Abstract
This review is focused on the basic principles, the main applications, and the theoretical models developed for various redox mechanisms in protein film voltammetry, with a special emphasis to square-wave voltammetry as a working technique. Special attention is paid to the thermodynamic and kinetic parameters of relevant enzymes studied in the last decade at various modified electrodes, and their use as a platform for the detection of reactive oxygen species is also discussed. A set of recurrent formulas for simulations of different redox mechanisms of lipophilic enzymes is supplied together with representative simulated voltammograms that illustrate the most relevant voltammetric features of proteins studied under conditions of square-wave voltammetry.
Similar content being viewed by others
References
Armstrong FA (2002) Voltammetry of proteins. In: Bard AJ, Stratmann M, Wilson GS (eds) Encyclopedia of electrochemistry, vol 9. Wiley VCH, Weinheim
Armstrong FA (2002) Voltammetric investigations of iron-sulfur clusters in proteins. In: Brajter-Toth A, Chambers JQ (eds) Electroanalytical methods for biological materials. Marcel Dekker, Basel
Armstrong FA (2002) J Chem Soc Dalton 5:661–671
Armstrong FA (1997) Applications of voltammetric methods for probing the chemistry of redox proteins. In: Lenaz G, Milazzo G (eds) Bioelectrochemistry: principles and practice, vol. 5. Birkhauser Verlag AG, Basel
Barlett PN (2008) Bioelectrochemistry: fundamentals, experimental techniques and application. Wiley, Chichester
Jones AK, Lamle SE, Pershad HR, Vincent KA, Albracht SPJ, Armstrong FA (2003) Enzyme Electrokinetics: Electrochemical Studies of the Anaerobic Interconversions between Active and Inactive States of Allochromatium vinosum [NiFe]-hydrogenase. J Am Chem Soc 125:8505–8514
Wijma HJ, Jeuken LJC, Verbeet MP, Armstrong FA, Canters GW (2007) Protein film voltammetry of copper-containing nitrite reductase reveals reversible inactivation. J Am Chem Soc 129:8557–8565
Mirceski V, Komorsky-Lovric S, Lovric M (2008) In: Scholz F (ed) Square-wave voltammetry, theory and application. Springer, Berlin
Gulaboski R, Lovrić M, Mirčeski V, Bogeski I, Hoth M (2008) Protein-film voltammetry: A theoretical study of the temperature effect using square-wave voltammetry. Biophys Chem 137:49–55
Hirst J (2006) Elucidating the mechanisms of coupled electron transfer and catalytic reactions by protein film voltammetry. Biochem Biophys Acta 1757:225–239
Heering HA, Wiertz FGM, Dekker C, de Vries S (2004) Direct immobilization of native yeast iso-1 cytochrome c on bare gold: Fast electron relay to redox enzymes and zeptomole protein-film voltammetry. J Am Chem Soc 126:11103–11112
Udit AK, Hindoyan N, Hill MG, Arnold FH, Gray HB (2005) Protein-surfactant film voltammetry of wild-type and mutant cytochrome P450 BM3. Inorg Chem 44:4109–4111
Sultana N, Schenkman JB, Rusling JF (2005) Protein film electrochemistry of microsomes genetically enriched in human cytochrome P450 monooxygenases. J Am Chem Soc 127:13460–13461
Léger C, Dementin S, Bertrand P, Rousset M, Guigliarelli B (2004) Inhibition and aerobic inactivation kinetics of Desulfovibrio fructosovorans NiFe hydrogenase studied by protein film voltammetry. J Am Chem Soc 126:12162–12172
Gwyer JD, Richardson DJ, Butt JN (2006) Inhibiting Escherichia coli cytochrome c nitrite reductase: Voltammetry reveals an enzyme equipped for action despite the chemical challenges it may face in vivo. Biochem Soc Trans 34:133–135
Lu H, Li Z, Hu N (2003) Direct voltammetry and electrocatalytic properties of catalase incorporated in polyacrylamide hydrogel films. Biophys Chem 104:623–632
Shen L, Hu N (2004) Heme proteins with polyamidoamine dendrimer: Direct electrochemistry and electrocatalysis. Biochem Biophys Acta 1608:23–33
Li M, He P, Zhang Y, Hu N (2005) An electrochemical investigation of hemoglobin and catalase incorporated in collagen films. Biochem Biophys Acta 1749:43–51
Sun W, Gao R, Jiao K (2007) Electrochemistry and electrocatalysis of hemoglobin in nafion/nano- CaCO3 film on a new ionic liquid BPPF6 modified carbon paste electrode. J Phys Chem B 111:4560–4567
Stutzmann M, Garrido JA, Eickhoff M, Brandt MS (2006) Direct biofunctionalization of semiconductors: A survey. Phys Stat A 203:3424–3437
Härtl A, Schmich E, Garrido JA, Hernando J, Catharino SCR, Walter S, Feulner P, Kromka A, Steinmüller D, Stutzmann M (2004) Protein-modified nanocrystalline diamond thin films for biosensor applications. Nat Mater 3:736–742
Barker CD, Reda T, Hirst J (2007) The flavoprotein subcomplex of complex I (NADH: ubiquinone oxidoreductase) from bovine heart mitochondria: Insights into the mechanisms of NADH oxidation and NAD+ reduction from protein film voltammetry. Biochem 46:3454–3464
Gwyer JD, Richardson DJ, Butt JN (2004) Resolving complexity in the interactions of redox enzymes and their inhibitors: Contrasting mechanisms for the inhibition of a cytochrome c nitrite reductase revealed by protein film voltammetry. Biochem 43:15086–15094
Munge B, Das SK, Ilagan R, Pendon Z, Yang J, Frank HA, Rusling JF (2003) Electron transfer reactions of redox cofactors in spinach Photosystem I reaction center protein in lipid films on electrodes. J Am Chem Soc 125:12457–12463
Bernhardt PV, Santini JM (2006) Protein film voltammetry of arsenite oxidase from the chemolithioautotrophic arsenite-oxidizing bacterium NT-26. Biochem 45:2804–2809
Fujita K, Nakamura N, Ohno H, Leigh BS, Niki K, Gray HB, Richards JH (2004) Mimicking protein-protein electron transfer: Voltammetry of Pseudomonas aeruginosa azurin and the Thermus thermophilus CuA domain at ω-derivatized self-assembled-monolayer gold electrodes. J Am Chem Soc 126:13954–13961
Liu A, Wei M, Honma I, Zhou H (2005) Direct electrochemistry of myoglobin in titanate nanotubes film. Anal Chem 77:8068–8074
Salimi A, Sharifi E, Noorbakhsh A, Soltanian S (2006) Direct voltammetry and electrocatalytic properties of hemoglobin immobilized on a glassy carbon electrode modified with nickel oxide nanoparticles. Electrochem Commun 8:1499–1508
Aguey-Zinsou K-F, Bernhardt PV, Kappler U, McEwan AG (2003) Direct electrochemistry of a bacterial sulfite dehydrogenase. J Am Chem Soc 125:530–535
Frangioni B, Arnoux P, Sabaty M, Pignol D, Bertrand P, Guigliarelli B, Léger C (2004) In Rhodobacter sphaeroides respiratory nitrate reductase, the kinetics of substrate binding favors intramolecular electron transfer. J Am Chem Soc 126:1328–1329
Astuti Y, Topoglidis E, Briscoe PB, Fantuzzi A, Gilardi G, Durrant JR (2004) Proton-coupled electron transfer of flavodoxin immobilized on nanostructured tin dioxide electrodes: Thermodynamics versus kinetics control of protein redox function. J Am Chem Soc 126:8001–8009
Xu Y, Peng W, Liu X, Li G (2004) A new film for the fabrication of an unmediated H2O2 biosensor. Biosens Bioelectron 20:533–537
Udit AK, Hill MG, Gray HB (2006) Electrochemistry of cytochrome P450 BM3 in sodium dodecyl sulfate films. Langmuir 25:10854–10857
Fleming BD, Tian Y, Bell SG, Wong L-L, Urlacher V, Hill HAO (2003) Redox properties of cytochrome P450 BM3 measured by direct methods. Eur J Biochem 270:4082–4088
Udit AK, Hill MG, Bittner VG, Arnold FH, Gray HB (2004) Reduction of dioxygen catalyzed by pyrene-wired heme domain cytochrome P450 BM3 electrodes. J Am Chem Soc 126:10218–10219
Zhao L, Liu H, Hu N (2006) Electroactive films of heme protein-coated multiwalled carbon nanotubes. J Coll Int Sci 296:204–211
Vincent KA, Belsey NA, Lubitz W, Armstrong FA (2006) Rapid and reversible reactions of [NiFe]-hydrogenases with sulfide. J Am Chem Soc 128:7448–7449
Cai C, Chen J, Lu T (2004) Direct electron transfer of glucose oxidase on the carbon nanotube electrode. Sci China, Ser B Chem 47:113–119
Salimi A, Hallaj R, Soltanian S (2007) Immobilization of hemoglobin on electrodeposited cobalt-oxide nanoparticles: Direct voltammetry and electrocatalytic activity. Biophys Chem 130:122–131
Lu Q, Hu S (2006) Studies on direct electron transfer and biocatalytic properties od hemoglobin in polytetrafluoroethylene film. Chem Phys Lett 424:167–171
Cai C, Chen J (2004) Direct electron transfer and bioelectrocatalysis of hemoglobin at a carbon nanotube electrode. Anal Biochem 325:285–292
Shumyantseva VV, Ivanov YD, Bistolas N, Scheller FW, Archakov AI, Wollenberger U (2004) Direct electron transfer of cytochrome P450 2B4 at electrodes modified with nonionic detergent and colloidal clay nanoparticles. Anal Chem 76:6046–6052
Xie Y, Liu H, Hu N (2007) Layer-by-layer films of hemoglobin or myoglobin assembled with zeolite particles: Electrochemistry and electrocatalysis. Bioelectrochem 70:311–319
Cao D, Hu N (2006) Direct electron transfer between hemoglobin and pyrolytic graphite electrodes. Biophys Chem 121:209–217
Ye T, Kaur R, Wen X, Bren KL, Elliott SJ (2005) Redox properties of wild-type and heme-binding loop mutants of bacterial cytochromes C measured by direct electrochemistry. Inorg Chem 24:8999–9006
Reeves JH, Song S, Bowden EF (1993) Application of square wave voltammetry to strongly adsorbed quasireversible redox molecules. Anal Chem 65:683–688
Saccucci TM, Rusling JF (2001) Modeling square-wave voltammetry of thin protein films using Marcus theory. J Phys Chem B 105:6142–6147
Zhang J, Si-X G, Bond AM, Honeychurch MJ, Oldham KB (2005) Novel kinetic and background current selectivity in the even harmonic components of fourier transformed square-wave voltammograms of surface-confined azurin. J Phys Chem B 109:8935–8947
Jeuken LJC, Jones AK, Chapman SK, Cecchini G, Armstrong FA (2002) Electron-Transfer Mechanisms through Biological Redox Chains in Multicenter Enzymes. J Am Chem Soc 124:5702–5713
Jeuken LJC, McEvoy JP, Armstrong FA (2002) Insights into Gated Electron-Transfer Kinetics at the Electrode-Protein Interface: A Square Wave Voltammetry Study of the Blue Copper Protein Azurin. J Phys Chem B 106:2304–2313
Huang H, Hu N, Zeng Y, Zhou G (2002) Elecrochemistry and electrocatalysis with heme proteins in chitosan biopolymer films. Anal Biochem 308:141–151
Alcantara K, Munge B, Pendon Z, Frank HA, Rusling JF (2006) Thin film voltammetry of spinach photosystem II. Proton-gated electron transfer involving the Mn4 cluster. J Am Chem Soc 128:14930–14937
Xu J, Lu Y, Liu B, Xu C, Kong J (2007) Sensitively probing the cofactor redox species and photo-induced electron transfer of wild-type and pheophytin-replaced photosynthetic proteins reconstituted in self-assembled monolayers. J Solid State Electrochem 11:1689–1695
Ma L, Tian Y, Rong Z (2007) Direct electrochemistry of hemoglobin in the hyaluronic acid films. J Biochem Biophys Meth 70:657–662
Zhou Y, Hu N, Zeng Y, Rusling JF (2002) Layer-by-layer assembly of ultrathin films of hemoglobin and clay nanoparticles with electrochemical and catalytic activity. Langmuir 18:8573–8579
O’Dea JJ, Osteryoung JG (1993) Characterization of quasi-reversible surface processes by square-wave voltammetry. Anal Chem 65:3090–3097
Komorsky-Lovrić S, Lovrić M (1995) Square-wave voltammetry of quasireversible surface redox reactions. J Electroanal Chem 384:115–122
Lovrić M (1991) Modelling of surface electrochemical reactions. Elektrokhimija 27:186–195
Komorsky-Lovrić Š, Lovrić M (1995) Measurements of redox kinetics of adsorbed azobenzene by a “quasireversible maximum” in square-wave voltammetry. Electrochim Acta 40:1781–1784
Komorsky-Lovrić Š, Lovrić M (1995) Kinetic measurements of a surface confined redox reaction. Anal Chim Acta 305:248–255
Mirčeski V, Lovrić M, Jordanoski V (1999) Redox kinetic measurements of probucole using square-wave voltammetry. Electroanal 11:660–663
Mirčeski V, Lovrić M, Gulaboski R (2001) Theoretical and experimental study of the surface redox reaction involving interactions between the adsorbed particles under conditions of square-wave voltammetry. J Electroanal Chem 515:91–100
Gulaboski R, Mirčeski V, Lovrić M, Bogeski I (2005) Theoretical study of a surface electrode reaction preceded by a homogeneous chemical reaction under conditions of square-wave voltammetry. Electrochem Commun 7:515–522
Mirčeski V, Lovrić M (2000) Adsorption effects in square-wave voltammetry of an EC mechanism. Croat Chem Acta 73:305–329
Mirčeski V, Gulaboski R (2001) Surface catalytic mechanism in square-wave voltammetry. Electroanalysis 13:1326–1334
Mirčeski V, Gulaboski R (2003) The surface catalytic mechanism: A comparative study with square-wave and staircase cyclic voltammetry. J Solid State Electrochem 7:157–165
O’Dea JJ, Osteryoung JG (1997) Square-wave voltammetry for two-step surface redox reactions. Anal Chem 69:650–658
Mirčeski V, Gulaboski R (2003) A theoretical and experimental study of a two-step quasireversible surface redox reaction by square-wave voltammetry. Croat Chem Acta 76:37–48
Gulaboski R (2009) Surface ECE mechanism in protein film voltammetry-a theoretical study under conditions of square-wave voltammetry. J Solid State Electrochem 13:1015–1024
Mirceski V, Lovric M (1997) Split square-wave voltammograms of surface redox reactions. Electroanal 9:1283–1287
Halliwell B, Gutteridge JM (2001) Free radicals in biology and medicine, 3rd edn. Oxford University Press, New York
Bard AJ (2008) Toward single enzyme molecule electrochemistry. ACS Nano 2:2437–2440
Amemiya S, Bard AJ, Fan F-RF, Mirkin MV, Unwin PR (2008) Scanning electrochemical microscopy. Ann Rev Anal Chem 1:95–131
McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483
Aguey-Zinsou KF, Bernhardt PV, Leimkuehler S (2003) Protein Film Voltammetry of Rhodobacter Capsulatus Xanthine Dehydrogenase. J Am Chem Soc 125:15352–15358
Gulaboski R, Mihajlov L (2011) Catalytic mechanism in successive two-step protein-film voltammetry. Theoretical study in square-wave voltammetry. Biophys Chem 155:1–9
Nicholson RS (1968) A method based on polynomial approximations for numerical solution of volterra integral equations. J Electroanal Chem 16:145–151
Acknowledgments
R.G. thanks the Alexander von Humboldt Foundation for providing a Return postdoctoral fellowship. This work is also supported by the Alexander von Humboldt Foundation via the joint German–Macedonian project from the Research Group Linkage Programme 3.4-Fokoop-DEU/1128670 (to V.M., R.G. I.B., and M.H.). M.H. also acknowledges the support by the Deutsche Forschungsgemeinschaft (SFB 530, SFB 894, GK 845, GK 1326).
Author information
Authors and Affiliations
Corresponding author
Additional information
Dedicated to the 75th birthday of Dr. Nina Fjodorovna Zakharchuk
Appendix
Appendix
The recurrent formulas given in the following table are derived with the aid of the step-function method for solving integral equations [77], assuming that electrode reactions obey Butler–Volmer kinetic formalism. An oxidative electrode reaction is assumed, in which at the beginning of the experiment (i.e., t = 0) only the reduced form (R) of the protein is present in a form of a monolayer at surface concentration Γ*. For numerical integration, both time and current are incremented, with the serial number of the increments designated with m. The time increment is defined as d = 1/50f, which means that the duration of each potential pulse is divided into 25 time increments. The results are presented in the form of dimensionless current \( \Psi = \frac{I}{{nFA{\Gamma^{ * }}f}} \), where n is the number of electrons, F is the Faraday constant, A is the electrode surface area, and f is the frequency of the potential modulation. The dimensionless current is the function of the dimensionless relative electrode potential \( \phi = \frac{{nF}}{{RT}}\left( {E - {E^{{\not{ \circ }}}}} \right) \), anodic electron transfer coefficient α a, and specific critical kinetic parameters. Here, E is the electrode potential, \( {E^{{\not{ \circ }}}} \) is the formal potential of the electrode reaction, R is the gas constant, and T is the thermodynamic temperature. The meaning of the kinetic parameters is explained below Table 2.
Rights and permissions
About this article
Cite this article
Gulaboski, R., Mirčeski, V., Bogeski, I. et al. Protein film voltammetry: electrochemical enzymatic spectroscopy. A review on recent progress. J Solid State Electrochem 16, 2315–2328 (2012). https://doi.org/10.1007/s10008-011-1397-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10008-011-1397-5