Recent advances in the electrochemistry and spectroelectrochemistry of membrane proteins

Biological Chemistry

Volumn 394, Issue 5, 2013, Pages 593-609

  Melin, Frederic ^a   Hellwig, Petra ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Bioelectrochemistry; Bioenergetics; Membrane proteins; Spectroelectrochemistry

Indexed keywords

CARBON NANOTUBE; FUMARATE REDUCTASE; GOLD NANOPARTICLE; IMMOBILIZED PROTEIN; MEMBRANE PROTEIN; NANOMATERIAL; OXIDOREDUCTASE; QUINOL FUMARATE REDUCTASE; QUINONE DERIVATIVE; SILVER NANOPARTICLE; SUCCINATE QUINONE OXIDOREDUCTASE; SUCCINIC ACID; UNCLASSIFIED DRUG;

ATOMIC FORCE MICROSCOPY; CELL RESPIRATION; CHEMICAL REACTION; CONFERENCE PAPER; CONFORMATIONAL TRANSITION; DENSITY FUNCTIONAL THEORY; ELECTROCHEMISTRY; ELECTRODE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; FOURIER TRANSFORM INFRARED PHOTOACOUSTIC SPECTROSCOPY; FOURIER TRANSFORMATION; INFRARED SPECTROSCOPY; LIPID MEMBRANE; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PHOTOSYNTHESIS; POTENTIOMETRY; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; RAMAN SPECTROMETRY; SCANNING ELECTRON MICROSCOPY; SPECTROELECTROCHEMISTRY; SPECTROSCOPY; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; ELECTROCHEMISTRY; IMMOBILIZED PROTEINS; MEMBRANE PROTEINS; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84881624897     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0344     Document Type: Conference Paper

References (141)

1. Abdulhalim, I., Zourob, M., and Lakhtakia, A. (2008). Surface plasmon resonance for biosensing: a mini-review. Electromagnetics 28, 214-242. (Pubitemid 351462589)
2. Albrecht, M.G. and Creighton, J.A. (1977). Anomalously intense Raman spectra of pyridine at a silver electrode. J. Am. Chem. Soc. 99, 5215-5217.
3. Alcantara, K., Munge, B., Pendon, Z., Frank, H.A., and Rusling, J.F. (2006). Thin film voltammetry of spinach photosystem II. Proton-fated electron rransfer involving the Mn4 Cluster. J. Am. Chem. Soc. 128, 14930-14937. (Pubitemid 44851633)
4. Armstrong, F.A. (1990). Probing metalloproteins by voltammetry. In: Structure and Bonding, Vol. 72 (Springer: Berlin/Heidelberg), pp. 137-221.
5. Armstrong, F.A., Heering, H.A., and Hirst, J. (1997). Reaction of complex metalloproteins studied by protein-film voltammetry. Chem. Soc. Rev. 26, 169-179.
6. Ataka, K. and Heberle, J. (2006). Use of Surface Enhanced Infrared Absorption Spectroscopy (SEIRA) to probe the functionality of a protein monolayer. Biopolymers 82, 415-419. (Pubitemid 44000915)
7. Ataka, K. and Heberle, J. (2007). Biochemical applications of surface-enhanced infrared absorption spectroscopy. Anal. Bioanal. Chem. 388, 47-54. (Pubitemid 46712490)
8. Ataka, K., Giess, F., Knoll, W., Naumann, R., Haber-Pohlmeier, S., Richter, B., and Heberle, J. (2004). Oriented attachment and membrane reconstitution of His-tagged cytochrome c oxidase to a gold electrode: in situ monitoring by surface-enhanced infrared absorption spectroscopy. J. Am. Chem. Soc. 126, 16199-16206. (Pubitemid 39627631)
9. Badura, A., Esper, B., Ataka, K., Grunwald, C., Wöll, C., Kuhlmann, J., Heberle, J., and Rögner, M. (2006). Light-driven water splitting for (bio-)hydrogen production: photosystem 2 as the central part of a bioelectrochemical device. Photochem. Photobiol. 82, 1385-1390. (Pubitemid 44702023)
10. Bain, C.D., Troughton, E.B., Tao, Y.T., Evall, J., Whitesides, G.M., and Nuzzo, R.G. (1989). Formation of monolayer films by the spontaneous assembly of organic thiols from solution onto gold. J. Am. Chem. Soc. 111, 321-335.
11. Banholzer, M.J., Millstone, J.E., Qin, L., and Mirkin, C.A. (2008). Rationally designed nanostructures for surface-enhanced Raman spectroscopy. Chem. Soc. Rev. 37, 885-897.
12. Bard, A.J. and Faulkner, L.R. (2001). Electrochemical Methods: Fundamentals and Applications, 2 nd edition (John Wiley & Sons: New York).
13. Baron, R., Willner, B., and Willner, I. (2007). Biomoleculenanoparticle hybrids as functional units for nanobiotechnology. Chem. Commun. 4, 323-332. (Pubitemid 46105509)
14. Barth, A. (2007). Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767, 1073-1101. (Pubitemid 47313388)
15. Baymann, F., Robertson, D.E., Dutton, P.L., and Mäntele, W. (1999). Electrochemical and spectroscopic investigations of the cytochrome bc1 complex from Rhodobacter capsulatus. Biochemistry 38, 13188-13199.
16. Behr, J., Hellwig, P., Mäntele, W., and Michel, H. (1998). Redox dependent changes at the heme propionates in cytochrome c oxidase from Paracoccus denitrificans: direct evidence from FTIR difference spectroscopy in combination with heme propionate 13 C labeling. Biochemistry 37, 7400-7406. (Pubitemid 28235223)
17. Behr, J., Michel, H., Mäntele, W., and Hellwig, P. (2000). Functional properties of the heme propionates in cytochrome c oxidase from Paracoccus denitrificans. Evidence from FTIR difference spectroscopy and site-directed mutagenesis. Biochemistry 39, 1356-1363. (Pubitemid 30090704)
18. Berthomieu, C. and Hienerwadel, R. (2005). Vibrational spectroscopy to study the properties of redox-active tyrosines in photosystem II and other proteins. Biochim. Biophys. Acta 1707, 51-66. (Pubitemid 40249941)
19. Berthomieu, C., Boussac, A., Maentele, W., Breton, J., and Nabedryk, E. (1992). Molecular changes following oxidoreduction of cytochrome b559 characterized by Fourier transform infrared difference spectroscopy and electron paramagnetic resonance: photooxidation in photosystem II and electrochemistry of isolated cytochrome b559 and iron protoporphyrin IX-bisimidazole model compounds. Biochemistry 31, 11460-11471.
20. Breton, J. (2001). Fourier transform infrared spectroscopy of primary electron donors in type I photosynthetic reaction centers. Biochim. Biophys. Acta. 1507, 180-193. (Pubitemid 33001519)
21. Brzezinski, P., Reimann, J., andÄdelroth, P. (2008). Molecular architecture of the proton diode of cytochrome c oxidase. Biochem. Soc. Trans. 36, 1169-1174.
22. Burgess, J.D. and Hawkridge, F.M. (2002). Direct electrochemistry of proteins and enzymes at electrodes. In: Electroanalytical Methods for Biological Materials, A. Brajter-Toth and J. Q. Chambers, eds. (Marcel Dekker, NY, USA), pp. 109-142.
23. Burgess, J.D., Rhoten, M.C., and Hawkridge, F.M. (1998). Cytochrome c oxidase immobilized in stable supported lipid bilayer membranes. Langmuir 14, 2467-2475. (Pubitemid 128567712)
24. Butt, J. and Armstrong, F.A. (2008). Voltammetry of adsorbed redox enzymes: mechanisms in the potential dimension. In: Bioinorganic Electrochemistry, O. Hammerich, J. Ulstrupp, eds. (Netherlands: Springer), pp. 91-128.
25. Calvert, J.F., Hill, J.L., and Dong, A. (1997). Redox-dependent conformational changes are common structural features of cytochrome c from various species. Arch. Biochem. Biophys. 346, 287-293. (Pubitemid 27439047)
26. Campion, A. and Kambhampati, P. (1998). Surface-enhanced Raman scattering. Chem. Soc. Rev. 27, 241-250.
27. Christenson, A., Gustavsson, T., Gorton, L., and Hägerh äll, C. (2008). Direct and mediated electron transfer between intact succinate:quinone oxidoreductase from Bacillus subtilis and a surface modified gold electrode reveals redox statedependent conformational changes. Biochim. Biophys. Acta 1777, 1203-1210.
28. Chu, H.-A., Hillier, W., Law, N.A., and Babcock, G.T. (2001). Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim. Biophys. Acta 1503, 69-82.
29. Ciobanu, M., Kincaid, H.A., Lo, V., Dukes, A.D., Kane Jennings, G., and Cliffel, D.E. (2007). Electrochemistry and photoelectrochemistry of photosystem I adsorbed on hydroxyl-terminated monolayers. J Electroanal. Chem. 599, 72-78. (Pubitemid 44880335)
30. Crawley, C.D. and Hawkridge, F.M. (1981). Spectroelectrochemical determination of the heterogeneous electron transfer kinetics of soluble spinach ferredoxin. Biochem. Biophys. Res. Commun. 99, 516-522.
31. Cullison, J.K., Hawkridge, F.M., Nakashima, N., and Yoshikawa, S. (1994). A study of cytochrome c oxidase in lipid bilayer membranes on electrode surfaces. Langmuir 10, 877-882.
32. Daniel, M.-C. and Astruc, D. (2003). Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. Chem. Rev. 104, 293-346.
33. Das, R., Kiley, P.J., Segal, M., Norville, J., Yu, A.A., Wang, L., Trammell, S.A., Reddick, L.E., Kumar, R., Stellacci, F., et al. (2004). Integration of photosynthetic protein molecular complexes in solid-state electronic devices. Nano. Lett. 4, 1079-1083. (Pubitemid 38859985)
34. Dollinger, G., Eisenstein, L., Lin, S.-L., Nakanishi, K., Odashima, K., Termini, J. (1986). [48] Bacteriorhodopsin: fourier transform infrared methods for studies of protonation of carboxyl groups. Methods Enzymol. 127, 649-662.
35. Dutton, P.L. (1978). Redox potentiometry: determination of mid-point potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol. 54, 411-435.
36. El Khoury, Y. and Hellwig, P. (2011). A combined far-infrared spectroscopic and electrochemical approach for the study of iron - sulfur proteins. Chem. Phys. Chem. 12, 2669-2674.
37. Engelhard, M., Gerwert, K., Hess, B., Siebert, F. (1985). Light-driven protonation changes of internal aspartic acids of bacteriorhodopsin: an investigation of static and time-resolved infrared difference spectroscopy using [4-13C]aspartic acid labeled purple membrane. Biochemistry 24, 400-407. (Pubitemid 15105616)
38. Faulkner, C.J., Lees, S., Ciesielski, P.N., Cliffel, D.E., and Jennings, G.K. (2008). Rapid assembly of photosystem I monolayers on gold electrodes. Langmuir, 24, 8409-8412.
39. Feng, J.-J., Gernert, U., Sezer, M., Kuhlmann, U., Murgida, D.H., David, C., Richter, M., Knorr, A., Hildebrandt, P., and Weidinger, I.M. (2008). Novel Au-Ag hybrid device for electrochemical SE(R)R spectroscopy in a wide potential and spectral range. Nano. Lett. 9, 298-303.
40. Feng, J.-J., Lu, Y.-H., Gernert, U., Hildebrandt, P., and Murgida, D.H. (2010). Electrosynthesis of SER-active silver nanopillar electrode arrays. J. Phys. Chem. C. 114, 7280-7284.
41. Fleischmann, M., Hendra, P.J., and McQuillan, A.J. (1974). Raman spectra of pyridine adsorbed at a silver electrode. Chem. Phys. Lett. 26, 163-166.
42. Flemming, D., Hellwig, P., and Friedrich, T. (2003). Involvement of tyrosines 114 and 139 of subunit NuoB in the proton pathway around Cluster N2 in Escherichia coli NADH:ubiquinone oxidoreductase. J. Biol. Chem. 278, 3055-3062. (Pubitemid 36801214)
43. Flemming, D., Stolpe, S., Schneider, D., Hellwig, P., and Friedrich, T. (2005). A possible role for iron-sulfur cluster N2 in proton translocation by the NADH:ubiquinone oxidoreductase (Complex I). J. Mol. Microbiol. Biotechnol. 10, 208-222. (Pubitemid 43800694)
44. Friedrich, M.G., Gie, F., Naumann, R., Knoll, W., Ataka, K., Heberle, J., Hrabakova, J., Murgida, D.H., and Hildebrandt, P. (2004). Active site structure and redox processes of cytochrome c oxidase immobilised in a novel biomimetic lipid membrane on an electrode. Chem. Commun. (Camb) 21, 2376-2377. (Pubitemid 39563838)
45. Friedrich, M.G., Robertson, J.W.F., Walz, D., Knoll, W., and Naumann, R.L.C. (2008). Electronic wiring of a multi-redox site membrane protein in a biomimetic surface architecture. Biophys. J. 94, 3698-3705.
46. Gerwert, K. (1999). Molecular reaction mechanisms of proteins monitored by time-resolved FTIR-spectroscopy. Biol. Chem. 380, 931-935. (Pubitemid 29412752)
47. Giess, F., Friedrich, M.G., Heberle, J., Naumann, R.L., and Knoll, W. (2004). The protein-tethered Lipid bilayer: a novel mimic of the biological membrane. Biophys. J. 87, 3213-3220. (Pubitemid 40468578)
48. Grosserueschkamp, M., Nowak, C., Schach, D., Schaertl, W., Knoll, W., and Naumann, R.L.C. (2009). Silver surfaces with optimized surface enhancement by self-assembly of silver nanoparticles for spectroelectrochemical applications. J. Phys. Chem. C. 113, 17698-17704.
49. Grzelczak, M., Perez-Juste, J., Mulvaney, P., and Liz-Marzan, L.M. (2008). Shape control in gold nanoparticle synthesis. Chem. Soc. Rev. 37, 1783-1791.
50. Haas, A.S., Pilloud, D.L., Reddy, K.S., Babcock, G.T., Moser, C.C., Blasie, J.K., and Dutton, P.L. (2001). Cytochrome c and cytochrome c oxidase: monolayer assemblies and catalysis. J. Phys. Chem. B 105, 11351-11362. (Pubitemid 35338487)
51. Ham, M.-H., Choi, J.H., Boghossian, A.A., Jeng, E.S., Graff, R.A., Heller, D.A., Chang, A.C., Mattis, A., Bayburt, T.H., Grinkova, Y.V., et al. (2010). Photoelectrochemical complexes for solar energy conversion that chemically and autonomously regenerate. Nat. Chem. 2, 929-936.
52. Hartstein, A., Kirtley, J.R., and Tsang, J.C. (1980). Enhancement of the infrared absorption from molecular monolayers with thin metal overlayers. Phys. Rev. Lett. 45, 201-204.
53. Heineman, W.R., Kuwana, T., and Hartzell, C.R. (1972). Indirect electrochemical titration of beef heart cytochrome c oxidase. Biochem. Biophys. Res. Commun. 49, 1-8.
54. Heineman, W.R. Meckstroth, M.L. Norris, B.J., and Su, C.-H. (1979). Optically transparent thin layer electrode techniques for the study of biological redox systems. Bioelectrochem. Bioenerg. 6, 577-585. (Pubitemid 10102342)
55. Hellwig, P., Behr, J., Ostermeier, C., Richter, O.-M. H., Pfitzner, U., Odenwald, A., Ludwig, B., Michel, H., and Mäntele, W. (1998). Involvement of Glutamic Acid 278 in the redox reaction of the cytochrome c oxidase from Paracoccus denitrificans investigated by FTIR spectroscopy. Biochemistry 37, 7390-7399. (Pubitemid 28235222)
56. Hellwig, P., Scheide, D., Bungert, S., Mäntele, W., and Friedrich, T. (2000). FT-IR spectroscopic characterization of NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli: oxidation of FeS cluster N2 is coupled with the protonation of an aspartate or glutamate side chain. Biochemistry 39, 10884-10891.
57. Hellwig, P., Yano, T., Ohnishi, T., and Gennis, R.B. (2002). Identification of the residues involved in stabilization of the semiquinone radical in the high-affinity ubiquinone binding site in cytochrome bo3 from Escherichia coli by site-directed mutagenesis and EPR spectroscopy. Biochemistry 41, 10675-10679. (Pubitemid 34913327)
58. Hinkle, P.C., Kim, J.J., and Racker, E. (1972). Ion transport and respiratory control in vesicles formed from cytochrome oxidase and phospholipids. J. Biol. Chem. 247, 1338-1339.
59. Hirst, J., Sucheta, A., Ackrell, B.A.C., and Armstrong, F.A. (1996). Electrocatalytic voltammetry of succinate dehydrogenase: direct quantification of the catalytic properties of a complex electron-transport enzyme. J. Am. Chem. Soc. 118, 5031-5038. (Pubitemid 26200977)
60. Hrabakova, J., Ataka, K., Heberle, J., Hildebrandt, P., and Murgida, D. H. (2006). Long distance electron transfer in cytochrome c oxidase immobilised on electrodes. A surface enhanced resonance Raman study. Phys. Chem. Chem. Phys. 8, 759-766.
61. Hudson, J.M., Heffron, K., Kotlyar, V., Sher, Y., Maklashina, E., Cecchini, G., and Armstrong, F.A. (2005). Electron transfer and catalytic control by the iron-sulfur clusters in a respiratory enzyme, E. coli fumarate reductase. J. Am. Chem. Soc. 127, 6977-6989. (Pubitemid 40676726)
62. Iijima, S. (1991). Helical microtubules of graphitic carbon. Nature 354, 56-58. (Pubitemid 21896780)
63. Iwaki, M., Andrianambinintsoa, S., Rich, P., and Breton, J. (2002). Attenuated total reflection Fourier transform infrared spectroscopy of redox transitions in photosynthetic reaction centers: comparison of perfusion- and light-induced difference spectra. Spectrochim. Acta A 58, 1523-1533. (Pubitemid 34466993)
64. Iwaki, M., Yakovlev, G., Hirst, J., Osyczka, A., Dutton, P.L., Marshall, D., and Rich, P.R. (2005). direct observation of redox-linked histidine protonation changes in the iron - sulfur protein of the cytochrome bc1 complex by ATR-FTIR spectroscopy. Biochemistry 44, 4230-4237. (Pubitemid 40403963)
65. Jeanmaire, D.L. and Van Duyne, R.P. (1977). Surface raman spectroelectrochemistry: Part I. Heterocyclic, aromatic, and aliphatic amines adsorbed on the anodized silver electrode. J. Electroanal. Chem. 84, 1-20.
66. Jenkins, A.T.A., Boden, N., Bushby, R.J., Evans, S.D., Knowles, P.F., Miles, R.E., Ogier, S.D., Schönherr, H., and Vancso, G.J. (1999). Microcontact printing of lipophilic self-assembled monolayers for the attachment of biomimetic lipid bilayers to surfaces. J. Am. Chem. Soc. 121, 5274-5280. (Pubitemid 29275735)
67. Jeuken, L.J.C. (2009). Electrodes for integral membrane enzymes. Nat. Prod. Rep. 26, 1234-1240.
68. Jeuken, L.C.J., Connell, S.D., Nurnabi, M., O'Reilly, J., Henderson, P.J.F., Evans, S.D., and Bushby, R.J. (2005). Direct electrochemical interaction between a modified gold electrode and a bacterial membrane extract. Langmuir 21, 1481-1488. (Pubitemid 40275087)
69. Jeuken, L.J.C., Connell, S.D., Henderson, P.J.F., Gennis, R.B., Evans, S.D., and Bushby, R.J. (2006). Redox enzymes in tethered membranes. J. Am. Chem. Soc. 128, 1711-1716. (Pubitemid 43214886)
70. Jiang, X., Zaitseva, E., Schmidt, M., Siebert, F., Engelhard, M., Schlesinger, R., Ataka, K., Vogel, R., and Heberle, J. (2008). Resolving voltage-dependent structural changes of a membrane photoreceptor by surface-enhanced IR difference spectroscopy. Proc. Natl. Acad Sci. USA 105, 12113-12117.
71. Kaniber, S.M., Brandstetter, M., Simmel, F.C., Carmeli, I., and Holleitner, A.W. (2010). On-chip functionalization of carbon nanotubes with photosystem I. J. Am. Chem. Soc. 132, 2872-2873.
72. Kato, Y., Sugiura, M., Oda, A., and Watanabe, T. (2009). Spectroelectrochemical determination of the redox potential of pheophytin a, the primary electron acceptor in photosystem II. Proc. Natl. Acad Sci. USA 106, 17365-17370.
73. Katz, E. and Willner, I. (2004). Integrated nanoparticle - biomolecule hybrid systems: synthesis, properties, and applications. Angew. Chem. Int. Ed. 43, 6042-6108.
74. Kim, S. and Barry, B.A. (1998). Vibrational spectrum associated with the reduction of tyrosyl radical D • in photosystem II: A comparative biochemical and kinetic study. Biochemistry 37, 13882-13892. (Pubitemid 28455566)
75. Kim, S., Sacksteder, C.A., Bixby, K.A., and Barry, B.A. (2001). A reaction-induced FT-IR study of cyanobacterial photosystem I. Biochemistry 40, 15384-15395. (Pubitemid 33151954)
76. Kinnear, K.T. and Monbouquette, H.G. (1993). Direct electron transfer to Escherichia coli fumarate reductase in self-assembled alkanethiol monolayers on gold electrodes. Langmuir 9, 2255-2257.
77. Ko, B.S., Babcock, B., Jennings, G.K., Tilden, S.G., Peterson, R.R., Cliffel, D., and Greenbaum, E. (2004). Effect of surface composition on the adsorption of photosystem I onto alkanethiolate self-assembled monolayers on gold. Langmuir 20, 4033-4038.
78. Kong, J., Lu, Z., Lvov, Y.M., Desamero, R.Z.B., Frank, H.A., and Rusling, J.F. (1998). Direct dlectrochemistry of cofactor redox sites in a bacterial photosynthetic reaction center protein. J. Am. Chem. Soc. 120, 7371-7372. (Pubitemid 28389373)
79. Kozuch, J., Steinem, C., Hildebrandt, P., and Millo, D. (2012). Combined electrochemistry and surface-enhanced infrared absorption spectroscopy of gramicidin A incorporated into tethered bilayer lipid membranes. Angew. Chem. Int. Ed. 51, 8114-8117.
80. Krassen, H., Schwarze, A., Friedrich, B., Ataka, K., Lenz, O., and Heberle, J. (2009). Photosynthetic hydrogen production by a hybrid complex of photosystem I and [NiFe]-hydrogenase. ACS Nano 3, 4055-4061.
81. Kreishman George, P., Su, C.-H., Anderson, C.W., Halsall, H.B., and Heineman William, R. (1980). The effect of bulk solvent structure and specific ion binding on the temperature dependence of the reduction potential of horse heart cytochrome c. Book Section 188, 169-185.
82. Kwee, S. (1986). A novel mediator for the investigation of the electrochemistry of metalloproteins. Bioelectrochem. Bioenerg. 16, 99-109. (Pubitemid 17495580)
83. Lal, S., Grady, N.K., Kundu, J., Levin, C.S., Lassiter, J.B., and Halas, N.J. (2008). Tailoring plasmonic substrates for surface enhanced spectroscopies. Chem. Soc. Rev. 37, 898-911.
84. Landrum, H.L. Salmon, R.T., and Hawkridge, F.M. (1977). A surfacemodified gold minigrid electrode which heterogeneously reduces spinach ferredoxin. J. Am. Chem. Soc 99, 3154-3158.
85. Lang, H., Duschl, C., and Vogel, H. (1994). A new class of thiolipids for the attachment of lipid bilayers on gold surfaces. Langmuir 10, 197-210.
86. Lee, I., Lee, J.W., and Greenbaum, E. (1997). Biomolecular electronics: vectorial arrays of photosynthetic reaction centers. Phys. Rev. Lett. 79, 3294-3297. (Pubitemid 127624771)
87. Leonhard, M. and Maentele, W. (1993). Fourier transform infrared spectroscopy and electrochemistry of the primary electron donor in Rhodobacter sphaeroides and Rhodopseudomonas viridis reaction centers: vibrational modes of the pigments in situ and evidence for protein and water modes affected by P + formation. Biochemistry 32, 4532-4538. (Pubitemid 23143239)
88. Li, J., Cheng, G., and Dong, S. (1996). Direct electron transfer to cytochrome c oxidase in self-assembled monolayers on gold electrodes. J. Electroanal. Chem. 416, 97-104. (Pubitemid 126389600)
89. Lisdat, F. and Schäfer, D. (2008). The use of electrochemical impedance spectroscopy for biosensing. Anal. Bioanal. Chem. 391, 1555-1567.
90. Lübben, M., Prutsch, A., Mamat, B., and Gerwert, K. (1999). Electron transfer induces side-chain conformational changes of glutamate-286 from cytochrome bo3. Biochemistry 38, 2048-2056.
91. Mahmoudi, M., Lynch, I., Ejtehadi, M.R., Monopoli, M.P., Bombelli, F.B., and Laurent, S. (2011). Protein-nanoparticle interactions: opportunities and challenges. Chem. Rev. 111, 5610-5637.
92. Maly, J., Krejci, J., Ilie, M., Jakubka, L., Masojídek, J., Pilloton, R., Sameh, K., Steffan, P., Stryhal, Z., and Sugiura, M. (2005). Monolayers of photosystem II on gold electrodes with enhanced sensor response-effect of porosity and protein layer arrangement. Anal. Bioanal. Chem. 381, 1558-1567. (Pubitemid 40609390)
93. Marboutin, L., Petitjean, H., Xerri, B., Vita, N., Dupeyrat, F., Flament, J.-P., Berthomieu, D., and Berthomieu, C. (2011). Profiling the active site of a copper enzyme through its far-infrared fingerprint. Angew. Chem. Int. Ed. 50, 8062-8066.
94. Marshall, D., Fisher, N., Grigic, L., Zickermann, V., Brandt, U., Shannon, R.J., Hirst, J., Lawrence, R., and Rich, P.R. (2006). ATR-FTIR redox difference spectroscopy of Yarrowia lipolytica and bovine complex I. Biochemistry 45, 5458-5467. (Pubitemid 43673177)
95. Marx, K.A. (2003). Quartz crystal microbalance: a useful tool for studying thin polymer films and complex biomolecular systems at the solution-surface interface. Biomacromolecules 4, 1099-1120. (Pubitemid 37184619)
96. McQuillan, A.J., Hendra, P.J., and Fleischmann, M. (1975). Raman spectroscopic investigation of silver electrodes. J. Electroanal. Chem. 65, 933-944.
97. Melin, F., Meyer, T., Lankiang, S., Choi, S.K., Gennis, R.B., Blanck, C., Schmutz, M., and Hellwig. P. (2013). Direct electrochemistry of cytochrome bo3 oxidase at a series of gold nanoparticlesmodified electrodes. Electrochem. Commun 26, 105-108.
98. Meyer, T., Gross, J., Blanck, C., Schmutz, M., Ludwig, B., Hellwig, P., and Melin, F. (2011). Electrochemistry of cytochrome c1, cytochrome c552, and CuA from the respiratory chain of thermus thermophilus immobilized on gold nanoparticles. J. Phys. Chem. B 115, 7165-7170.
99. Miyachi, M., Yamanoi, Y., Shibata, Y., Matsumoto, H., Nakazato, K., Konno, M., Ito, K., Inoue, Y., and Nishihara, H. (2010). A photosensing system composed of photosystem I, molecular wire, gold nanoparticle, and double surfactants in water. Chem. Commun. 46, 2557-2559.
100. Moskovits, M. (1985). Surface-enhanced spectroscopy. Rev. Mod. Phys. 57, 783-826.
101. Moss, D., Nabedryk, E., Breton, J., and Mäntele, W. (1990). Redox-linked conformational changes in proteins detected by a combination of infrared spectroscopy and protein electrochemistry. Eur. J. Biochem. 187, 565-572. (Pubitemid 20074919)
102. Moss, D.A., Leonhard, M., Bauscher, M., and Mäntele, W. (1991). Electrochemical redox titration of cofactors in the reaction center from Rhodobacter sphaeroides. FEBS Lett. 283, 33-36.
103. Munge, B., Das, S.K., Ilagan, R., Pendon, Z., Yang, J., Frank, H.A., and Rusling, J.F. (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. (Pubitemid 37254762)
104. Murgida, D.H. and Hildebrandt, P. (2005). Redox and redox-coupled processes of heme proteins and enzymes at electrochemical interfaces. Phys. Chem. Chem. Phys. 7, 3773-3784. (Pubitemid 41718295)
105. Nabedryk, E. and Breton, J. (2008). Coupling of electron transfer to proton uptake at the QB site of the bacterial reaction center: a perspective from FTIR difference spectroscopy. Biochim. Biophys. Acta 1777, 1229-1248.
106. Nabedryk, E., Leonhard, M., Maentele, W., and Breton, J. (1990). Fourier transform infrared difference spectroscopy shows no evidence for an enolization of chlorophyll a upon cation formation either in vitro or during P700 photooxidation. Biochemistry 29, 3242-3247. (Pubitemid 20131465)
107. Nakamura, A., Suzawa, T., Kato, Y., and Watanabe, T. (2011). Species dependence of the redox potential of the primary electron donor P700 in photosystem I of oxygenic photosynthetic organisms revealed by spectroelectrochemistry. Plant. Cell Physiol. 52, 815-823.
108. Naumann, R., Schmidt, E.K., Jonczyk, A., Fendler, K., Kadenbach, B., Liebermann, T., Offenhäusser, A., and Knoll, W. (1999). The peptide-tethered lipid membrane as a biomimetic system to incorporate cytochrome c oxidase in a functionally active form. Biosens. Bioelectron. 14, 651-662. (Pubitemid 29528195)
109. Naumann, R.L.C., Nowak, C., and Knoll, W. (2011). Proteins in biomimetic membranes: promises and facts. Soft Matter. 7, 9535-9548.
110. Norris, B.J., Meckstroth, M.L., and Heineman, W.R. (1976). Optically transparent thin layer electrode for anaerobic measurements on redox enzymes. Anal. Chem. 48, 630-632.
111. Ohnishi, T. (1998). Iron-sulfur clusters/semiquinones in Complex I. Biochim. Biophys. Acta 1364, 186-206. (Pubitemid 28291839)
112. Ohnishi, T., Moser, C.C., Page, C.C., Dutton, P.L., and Yano, T. (2000). Simple redox-linked proton-transfer design: new insights from structures of quinol-fumarate reductase. Structure 8, R23-32. (Pubitemid 30097356)
113. Osawa, M. (2001). Surface-enhanced infrared absorption near-field optics and surface plasmon polaritons. Book Section 81, 163-187.
114. Page, C.C., Moser, C.C., Chen, X., and Dutton, P.L. (1993). Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47-52.
115. Prime, K. and Whitesides, G. (1991). Self-assembled organic monolayers: model systems for studying adsorption of proteins at surfaces. Science 252, 1164-1167. (Pubitemid 21917027)
116. Pumera, M. (2009). The electrochemistry of carbon nanotubes: fundamentals and applications. Chem. Eur. J. 15, 4970-4978.
117. Ritter, M., Anderka, O., Ludwig, B., Mäntele, W., and Hellwig, P. (2003). Electrochemical and FTIR spectroscopic characterization of the cytochrome bc1 complex from Paracoccus denitrificans: evidence for protonation reactions coupled to quinone binding. Biochemistry 42, 12391-12399. (Pubitemid 37296515)
118. Rothschild, K.J., Zagaeski, M., and Cantore, W.A. (1981). Conformational changes of bacteriorhodopsin detected by Fourier transform infrared difference spectroscopy. Biochem. Biophys. Res. Com. 103, 483-489.
119. Rubinson, K.A. and Mark, H.B. (1982). Long-Path, small volume spectroelectrochemistry cell. Anal. Chem. 54, 1204-1206.
120. Rusling, J.F. (1998). Enzyme bioelectrochemistry in cast biomembrane-like films. Acc Chem. Res. 31, 363-369. (Pubitemid 128474596)
121. Sailasuta, N., Anson, F.C., and Gray, H.B. (1979). Studies of the thermodynamics of electron transfer reactions of blue copper proteins. J. Am. Chem. Soc. 101, 455-458.
122. Salamon, Z., Hazzard, J.T., and Tollin, G. (1993). Direct measurement of cyclic current-voltage responses of integral membrane proteins at a self-assembled lipid-bilayer-modified electrode: cytochrome f and cytochrome c oxidase. Proc. Nat. Acad Sci. USA 90, 6420-6423. (Pubitemid 23207224)
123. Salamon, Z., Wang, Y., Soulages, J.L., Brown, M.F., and Tollin, G. (1996). Surface plasmon resonance spectroscopy of membrane proteins: transducin binding and activation by rhodopsin monitored in thin membrane films. Biophys. J. 71, 283-294. (Pubitemid 26227314)
124. Schach, D., Nowak, C., Gennis, R.B., Ferguson-Miller, S., Knoll, W., Walz, D., and Naumann, R.L.C. (2010). Modeling direct electron transfer to a multi-redox center protein: cytochrome c oxidase. J. Electroanal. Chem. 649, 268-276.
125. Schiller, S.M., Naumann, R., Lovejoy, K., Kunz, H., and Knoll, W. (2003). Archaea analogue thiolipids for tethered bilayer lipid membranes on ultrasmooth gold surfaces. Angew. Chem. Int. Ed. 42, 208-211. (Pubitemid 36125579)
126. Schkolnik, G., Salewski, J., Millo, D., Zebger, I., Franzen, S., and Hildebrandt, P. (2012). Vibrational stark effect of the electricfield reporter 4-mercaptobenzonitrile as a tool for investigating electrostatics at electrode/SAM/solution interfaces. Int. J. Mol. Sci. 13, 7466-7482.
127. Simone, M.K., Friedrich, C.S., Alexander, W.H., and Itai, C. (2009). The optoelectronic properties of a photosystem I-carbon nanotube hybrid system. Nanotechnology 20, 345701, 1-7.
128. Song, S. and Dong, S. (1988). Spectroelectrochemistry of the quasi-reversible reduction and oxidation of hemoglobin at a methylene blue adsorbed modified electrode. Bioelectrochem. Bioenerg. 19, 337-346.
129. Szentrimay, R., Yeh, P., and Kuwana, T. (1977). Evaluation of mediator-titrants for the indirect coulometric titration of biocomponents. In: Electrochemical Studies of Biological Systems, ACS Symposium Series, Vol. 38, D.T. Sawyer, ed. (Washington, DC: American Chemical Society), pp. 143-169.
130. Sucheta, A., Ackrell, B.A.C., Cochran, B., and Armstrong, F.A. (1992). Diode-like behaviour of a mitochondrial electron-transport enzyme. Nature 356, 361-362.
131. Taniguchi, V.T., Sailasuta-Scott, N., Anson, F.C., and Gray, H.B. (1980). Thermodynamics of metalloprotein electron transfer reactions. Pure Appl. Chem. 52, 2275-2282.
132. Tans, S.J., Devoret, M.H., Dai, H., Thess, A., Smalley, R.L., Geerligs, L.J., and Dekker, C. (1997). Individual single-wall carbon nanotubes as quantum wires. Nature 386, 474-477. (Pubitemid 27164068)
133. Todorovic, S., Verissimo, A., Wisitruangsakul, N., Zebger, I. Hildebrandt, P., Pereira, M.M., Teixeira, M., and Murgida, D.H. (2008). SERR-spectroelectrochemical study of a cbb3 oxygen reductase in a biomimetic construct. J. Phys. Chem. B 112, 16952-16959.
134. Vogel, R. and Siebert, F. (2000). Vibrational spectroscopy as a tool for probing protein function. Curr. Opin. Chem. Biol. 4, 518-523.
135. Weiss, S.A., Bushby, R.J., Evans, S.D., and Jeuken, L.J.C. (2010). A study of cytochrome bo3 in a tethered bilayer lipid membrane. Biochim. Biophys. Acta 1797, 1917-1923.
136. Whittaker, J.W. (2003). Free radical catalysis by galactose oxidase. Chem. Rev. 103, 2347-2364.
137. Willner, I. and Katz, E. (2000). Integration of layered redox proteins and conductive supports for bioelectronic applications. Angew. Chem. Int. Ed. 39, 1180-1218. (Pubitemid 30219908)
138. Xiao, Y., Patolsky, F., Katz, E., Hainfeld, J. F., and Willner, I. (2003). "Plugging into Enzymes": nanowiring of redox enzymes by a gold nanoparticle. Science 299, 1877-1881. (Pubitemid 36356654)
139. Yeh, Y.-C., Creran, B., and Rotello, V.M. (2012). Gold nanoparticles: preparation, properties, and applications in bionanotechnology. Nanoscale 4, 1871-1880.
140. Zscherp, C. and Barth, A. (2001). Reaction-induced infrared difference spectroscopy for the study of protein reaction mechanisms. Biochemistry 40, 1875-1883. (Pubitemid 32165654)
141. Zu, Y., Shannon, R.J., and Hirst, J. (2003). Reversible, electrochemical interconversion of NADH and NAD by the catalytic (I) subcomplex of mitochondrial NADH:ubiquinone oxidoreductase (Complex I). J. Am. Chem. Soc. 125, 6020-6021. (Pubitemid 36582950)