Reactions of electron-transfer proteins at electrodes

Studies of electron-transfer reactions of redox proteins have, in recent years, attracted widespread interest and attention. Progress has been evident from both physical and biological standpoints, with the increasing availability of three-dimensional structural data for many small electron-transfer proteins prompting a variety of systematic investigations (Isied, 1985). Most recently, attention has been directed towards questions concerning the elementary transfer of electrons between spatially remote redox sites, and the nature of protein–protein interactions which, for intermolecular processes, stabilize specific precursor complexes which may be optimally juxtaposed for electron-transfer. These and other issues, including the necessary reversibility of protein interfacial interactions and the dynamic properties of proteins as carriers of electrons in biological electron-transport systems, are now being addressed in the rapidly emerging field of direct (unmediated) protein electrochemistry. It is our intention in this article to discuss developments made in this area and highlight points which we believe to have the most bearing on our current understanding of diffusion-dominated, protein-mediated electron transport at electrode surfaces. First we shall outline some basic considerations which are best considered with reference to homogeneous systems.

[1]  M. Senda,et al.  Electrochemical behavior of ferredoxins adsorbed on mercury electrode surface. Cyclic d.c. and a.c. voltammetric studies with hanging mercury drop electrode. , 1979 .

[2]  Richard S. Nicholson,et al.  Theory and Application of Cyclic Voltammetry for Measurement of Electrode Reaction Kinetics. , 1965 .

[3]  C. Anderson,et al.  Electrochemistry of cytochrome c at single carbon fiber electrodes , 1984 .

[4]  H. C. Freeman.  ELECTRON TRANSFER IN ‘BLUE’ COPPER PROTEINS , 1981 .

[5]  W. Norde,et al.  Thermodynamics of protein adsorption. Theory with special reference to the adsorption of human plasma albumin and bovine pancreas ribonuclease at polystyrene surfaces , 1979 .

[6]  N. Walton,et al.  Electrochemically driven respiration in mitochondria and Paracoccus denitrificans , 1983, FEBS letters.

[7]  E. Margoliash,et al.  Guided by electrostatics, a textbook protein comes of age , 1983 .

[8]  H. Hill,et al.  The enzyme-catalysed electrochemical conversion of p-cresol into p-hydroxybenzaldehyde , 1985 .

[9]  T. Cotton,et al.  Reaction of redox proteins at a 4,4′-bipyridyl-modified carbon paste electrode , 1983 .

[10]  E. Margoliash,et al.  The asymmetric distribution of charges on the surface of horse cytochrome c. Functional implications. , 1982, The Journal of biological chemistry.

[11]  Jan F. Chlebowski,et al.  Cyclic voltammetry and derivative cyclic voltabsorptometry of purified horse heart cytochrome c at tin-doped indium oxide optically transparent electrodes , 1982 .

[12]  I. Taniguchi,et al.  Purines as new promoters for the voltammetric response of horse heart cytochrome c at a gold electrode , 1984 .

[13]  Masao Kakudo,et al.  X-Ray Analysis of a [2Fe-2S] Ferredoxin from ‘Spirulina platensis. Main Chain Fold and Location of Side Chains at 2.5 Å Resolution , 1981 .

[14]  A. Cass,et al.  Ferricinium ion as an electron acceptor for oxido-reductases , 1985 .

[15]  F. Scheller,et al.  Interfacial behaviour and cathodic reduction of globular proteins , 1976 .

[16]  R. Thorneley,et al.  Nitrogenase of Klebsiella pneumoniae. Kinetics of the dissociation of oxidized iron protein from molybdenum-iron protein: identification of the rate-limiting step for substrate reduction. , 1983, The Biochemical journal.

[17]  I. Taniguchi,et al.  Surface enhanced Raman scattering study of horse heart cytochrome c at a silver electrode in the presence of bis(4-pyridyl)disulfide and purine , 1984 .

[18]  R. S. Nicholson,et al.  Theory of Stationary Electrode Polarography. Single Scan and Cyclic Methods Applied to Reversible, Irreversible, and Kinetic Systems. , 1964 .

[19]  F. M. Hawkridge,et al.  Heterogeneous electron-transfer kinetic parameters of metalloproteins as studied by channel-flow hydrodynamic voltammetry , 1983 .

[20]  B. Hoffman,et al.  Temperature dependence of long-range electron transfer in [Zn,FeIII] hybrid hemoglobin , 1984 .

[21]  F. Richards,et al.  Electrostatic orientation during electron transfer between flavodoxin and cytochrome c , 1983, Nature.

[22]  H. Hill,et al.  Homogeneous ferrocene-mediated amperometric immunoassay. , 1986, Analytical chemistry.

[23]  M. G. Segal,et al.  Kinetic Studies on 1:1 Electron-Transfer Reactions Involving Blue Copper Proteins. 1. Evidence for an Unreactive Form of the Reduced Protein (pH<5) and for Protein-Complex Association in Reactions of Parsley (and Spinach) Plastocyanin , 1978 .

[24]  E. Margoliash,et al.  Species specificity of long-range electron transfer within the complex between zinc-substituted cytochrome c peroxidase and cytochrome c , 1985 .

[25]  H. Hill,et al.  Electrochemistry of horse heart cytochrome c , 1979 .

[26]  A. Hamnett,et al.  The determination, by ellipsometry, of the mode of adsorption on gold of some promoters of redox-protein direct electrochemistry , 1986 .

[27]  J. Rusling,et al.  Electrochemical and electron spectroscopic studies of highly polished glassy carbon electrodes. , 1985, Analytical chemistry.

[28]  E. Stellwagen.  Haem exposure as the determinate of oxidation–reduction potential of haem proteins , 1978, Nature.

[29]  N. Sutin,et al.  A comparison of the rates of electron exchange reactions of ammine complexes of ruthenium(II) and -(III) with the predictions of adiabatic, outer-sphere electron transfer models , 1979 .

[30]  C. D. Crawley,et al.  Spectroelectrochemical determination of the heterogeneous electron transfer kinetics of soluble spinach ferredoxin. , 1981, Biochemical and biophysical research communications.

[31]  P. Wright,et al.  NMR study of the interaction of plastocyanin with chromium(II) analogues of inorganic electron transfer reagents. , 1980, Biochimica et biophysica acta.

[32]  H. Gray,et al.  Distances of electron transfer to and from metalloprotein redox sites in reactions with inorganic complexes , 1980 .

[33]  C. A. Lewis,et al.  Kinetics and mechanisms of reduction of rusticyanin, a blue copper protein from Thiobacillus ferrooxidans, by inorganic cations , 1985 .

[34]  F. Scheller,et al.  Radiochemische und elektrochemische untersuchung der adsorption von cytochrom c an der phasengrenze elektrolyt/quecksilber , 1976 .

[35]  H. Beinert,et al.  Mössbauer studies of beef heart aconitase: evidence for facile interconversions of iron-sulfur clusters. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[36]  M. Harmer,et al.  The direct electrochemistry of redox proteins at metal oxide electrodes , 1985 .

[37]  H. Gray,et al.  Kinetics of intermolecular and intramolecular electron transfer from ruthenium(II) complexes to ferricytochrome c , 1984 .

[38]  R. M. Burnett,et al.  The structure of the oxidized form of clostridial flavodoxin at 1.9-A resolution. , 1974, The Journal of biological chemistry.

[39]  Nechaeva Ga.  Identification of specific carboxylate groups on cytochrome c oxidase that are involved in binding cytochrome c. , 1983 .

[40]  M. Comtat,et al.  Investigation of electron transfer between platinum and large biological molecules by thin-layer spectroelectrochemistry. , 1982, Analytical chemistry.

[41]  I. Taniguchi,et al.  Surface enhanced Raman scattering from bis (4-pyridyl)-disulfide and 4,4'-bipyridine-modified gold electrodes , 1985 .

[42]  L. C. Clark,et al.  ELECTRODE SYSTEMS FOR CONTINUOUS MONITORING IN CARDIOVASCULAR SURGERY , 1962 .

[43]  R. Parsons,et al.  Electrochemical and spectroreflectance studies of the adsorbed horse heart cytochrome c and cytochrome c3 from D. Vulgaris, miyazaki strain, at gold electrode , 1983 .

[44]  W. Norde,et al.  The adsorption of human plasma albumin and bovine pancreas ribonuclease at negatively charged polystyrene surfaces: I. Adsorption isotherms. Effects of charge, ionic strength, and temperature , 1978 .

[45]  F. M. Hawkridge,et al.  A surface-modified gold minigrid electrode which heterogeneously reduces spinach ferredoxin. , 1977, Journal of the American Chemical Society.

[46]  J. Kraut,et al.  A hypothetical model of the cytochrome c peroxidase . cytochrome c electron transfer complex. , 1980, The Journal of biological chemistry.

[47]  S. S. Isied,et al.  Electron transfer across polypeptides. 2. Amino acids and flexible dipeptide bridging ligands , 1984 .

[48]  M. Bruschi,et al.  Voltammetric determination of the redox potential of bacterial ferredoxins: Clostridium thermocellum ferredoxin , 1984 .

[49]  A. Turner,et al.  Ferrocene-mediated enzyme electrode for amperometric determination of glucose. , 1984, Analytical chemistry.

[50]  W. Norde,et al.  Ion participation in protein adsorption at solid surfaces , 1981 .

[51]  F. Armstrong,et al.  Catalysis of plastocyanin electron self‐exchange by redox‐inert multivalent cations , 1985 .

[52]  N. Sutin.  Nuclear, electronic, and frequency factors in electron transfer reactions , 1982 .

[53]  J. Hupp,et al.  The frequency factor for outer-sphere electrochemical reactions , 1983 .

[54]  S. Chapman,et al.  Kinetic studies on 1 : 1 electron-transfer reactions involving blue copper proteins. Part 6. Competitive inhibition of the [Co(phen)3]3+(phen = 1,10-phenanthroline) oxidation of parsley plastocyanin PCu(I) by redox-inactive complexes , 1983 .

[55]  F R Salemme,et al.  An hypothetical structure for an intermolecular electron transfer complex of cytochromes c and b5. , 1976, Journal of molecular biology.

[56]  W. Norde,et al.  The adsorption of HPA and Bovine Pancreas Ribonuclease at Negatively Charged Polystyrene Latices. IV. The Charge Distribution in the Adsorbed State , 1978 .

[57]  A. Hillman,et al.  Mechanism of the reduction and oxidation reaction of cytochrome c at a modified gold electrode , 1981 .

[58]  H. Bosshard,et al.  Comparison of the binding sites on cytochrome c for cytochrome c oxidase, cytochrome bc1, and cytochrome c1. Differential acetylation of lysyl residues in free and complexed cytochrome c. , 1980, The Journal of biological chemistry.

[59]  H. Hill,et al.  Investigation of the binding of inorganic complexes to blue copper proteins by 1H nmr spectroscopy, I. The interaction between the [Cr(phen)3]3+ and [Cr(CN)6]3− ions and the copper(I) form of parsley plastocyanin , 1980 .

[60]  B L Trus,et al.  Tuna cytochrome c at 2.0 A resolution. I. Ferricytochrome structure analysis. , 1977, The Journal of biological chemistry.

[61]  L. Sieker,et al.  Structure of the oxidized form of a flavodoxin at 2.5-Angstrom resolution: resolution of the phase ambiguity by anomalous scattering. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[62]  L. Sieker,et al.  The structure of rubredoxin at 1.2 A resolution. , 1979, Journal of molecular biology.

[63]  K. Uosaki,et al.  The electrochemistry of cytochrome c. Investigation of the mechanism of the 4,4′-bipyridyl surface modified gold electrode* , 1980 .

[64]  T. Cotton,et al.  Surface-enhanced Raman scattering study of bipyridyl-modified silver electrodes , 1983 .

[65]  F. Salemme.  Structure and function of cytochromes c. , 1977, Annual review of biochemistry.

[66]  Nicholas J. Walton,et al.  Surface modifiers for the promotion of direct electrochemistry of cytochrome c , 1984 .

[67]  K. Burkey,et al.  Chemical modification of spinach plastocyanin: separation and characterization of four different forms. , 1982, Biochemistry.

[68]  A. Cass,et al.  The reaction of flavocytochrome b2 with cytochrome c and ferricinium carboxylate. Comparative kinetics by cyclic voltammetry and chronoamperometry , 1985 .

[69]  I. Taniguchi,et al.  Cyclic voltammetic behavior of horse heart cytochrome c at a platinum electrode in the presence of 4,4′-bipyridine , 1982 .

[70]  Isao Taniguchi,et al.  Reversible electrochemical reduction and oxidation of cytochrome c at a bis(4-pyridyl) disulphide-modified gold electrode , 1982 .

[71]  F. Armstrong,et al.  Direct electrochemical oxidation of Clostridium pasteurianum ferredoxin , 1982 .

[72]  D. Hall,et al.  Low-temperature magnetic circular dichroism evidence for the conversion of four-iron-sulphur clusters in a ferredoxin from Clostridium pasteurianum into three-iron-sulphur clusters , 1981 .

[73]  J. A. Watkins,et al.  Electron transfer between flavodoxin semiquinone and c-type cytochromes: correlations between electrostatically corrected rate constants, redox potentials, and surface topologies. , 1984, Biochemistry.

[74]  W. Orme-Johnson,et al.  Oxidation-reduction properties of several low potential iron-sulfur proteins and of methylviologen. , 1976, Biochemistry.

[75]  F. Armstrong,et al.  Direct electrochemistry of the photosynthetic blue copper protein plastocyanin. Electrostatic promotion of rapid charge transfer at an edge-oriented pyrolytic graphite electrode , 1985 .

[76]  Theodore Kuwana,et al.  REVERSIBLE ELECTRODE REACTION OF CYTOCHROME C , 1977 .

[77]  A. Fersht.  Enzyme structure and mechanism , 1977 .

[78]  P. Wright,et al.  Acid dissociation constants for plastocyanin in the CuI state , 1985 .

[79]  M. Murata,et al.  X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution , 1978, Nature.

[80]  N. Walton,et al.  Direct electrochemistry, at modified gold electrodes, of redox proteins having negatively-charged binding domains: spinach plastocyanin and a multi-substituted carboxydinitrophenyl derivative of horse heart cytochrome c , 1985 .

[81]  Allen J. Bard,et al.  Electrochemical Methods: Fundamentals and Applications , 1980 .

[82]  F. Armstrong,et al.  Direct electrochemical reduction of ferredoxin promoted by Mg2+ , 1982 .

[83]  C. Veeger,et al.  Electrochemical behaviour of low-potential electron- transferring proteins at the mercury electrode , 2001 .

[84]  D. Eisenberg,et al.  Ferricytochrome c. I. General features of the horse and bonito proteins at 2.8 A resolution. , 1971, The Journal of biological chemistry.

[85]  I. Taniguchi,et al.  Voltammetric response of horse heart cytochrome c at a gold electrode in the presence of sulfur bridged bipyridines , 1982 .

[86]  T. Poulos,et al.  Models for the complexes formed between cytochrome b5 and the subunits of methemoglobin. , 1983, The Journal of biological chemistry.

[87]  J. Lyklema.  Proteins at solid—liquid interfaces A colloid-chemical review , 1984 .

[88]  E. Ulrich,et al.  Nuclear Magnetic Resonance Studies of Two-Iron-Two-Sulfur Ferredoxins. 4. Interactions with Redox Partners? , 1983 .

[89]  F. Millett,et al.  Electrostatic interaction of cytochrome c with cytochrome c1 and cytochrome oxidase. , 1981, The Journal of biological chemistry.

[90]  Henry N. Blount,et al.  Interfacial electrochemistry of cytochrome c at tin oxide, indium oxide, gold, and platinum electrodes , 1984 .

[91]  Robert J.P. Williams,et al.  Electrostatic interactions between organic ions , 1984 .

[92]  Kohei Uosaki,et al.  Electrochemistry of cytochrome c. Comparison of the electron transfer at a surface-modified gold electrode with that to cytochrome oxidase , 1979 .

[93]  H. Gray,et al.  Kinetics of long-distance ruthenium-to-copper electron transfer in [Pentaammineruthenium histidine-83]azurin , 1983 .

[94]  S. Itoh,et al.  Electron transfer between plastocyanin and P700 in highly-purified photosystem I reaction center complex. Effects of pH, cations, and subunit peptide composition. , 1983, Journal of biochemistry.

[95]  L. Sieker,et al.  Structure of a bacterial ferredoxin. , 1973, The Journal of biological chemistry.

[96]  T. Kuwana,et al.  Indirect coulometric titration of biological electron transport components. , 1973, Analytical chemistry.

[97]  S. Katoh,et al.  Purification and some properties of spinach plastocyanin. , 1962, Journal of biochemistry.

[98]  S. S. Isied,et al.  Ruthenium-modified cytochrome c: temperature dependence of the rate of intramolecular electron transfer , 1984 .

[99]  E. Margoliash,et al.  Mitochondrial cytochrome c: preparation and activity of native and chemically modified cytochromes c. , 1978, Methods in enzymology.

[100]  W. Lovenberg.  Iron-sulfur proteins, , 1973 .

[101]  M. Klapper,et al.  Electrochemical studies of heme proteins. Coulometric, polarographic, and combined spectroelectrochemical methods for reduction of the heme prosthetic group in cytochrome c. , 1972, Journal of the American Chemical Society.

[102]  J J Hopfield,et al.  Electron transfer between biological molecules by thermally activated tunneling. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[103]  J. Robbins,et al.  A new ferrocenophane surface derivatizing reagent for the preparation of nearly reversible electrodes for horse heart ferri-/ferrocytochrome c: 2,3,4,5-tetramethyl-1-[(dichlorosilyl)methyl][2]ferrocenophane , 1983 .

[104]  V. Massey,et al.  Oxidation-reduction properties of flavodoxin from Peptostreptococcus elsdenii. , 1969, The Journal of biological chemistry.

[105]  F. Armstrong,et al.  Surface selectivity in the direct electrochemistry of redox proteins. Contrasting behaviour at edge and basal planes of graphite , 1984 .