), pp. 115-120
  • Hazzard, J.T., Rong, S.Y., Tollin, G., Ionic strength dependence of the kinetics of electron transfer from bovine mitochondrial cytochrome c to bovine cytochrome c oxidase (1991) Biochemistry, 30 (1), pp. 213-222
  • Ubbink, M., Ejdeback, M., Karlsson, B.G., Bendall, D.S., The structure of the complex of plastocyanin and cytochrome f, determined by paramagnetic NMR and restrained rigid-body molecular dynamics (1998) Structure, 6 (3), pp. 323-335
  • Crowley, P.B., Ubbink, M., Close encounters of the transient kind: Protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy (2003) Acc. Chem. Res., 36 (10), pp. 723-730
  • Volkov, A.N., Worrall, J.A.R., Holtzmann, E., Ubbink, M., Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR (2006) Proceedings of the National Academy of Sciences of the United States of America, 103 (50), pp. 18945-18950. , http://www.pnas.org/cgi/reprint/103/50/18945, DOI 10.1073/pnas.0603551103
  • Muresanu, L., Pristovsek, P., Lohr, F., Maneg, O., Mukrasch, M.D., Ruterjans, H., Ludwig, B., Lucke, C., The electron transfer complex between cytochrome c552 and the CuA domain of the Thermus thermophilus ba3 oxidase: A combined NMR and computational approach (2006) Journal of Biological Chemistry, 281 (20), pp. 14503-14513. , http://www.jbc.org/cgi/reprint/281/20/14503, DOI 10.1074/jbc.M601108200
  • Prime, K.L., Whitesides, G.M., Self-assembled organic monolayers: Model systems for studying adsorption of proteins at surfaces (1991) Science, 252 (5009), pp. 1164-1167
  • Samanta, D., Sarkar, A., Immobilization of bio-macromolecules on self-assembled monolayers: Methods and sensor applications (2011) Chem. Soc. Rev., 40 (5), pp. 2567-2592
  • Arya, S.K., Solanki, P.R., Datta, M., Malhotra, B.D., Recent advances in self-assembled monolayers based biomolecular electronic devices (2009) Biosens. Bioelectron., 24 (9), pp. 2810-2817
  • Chidsey, C.E., Free energy and temperature dependence of electron transfer at the metal-electrolyte interface (1991) Science, 251 (4996), pp. 919-922
  • McConnell, H.M., Intramolecular charge transfer in aromatic free radicals (1961) J. Chem. Phys., 35, pp. 508-515
  • Naleway, C.A., Curtiss, L.A., Miller, J.R., Superexchange-pathway model for long-distance electronic couplings (1991) J. Phys. Chem., 95 (22), pp. 8434-8437
  • Avila, A., Gregory, B.W., Niki, K., Cotton, T.M., An Electrochemical Approach to Investigate Gated Electron Transfer Using a Physiological Model System: Cytochrome c Immobilized on Carboxylic Acid-Terminated Alkanethiol Self-Assembled Monolayers on Gold Electrodes (2000) Journal of Physical Chemistry B, 104 (12), pp. 2759-2766. , DOI 10.1021/jp992591p
  • Chi, Q., Zhang, J., Andersen, J.E.T., Ulstrup, J., Ordered assembly and controlled electron transfer of the blue copper protein azurin at gold (111) single-crystal substrates (2001) Journal of Physical Chemistry B, 105 (20), pp. 4669-4679. , DOI 10.1021/jp0105589
  • Davis, K.L., Waldeck, D.H., Effect of deuterium substitution on electron transfer at cytochrome OSAM interfaces (2008) J. Phys. Chem. B, 112 (39), pp. 12498-12507
  • El Kasmi, A., Wallace, J.M., Bowden, E.F., Binet, S.M., Linderman, R.J., Controlling interfacial electron-transfer kinetics of cytochrome c with mixed self-assembled monolayers (1998) Journal of the American Chemical Society, 120 (1), pp. 225-226. , DOI 10.1021/ja973417m
  • Feng, J.J., Gated electron transfer of yeast iso-1 cytochrome c on SAM-coated electrodes (2008) J. Phys. Chem. B, 112, pp. 15202-15211
  • Kranich, A., Gated electron transfer of cytochrome c6 at biomimetic interfaces: A time-resolved SERR study (2009) Phys. Chem. Chem. Phys., 11 (34), pp. 7390-7397
  • Molinas, M.F., Electron transfer dynamics of Rhodothermus marinus caa3 cytochrome c domains on biomimetic films (2011) Phys. Chem. Chem. Phys., 13 (40), pp. 18088-18098
  • Murgida, D.H., Hildebrandt, P., Proton-coupled electron transfer of cytochrome c (2001) Journal of the American Chemical Society, 123 (17), pp. 4062-4068. , DOI 10.1021/ja004165j
  • Niki, K., Coupling to lysine-13 promotes electron tunneling through carboxylate-terminated alkanethiol self-assembled monolayers to cytochrome c (2003) J. Phys. Chem. B, 107 (37), pp. 9947-9949
  • Wei, J.J., Electron-transfer dynamics of cytochrome C: A change in the reaction mechanism with distance (2002) Angew. Chem. Int. Ed., 41 (24), pp. 4700-4703
  • Xu, J., Bowden, E.F., Determination of the orientation of adsorbed cytochrome c on carboxyalkanethiol self-assembled monolayers by in situ differential modification (2006) Journal of the American Chemical Society, 128 (21), pp. 6813-6822. , DOI 10.1021/ja054219v
  • Yue, H.J., On the electron transfer mechanism between cytochrome c and metal electrodes. Evidence for dynamic control at short distances (2006) J. Phys. Chem. B, 110 (40), pp. 19906-19913
  • Zuo, P., Albrecht, T., Barker, P.D., Murgida, D.H., Hildebrandt, P., Interfacial redox processes of cytochrome b562 (2009) Phys. Chem. Chem. Phys., 11 (34), pp. 7430-7436
  • Fujita, K., Nakamura, N., Ohno, H., Leigh, B.S., Niki, K., Gray, H.B., Richards, J.H., Mimicking protein-protein electron transfer: Voltammetry of Pseudomonas aeruginosa azurin and the Thermus thermophilus CuA domain at ω-derivatized self-assembled-monolayer gold electrodes (2004) Journal of the American Chemical Society, 126 (43), pp. 13954-13961. , DOI 10.1021/ja047875o
  • 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 (8), pp. 1578-1586
  • 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 (11), pp. 854-861
  • Murgida, D.H., Hildebrandt, P., Disentangling interfacial redox processes of proteins by SERR spectroscopy (2008) Chem. Soc. Rev., 37 (5), pp. 937-945
  • Moskovits, M., Suh, J.S., Surface selection rules for surface-enhanced Raman spectroscopy: Calculations and application to the surface-enhanced Raman spectrum of phthalazine on silver (1984) J. Phys. Chem., 88 (23), pp. 5526-5530
  • Wackerbarth, H., Klar, U., Gunther, W., Hildebrandt, P., Novel time-resolved surface-enhanced (resonance) Raman spectroscopic technique for studying the dynamics of interfacial processes: Application to the electron transfer reaction of cytochrome c at a silver electrode (1999) Appl. Spectrosc., 53 (3), pp. 283-291
  • Alvarez-Paggi, D., Molecular basis of coupled protein and electron transfer dynamics of cytochrome c in biomimetic complexes (2010) J. Am. Chem. Soc., 132 (16), pp. 5769-5778
  • Ly, H.K., Thermal fluctuations determine the electron-transfer rates of cytochrome c in electrostatic and covalent complexes (2010) ChemPhysChem, 11 (6), pp. 1225-1235
  • Paggi, D.A., Computer simulation and SERR detection of cytochrome c dynamics at SAM-coated electrodes (2009) Electrochim. Acta, 54 (22), pp. 4963-4970
  • Koppenol, W.H., Rush, J.D., Mills, J.D., Margoliash, E., The dipole-moment of cytochrome-C (1991) Mol. Biol. Evol., 8 (4), pp. 545-558
  • Clarke, R.J., Dipole potential of phospholipid membranes and methods for its detection (2001) Advances in Colloid and Interface Science, 89-90, pp. 263-281. , DOI 10.1016/S0001-8686(00)00061-0
  • Smith, C.P., Dwhite, H.S., Theory of the interfacial potential distribution and reversible voltammetric response of electrodes coated with electroactive molecular films (1992) Anal. Chem., 64 (20), pp. 2398-2405
  • Pelletier, H., Kraut, J., Crystal structure of a complex between electron transfer partners, cytochrome c peroxidase and cytochrome c (1992) Science, 258 (5089), pp. 1748-1755
  • Lange, C., Hunte, C., Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c (2002) Proceedings of the National Academy of Sciences of the United States of America, 99 (5), pp. 2800-2805. , DOI 10.1073/pnas.052704699
  • Roberts, V.A., Pique, M.E., Definition of the interaction domain for cytochrome c on cytochrome c oxidase (1999) J. Biol. Chem., 274 (53), pp. 38051-38060
  • Onuchic, J.N., Beratan, D.N., Winkler, J.R., Gray, H.B., Pathway analysis of protein electron-transfer reactions (1992) Annu. Rev. Bioph. Biom., 21 (1), pp. 349-377
  • Beratan, D.N., Onuchic, J.N., Winkler, J.R., Gray, H.B., Electron-tunneling pathways in proteins (1992) Science, 258 (5089), pp. 1740-1741
  • Alvarez-Paggi, D., Disentangling electron tunneling and protein dynamics of cytochrome c through a rationally designed surface mutation (2013) J. Phys. Chem. B, 117 (20), pp. 6061-6068
  • Marcus, R.A., On the theory of oxidation-reduction reactions involving electron transfer. i (1956) J. Chem. Phys., 24 (5), pp. 966-978
  • Babini, E., Bertini, I., Borsari, M., Capozzi, F., Luchinat, C., Zhang, X., Moura, G.L.C., Gray, H.B., Bond-mediated electron tunneling in ruthenium-modified high-potential iron-sulfur protein [13] (2000) Journal of the American Chemical Society, 122 (18), pp. 4532-4533. , DOI 10.1021/ja994472t
  • Miyashita, O., Okamura, M.Y., Onuchic, J.N., Theoretical understanding of the interprotein electron transfer between cytochrome c2 and the photosynthetic reaction center (2003) J. Phys. Chem. B, 107 (5), pp. 1230-1241
  • Winkler, J.R., Wittung-Stafshede, P., Leckner, J., Malmstrom, B.G., Gray, H.B., Effects of folding on metalloprotein active sites (1997) Proceedings of the National Academy of Sciences of the United States of America, 94 (9), pp. 4246-4249. , DOI 10.1073/pnas.94.9.4246
  • Huber, R., E. Antonini plenary lecture A structural basis of light energy and electron transfer in biology (1991) EJB Reviews 1990, pp. 25-47. , Springer
  • Lancaster, K.M., Electron transfer reactivity of type zero Pseudomonas aeruginosa azurin (2011) J. Am. Chem. Soc., 133 (13), pp. 4865-4873
  • Tipmanee, V., Oberhofer, H., Park, M., Kim, K.S., Blumberger, J., Prediction of reorganization free energies for biological electron transfer: A comparative study of Ru-modified cytochromes and a 4-helix bundle protein (2010) J. Am. Chem. Soc., 132 (47), pp. 17032-17040
  • Sigfridsson, E., Olsson, M.H.M., Ryde, U., A comparison of the inner-sphere reorganization energies of cytochromes, iron-sulfur clusters, and blue copper proteins (2001) Journal of Physical Chemistry B, 105 (23), pp. 5546-5552. , DOI 10.1021/jp0037403
  • Bortolotti, C.A., The reorganization energy in cytochrome c is controlled by the accessibility of the heme to the solvent (2011) J. Phys. Chem. Lett., 2 (14), pp. 1761-1765
  • Muegge, I., Qi, P.X., Wand, A.J., Chu, Z.T., Warshel, A., The reorganization energy of cytochrome c revisited (1997) Journal of Physical Chemistry B, 101 (5), pp. 825-836
  • Jasaitis, A., Johansson, M.P., Wikström, M., Vos, M.H., Verkhovsky, M.I., Nanosecond electron tunneling between the hemes in cytochrome bo 3 (2007) Proc. Natl. Acad. Sci. U. S. A., 104 (52), pp. 20811-20814
  • Kim, Y.C., Wikström, M., Hummer, G., Kinetic gating of the proton pump in cytochrome c oxidase (2009) Proc. Natl. Acad. Sci. U. S. A., 106 (33), pp. 13707-13712
  • Andrew, S.M., Thomasson, K.A., Northrup, S.H., Simulation of electron-transfer self-exchange in cytochrome c and cytochrome b5 (1993) J. Am. Chem. Soc., 115 (13), pp. 5516-5521
  • Dolidze, T.D., Rondinini, S., Vertova, A., Waldeck, D.H., Khoshtariya, D.E., Impact of self-assembly composition on the alternate interfacial electron transfer for electrostatically immobilized cytochrome C (2007) Biopolymers, 87 (1), pp. 68-73. , DOI 10.1002/bip.20789
  • Fedurco, M., Augustynski, J., Indiani, C., Smulevich, G., Antalik, M., Bano, M., Sedlak, E., Dawson, J.H., Electrochemistry of unfolded cytochrome c in neutral and acidic urea solutions (2005) Journal of the American Chemical Society, 127 (20), pp. 7638-7646. , DOI 10.1021/ja050321g
  • Gray, H.B., Winkler, J.R., Electron tunneling through proteins (2003) Quarterly Reviews of Biophysics, 36 (3), pp. 341-372. , DOI 10.1017/S0033583503003913
  • Nahir, T.M., Clark, R.A., Bowden, E.F., Linear-sweep voltammetry of irreversible electron-transfer in surface-confined species using the Marcus theory (1994) Anal. Chem., 66 (15), pp. 2595-2598
  • Shafiey, H., Ghourchian, H., Mogharrab, N., How does reorganization energy change upon protein unfolding? Monitoring the structural perturbations in the heme cavity of cytochrome c (2008) Biophys. Chem., 134 (3), pp. 225-231
  • Song, S., Clark, R.A., Bowden, E.F., Tarlov, M.J., Characterization of cytochrome c alkanethiolate structures prepared by self-assembly on gold (1993) J. Phys. Chem., 97 (24), pp. 6564-6572
  • Terrettaz, S., Cheng, J., Miller, C.J., Guiles, R.D., Kinetic parameters for cytochrome c via insulated electrode voltammetry (1996) Journal of the American Chemical Society, 118 (33), pp. 7857-7858. , DOI 10.1021/ja960866y
  • Matyushov, D.V., Nanosecond stokes shift dynamics, dynamical transition, and gigantic reorganization energy of hydrated heme proteins (2011) J. Phys. Chem. B, 115 (36), pp. 10715-10724
  • Gray, H.B., Winkler, J.R., Electron transfer in proteins (1996) Annual Review of Biochemistry, 65, pp. 537-561
  • Ying, T., Tyrosine-67 in cytochrome c is a possible apoptotic trigger controlled by hydrogen bonds via a conformational transition (2009) Chem. Commun., 30, pp. 4512-4514
  • Abriata, L.A., Nitration of solvent-exposed tyrosine 74 on cytochrome c triggers heme iron-methionine 80 bond disruption (2009) J. Biol. Chem., 284 (1), pp. 17-26
  • Berghuis, A.M., The role of a conserved internal water molecule and its associated hydrogen bond network in cytochrome c (1994) J. Mol. Biol., 236 (3), pp. 786-799
  • 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 (10), pp. 3524-3528
  • 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) Journal of Pharmaceutical and Biomedical Analysis, 19 (1-2), pp. 115-125. , DOI 10.1016/S0731-7085(98)00291-X, PII S073170859800291X
  • Battistuzzi, G., Role of Met80 and Tyr67 in the low-pH conformational equilibria of cytochrome c (2012) Biochemistry, 51 (30), pp. 5967-5978
  • García-Heredia, J.M., Nitration of tyrosine 74 prevents human cytochrome c to play a key role in apoptosis signaling by blocking caspase-9 activation (2010) BBA-Bioenergetics, 1797 (6), pp. 981-993
  • Zhou, P., Tian, F., Lv, F., Shang, Z., Geometric characteristics of hydrogen bonds involving sulfur atoms in proteins (2009) Proteins Struct. Funct. Bioinf., 76 (1), pp. 151-163
  • Alvarez-Paggi, D., Electrostatically driven second-sphere ligand switch between high and low reorganization energy forms of native cytochrome c (2013) J. Am. Chem. Soc., 135 (11), pp. 4389-4397
  • Kokhan, O., Wraight, C.A., Tajkhorshid, E., The binding interface of cytochrome c and cytochrome c1 in the bc1 complex: Rationalizing the role of key residues (2010) Biophys. J., 99 (8), pp. 2647-2656
  • Takayama, S.J., Electron transfer from cytochrome c to cupredoxins (2009) J. Biol. Inorg. Chem., 14 (6), pp. 821-828
  • Beinert, H., Copper A of cytochrome c oxidase, a novel, long-embattled, biological electron-transfer site (1997) European Journal of Biochemistry, 245 (3), pp. 521-532
  • Brown, K., Tegoni, M., Prudencio, M., Pereira, A.S., Besson, S., Moura, J.J., Moura, I., Cambillau, C., A novel type of catalytic copper cluster in nitrous oxide reductase (2000) Nature Structural Biology, 7 (3), pp. 191-195. , DOI 10.1038/73288
  • Haltia, T., Crystal structure of nitrous oxide reductase from Paracoccus denitrificans at 1.6 Å resolution (2003) Biochem. J., 369 (PART 1), p. 77
  • Babcock, G.T., Wikström, M., Oxygen activation and the conservation of energy in cell respiration (1992) Nature, 356 (6367), pp. 301-309
  • Wikstrom, M., Cytochrome c oxidase: 25 Years of the elusive proton pump (2004) Biochimica et Biophysica Acta - Bioenergetics, 1655 (1-3), pp. 241-247. , DOI 10.1016/j.bbabio.2003.07.013, PII S0005272803002330
  • Tsukihara, T., Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å (1995) Science, 269 (5227), pp. 1069-1074
  • Iwata, S., Ostermeier, C., Ludwig, B., Michel, H., Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans (1995) Nature, 376 (6542), pp. 660-668
  • Slutter, C.E., Water-soluble, recombinant CuA-domain of the cytochrome ba3 subunit II from Thermus thermophilus (1996) Biochemistry, 35 (11), pp. 3387-3395
  • Van Der Oost, J., Restoration of a lost metal-binding site: Construction of two different copper sites into a subunit of the E. Coli cytochrome o quinol oxidase complex (1992) EMBO J., 11 (9), p. 3209
  • Dennison, C., Vijgenboom, E., De Vries, S., Van Der Oost, J., Canters, G.W., Introduction of a CuA site into the blue copper protein amicyanin from Thiobacillus versutus (1995) FEBS Lett., 365 (1), pp. 92-94
  • Wilmanns, M., Lappalainen, P., Kelly, M., Sauer-Eriksson, E., Saraste, M., Crystal structure of the membrane-exposed domain from a respiratory quinol oxidase complex with an engineered dinuclear copper center (1995) Proc. Natl. Acad. Sci. U. S. A., 92 (26), p. 11955
  • Uchida, A., Kusano, T., Mogi, T., Anraku, Y., Sone, N., Expression of the Escherichia coli bo-type ubiquinol oxidase with a chimeric subunit II having the Cu(A)-Cytochrome c domain from the thermophilic bacillus caa3-type cytochrome c oxidase (1997) Journal of Biochemistry, 122 (5), pp. 1004-1009
  • Dennison, C., Vijgenboom, E., Hagen, W.R., Canters, G.W., Loop-directed mutagenesis converts amicyanin from Thiobacillus versutus into a novel blue copper protein (1996) Journal of the American Chemical Society, 118 (31), pp. 7406-7407. , DOI 10.1021/ja953256r
  • Jones, L.H., Liu, A., Davidson, V.L., An Engineered CUA Amicyanin Capable of Intermolecular Electron Transfer Reactions (2003) Journal of Biological Chemistry, 278 (47), pp. 47269-47274. , DOI 10.1074/jbc.M308863200
  • Hay, M., Richards, J.H., Lu, Y., Construction and characterization of an azurin analog for the purple copper site in cytochrome c oxidase (1996) Proc. Natl. Acad. Sci. U. S. A., 93 (1), p. 461
  • Hay, M.T., Ang, M.C., Camelin, D.R., Solomon, E.I., Antholine, W.E., Ralle, M., Blackburn, N.J., Lu, Y., Spectroscopic Characterization of an Engineered Purple CuA Center in Azurin (1998) Inorganic Chemistry, 37 (2), pp. 191-198
  • Harkins, S.B., Peters, J.C., Amido-Bridged Cu2N2 Diamond Cores that Minimize Structural Reorganization and Facilitate Reversible Redox Behavior between a Cu1Cu1 and a Class III Delocalized Cu1.5Cu 1.5 Species (2004) Journal of the American Chemical Society, 126 (9), pp. 2885-2893. , DOI 10.1021/ja037364m
  • He, C., Lippard, S.J., Synthesis and characterization of several dicopper (I) complexes and a spin-delocalized dicopper (I, II) mixed-valence complex using a 1, 8-naphthyridine-based dinucleating ligand (2000) Inorg. Chem., 39 (23), pp. 5225-5231
  • Gupta, R., Zhang, Z.H., Powell, D., Hendrich, M.P., Borovik, A.S., Synthesis and characterization of completely delocalized mixed-valent dicopper complexes (2002) Inorg. Chem., 41 (20), pp. 5100-5106
  • Savelieff, M.G., Lu, Y., PH dependent copper binding properties of a CuA azurin variant with both bridging cysteines replaced with serines (2008) Inorg. Chim. Acta, 361 (4), pp. 1087-1094
  • Harding, C., McKee, V., Nelson, J., Highly delocalized Cu (I)/Cu (II); A coppercopper bond? (1991) J. Am. Chem. Soc., 113 (25), pp. 9684-9685
  • Barr, M.E., Smith, P.H., Antholine, W.E., Spencer, B., Crystallographic, spectroscopic and theoretical studies of an electron-deiocalized Cu (1.5)-Cu (1.5) complex (1993) J. Chem. Soc. Chem. Commun., 21, pp. 1649-1652
  • Farrar, J.A., Spectroscopic studies on the average-valence copper site Cu23 + (1995) Inorg. Chem., 34 (6), pp. 1302-1303
  • Farrar, J.A., Grinter, R., Neese, F., Nelson, J., Thomson, A.J., The electronic structure of the mixed-valence copper dimer [Cu2{N (CH2CH2N = CHCH = NCH2CH2)3 N}]3 + (1997) J. Chem. Soc. Dalton, pp. 4083-4088
  • Al-Obaidi, A., Baranovic, G., Coyle, J., Coates, C.G., McGarvey, J.J., McKee, V., Nelson, J., Raman Spectroscopy of Three Average-Valence Dicopper Cryptates: Evidence for Copper-Copper Bonding (1998) Inorganic Chemistry, 37 (14), pp. 3567-3574
  • Houser, R.P., Halfen, J.A., Young, Jr.V.G., Blackburn, N.J., Tolman, W.B., Structural characterization of the first example of a bis (μ-thiolato) dicopper (II) complex. Relevance to proposals for the electron transfer sites in cytochrome c oxidase and nitrous oxide reductase (1995) J. Am. Chem. Soc., 117 (43), pp. 10745-10746
  • Houser, R.P., Young, Jr.V.G., Tolman, W.B., A thiolate-bridged, fully delocalized mixed-valence dicopper (I, II) complex that models the CuA biological electron-transfer site (1996) J. Am. Chem. Soc., 118 (8), pp. 2101-2102
  • Alvarez-Paggi, D., Abriata, L.A., Murgida, D.H., Vila, A.J., Native CuA redox sites are largely resilient to pH variations within physiological range (2013) Chem. Commun., 49 (47), pp. 5381-5383
  • Ledesma, G.N., Murgida, D.H., Hoang, K.L., Wackerbarth, H., Ulstrup, J., Costa-Filho, A.J., Vila, A.J., The met axial ligand determines the redox potential in CuA sites (2007) Journal of the American Chemical Society, 129 (39), pp. 11884-11885. , DOI 10.1021/ja0731221
  • Abriata, L.A., Alternative ground states enable pathway switching in biological electron transfer (2012) Proc. Natl. Acad. Sci., 109 (43), pp. 17348-17353
  • Ramirez, B.E., Malmström, B.G., Winkler, J.R., Gray, H.B., The currents of life: The terminal electron-transfer complex of respiration (1995) Proc. Natl. Acad. Sci. U. S. A., 92 (26), p. 11949
  • Farver, O., Chen, Y., Fee, J.A., Pecht, I., Electron transfer among the CuA-, heme b- and a 3-centers of Thermus thermophilus cytochrome ba3 (2006) FEBS Letters, 580 (14), pp. 3417-3421. , DOI 10.1016/j.febslet.2006.05.013, PII S0014579306006004
  • Brzezinski, P., Internal electron-transfer reactions in cytochrome c oxidase (1996) Biochemistry, 35 (18), pp. 5611-5615. , DOI 10.1021/bi960260m
  • Randall, D.W., Gamelin, D.R., Lacroix, L.B., Solomon, E.I., Electronic structure contributions to electron transfer in blue Cu and CuA (2000) J. Biol. Inorg. Chem., 5 (1), pp. 16-29
  • Bertini, I., Bren, K.L., Clemente, A., Fee, J.A., Gray, H.B., Luchinat, C., Malmstrom, B.G., Slutter, C.E., The Cu(A) center of a soluble domain from Thermus cytochrome ba 3. An NMR investigation of the paramagnetic protein (1996) Journal of the American Chemical Society, 118 (46), pp. 11658-11659. , DOI 10.1021/ja9621410, PII S0002786396021415
  • Kroneck, P.M.H., Antholine, W.E., Kastrau, D.H.W., Buse, G., Steffens, G.C.M., Zumft, W.G., Multifrequency EPR evidence for a bimetallic center at the Cu(A) site in cytochrome c oxidase (1990) FEBS Letters, 268 (1), pp. 274-276. , DOI 10.1016/0014-5793(90)81026-K
  • Hwang, H.J., Lu, Y., PH-dependent transition between delocalized and trapped valence states of a CuA center and its possible role in proton-coupled electron transfer (2004) Proc. Natl. Acad. Sci. U. S. A., 101 (35), p. 12842
  • Lukoyanov, D., Berry, S.M., Lu, Y., Antholine, W.E., Scholes, C.P., Role of the coordinating histidine in altering the mixed valency of CuA: An electron nuclear double resonance-electron paramagnetic resonance investigation (2002) Biophysical Journal, 82 (5), pp. 2758-2766
  • Xie, X., Gorelsky, S.I., Sarangi, R., Garner, D.K., Hee, J.H., Hodgson, K.O., Hedman, B., Solomon, E.I., Perturbations to the geometric and electronic structure of the Cu A site: Factors that influence derealization and their contributions to electron transfer (2008) Journal of the American Chemical Society, 130 (15), pp. 5194-5205. , DOI 10.1021/ja7102668
  • Farver, O., Hwang, H.J., Lu, Y., Pecht, I., Reorganization energy of the CuA center in purple azurin: Impact of the mixed valence-to-trapped valence state transition (2007) Journal of Physical Chemistry B, 111 (24), pp. 6690-6694. , DOI 10.1021/jp0672555
  • Hwang, H.J., Berry, S.M., Nilges, M.J., Lu, Y., Axial methionine has much less influence on reduction potentials in a CuA center than in a blue copper center (2005) Journal of the American Chemical Society, 127 (20), pp. 7274-7275. , DOI 10.1021/ja0501114
  • Li, H., Webb, S.P., Ivanic, J., Jensen, J.H., Determinants of the relative reduction potentials of type-1 copper sites in proteins (2004) Journal of the American Chemical Society, 126 (25), pp. 8010-8019. , DOI 10.1021/ja049345y
  • John, F., Kanbi, L.D., Richard, W., Hasnain, S.S., Role of the axial ligand in type 1 Cu centers studied by point mutations of Met148 in rusticyanin (1999) Biochemistry, 38 (39), pp. 12675-12680
  • Farrar, J.A., Neese, F., Lappalainen, P., Kroneck, P.M.H., Saraste, M., Zumft, W.G., Thomson, A.J., The electronic structure of Cu(A): A novel mixed-valence dinuclear copper electron-transfer center (1996) Journal of the American Chemical Society, 118 (46), pp. 11501-11514. , DOI 10.1021/ja9618715, PII S0002786396018719
  • Gorelsky, S.I., Xie, X., Chen, Y., Fee, J.A., Solomon, E.I., The two-state issue in the mixed-valence binuclear CuA center in cytochrome c oxidase and N2O reductase (2006) Journal of the American Chemical Society, 128 (51), pp. 16452-16453. , DOI 10.1021/ja067583i
  • Neese, F., Zumft, W.G., Antholine, W.E., Kroneck, P.M.H., The purple mixed-valence Cu(A) center in nitrous-oxide reductase: EPR of the copper-63-, copper-65-, and both copper-65- and [15N]histidine- enriched enzyme and a molecular orbital interpretation (1996) Journal of the American Chemical Society, 118 (36), pp. 8692-8699. , DOI 10.1021/ja960125x
  • Neese, F., Kappl, R., Huttermann, J., Zumft, W.G., Kroneck, P.M.H., Probing the ground state of the purple mixed valence CU(A) center in nitrous oxide reductase: A CW ENDOR (X-band) study of the 65Cu, 15N- histidine labeled enzyme and interpretation of hyperfine couplings by molecular orbital calculations (1998) Journal of Biological Inorganic Chemistry, 3 (1), pp. 53-67. , DOI 10.1007/s007750050207
  • Abriata, L.A., Ledesma, G.N., Pierattelli, R., Vila, A.J., Electronic structure of the ground and excited states of the Cu A site by NMR spectroscopy (2009) J. Am. Chem. Soc., 131 (5), pp. 1939-1946
  • Olsson, M.H.M., Ryde, U., Geometry, reduction potential, and reorganization energy of the binuclear Cua site, studied by density functional theory (2001) Journal of the American Chemical Society, 123 (32), pp. 7866-7876. , DOI 10.1021/ja010315u
  • Gamelin, D.R., Randall, D.W., Hay, M.T., Houser, R.P., Mulder, T.C., Canters, G.W., De Vries, S., Solomon, E.I., Spectroscopy of mixed-valence Cu(A)-type centers: Ligand-field control of ground-state properties related to electron transfer (1998) Journal of the American Chemical Society, 120 (21), pp. 5246-5263. , DOI 10.1021/ja973161k
  • George, S.D.B., A quantitative description of the ground-state wave function of Cu A by X-ray absorption spectroscopy: Comparison to plastocyanin and relevance to electron transfer (2001) J. Am. Chem. Soc., 123 (24), pp. 5757-5767
  • Giudici-Orticoni, M.T., Guerlesquin, F., Bruschi, M., Nitschke, W., Interaction-induced redox switch in the electron transfer complex rusticyanin-cytochrome c4 (1999) J. Biol. Chem., 274 (43), pp. 30365-30369
  • Diaz-Moreno, I., Diaz-Quintana, A., Diaz-Moreno, S., Subias, G., De La Rosa, M.A., Transient binding of plastocyanin to its physiological redox partners modifies the copper site geometry (2006) FEBS Letters, 580 (26), pp. 6187-6194. , DOI 10.1016/j.febslet.2006.10.020, PII S0014579306012324
  • Wang, L., Waldeck, D.H., Denaturation of cytochrome c and its peroxidase activity when immobilized on SAM films (2008) Journal of Physical Chemistry C, 112 (5), pp. 1351-1356. , DOI 10.1021/jp076807w
  • Kagan, V.E., Cytochrome c/cardiolipin relations in mitochondria: A kiss of death (2009) Free Radic. Biol. Med., 46 (11), pp. 1439-1453

Citas:

---------- APA ----------
Alvarez-Paggi, D., Zitare, U. & Murgida, D.H. (2014) . The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer. Biochimica et Biophysica Acta - Bioenergetics, 1837(7), 1196-1207.
http://dx.doi.org/10.1016/j.bbabio.2014.01.019
---------- CHICAGO ----------
Alvarez-Paggi, D., Zitare, U., Murgida, D.H. "The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer" . Biochimica et Biophysica Acta - Bioenergetics 1837, no. 7 (2014) : 1196-1207.
http://dx.doi.org/10.1016/j.bbabio.2014.01.019
---------- MLA ----------
Alvarez-Paggi, D., Zitare, U., Murgida, D.H. "The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer" . Biochimica et Biophysica Acta - Bioenergetics, vol. 1837, no. 7, 2014, pp. 1196-1207.
http://dx.doi.org/10.1016/j.bbabio.2014.01.019
---------- VANCOUVER ----------
Alvarez-Paggi, D., Zitare, U., Murgida, D.H. The role of protein dynamics and thermal fluctuations in regulating cytochrome c/cytochrome c oxidase electron transfer. Biochim. Biophys. Acta Bioenerg. 2014;1837(7):1196-1207.
http://dx.doi.org/10.1016/j.bbabio.2014.01.019