Electron tunneling through proteins

Quarterly Reviews of Biophysics

Volumn 36, Issue 3, 2003, Pages 341-372

  Gray, Harry B ^a   Winkler, Jay R ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME B; CYTOCHROME C; HEMOGLOBIN; IRON COMPLEX; ZINC COMPLEX;

ELECTRON TRANSPORT; ENERGY RESOURCE; OXIDATION; PHOTOSYNTHESIS; PREDICTION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REDUCTION; REVIEW; THERMODYNAMICS;

AZURIN; BINDING SITES; COMPUTER SIMULATION; CYTOCHROMES C; ELECTRON TRANSPORT; ENERGY TRANSFER; MODELS, MOLECULAR; OXIDATION-REDUCTION; PHOTOSYNTHESIS; RUTHENIUM;

EID: 1442328094     PISSN: 00335835     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0033583503003913     Document Type: Review

References (164)

1. ADMAN, E. T. (1991). Copper protein structures. Advances in Protein Chemistry 42, 145-197.
2. ADMAN, E. T. & JENSEN, L. H. (1981). Structural features of azurin at 2.7 Å resolution. Israel Journal of Chemistry 21, 8-12.
3. ALEGRIA, G. & DUTTON, P. L. (1991a). I. Langmuir-Blodgett monolayer films of bacterial photosynthetic membranes and isolated reaction centers: preparation, spectrophotometric and electrochemical characterization. Biochimica et Biophysica Acta 1057, 239-257.
4. ALEGRIA, G. & DUTTON, P. L. (1991b). II. Langmuir-Blodgett monolayer films of the Rhodopseudomonas viridis reaction center: determination of the order of the hemes in the cytochrome c subunit. Biochimica et Biophysica Acta 1057, 258-272.
5. ALLEN, J. P., FEHER, G., YEATES, T. O., KOMIYA, H. & REES D. C. (1987). Structure of the reaction center from Rhodobacter sphaeroides R-26 - the cofactors. Proceedings of the National Academy of Sciences USA 84, 5730-5734.
6. 2: reaction center ET complex from Rhodobacter sphaeroides. Journal of Molecular Biology 319, 501-515.
7. BABINI, E., BERTINI, I., BORSARI, M., CAPOZZI, F., LUCHINAT, C., ZHANG, X., MOURA, G. L. C., KURNIKOV, I. V., BERATAN, D. N., PONCE, A., DI BILIO, A. J., WINKLER, J. R. & GRAY, H. B. (2000). Bond-mediated electron tunneling in ruthenium-modified high-potential iron-sulfur protein. Journal of the American Chemical Society 122, 4532-4533.
8. BALABIN, I. A. & ONUCHIC, J. N. (1998). A new framework for electron-transfer calculations - beyond the pathways-like models. Journal of Phyical Chemistry (B) 102, 7497-7505.
9. BATTISTUZZI, G., BORSARI, M., COWAN, J. A., RANTERI A. A. & SOLA, M. (2002). Control of cytochrome c redox potential: axial ligation and protein environment effects. Journal of the American Chemical Society 124, 5315-5324.
10. BATTISTUZZI, G., BORSARI, M. & SOLA, M. (2001). Medium and temperature effects on the redox chemistry of cytochrome c. European Journal of Inorganic Chemistry, 2989-3004.
11. BATTISTUZZI, G., BORSARI, M., SOLA, M. & FRANIA, F. (1997). Redox thermodynamics of the native and alkaline forms of eucaryotic and bacterial class I cytochromes c. Biochemistry 36, 16247-16258.
12. BAYMANN, F. & RAPPAPORT, F. (1998). Electrostatic interactions at the donor side of the photosynthetic reaction center of Rhodopseudomonas viridis. Biochemistry 37, 15320-15326.
13. BERATAN, D. N., BETTS, J. N. & ONUCHIC, J. N. (1991). Protein ET rates set by the bridging secondary and tertiary structure. Science 252, 1285-1288.
14. BERATAN, D. N., BETTS, J. N. & ONUCHIC, J. N. (1992). Tunneling pathway and redox-state dependent electronic couplings at nearly fixed distance in electron-transfer proteins. Journal of Physical Chemistry 96, 2852-2855.
15. BERATAN, D. N. & ONUCHIC, J. N. (1989). Electron tunneling pathways in proteins: influences on the transfer rate. Photosynthesis Research 22, 173-186.
16. BERATAN, D. N., ONUCHIC J. N. & HOPFIELD, J. J. (1987). Electron tunneling through covalent and noncovalent pathways in proteins. Journal of Chemical Physics 86, 4488-4498.
17. BIXLER, J., BAKKER, G. & MCLENDON, G. (1992). Electrochemical probes of protein folding. Journal of the American Chemical Society 114, 6938-6939.
18. BJERRUM, M. J., CASIMIRO, D. R., CHANG, I.-J., DI BILIO, A. J., GRAY, H. B., HILL, M. G., LANGEN, R., MINES, G. A., SKOV, L. K., WINKLER, J. R. & WUTTKE, D. S. (1995). Electron transfer in ruthenium-modified proteins. Journal of Bioenergetics and Biomembranes 27, 295-302.
19. BOLLINGER JR., J. M., EDMONDSON, D. E., HUYNH, B. H., FILLEY, J., NORTON, J. R. & STUBBE, J. (1991). Mechanism of assembly of the tyrosyl radical-dinuclear iron cluster cofactor of ribonucleotide reductase. Science 253, 292-298.
20. BROWN, G. M. & SUTIN, N. (1979). 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. Journal of the American Chemical Society 101, 883-892.
21. BRUNSCHWIG, B. S. & SUTIN, N. (1987). Rate-constant expressions for nonadiabaitic electron-transfer reactions. Comments on Inorganic Cbemistry, 6, 209-235.
22. BRUNSCHWIG B. S. & SUTIN, N. (1989). Directional electron transfer: conformational interconversions and their effects on observed electron-transfer rate constants. Journal of the American Chemical Society 111, 7454-7465.
23. BRZEZINSKI, P. & LARSSON, G. (2003). Redox-driven proton pumping by heme-copper oxidases. Biochimica et Biophysica Acta - Bioenergetics 1605, 1-13.
24. CALCATERRA, L. T., CLOSS, G. L. & MILLER, J. R. (1983). Intramolecular electron transfer in radical ions over long distances across rigid saturated hydrocarbon spacers. Journal of the American Chemical Society 105, 670-671.
25. CASIMIRO, D. R., RICHARDS, J. H., WINKLER, J. R. & GRAY, H. B. (1993). Electron transfer in ruthenium-modified cytochromes c. σ-Tunneling pathways through aromatic residues. Journal of Physical Chemistry 97, 13073-13077.
26. CHANCE, B. & WILLIAMS, G. R. (1956). The respiratory chain and oxidative phosphorylation. Advances in Enzymology 17, 65-134.
27. 3+. Journal of the American Chemical Society, 113, 7056-7067.
28. CHANG, T. K., IVERSON, S. A., RODRIGUES, C. G., KISER, C. N., LEW, A. Y., GERMANAS, J. P. & RICHARDS, J. H. (1991b). Gene synthesis, expression and mutagenesis of the blue copper proteins azurin and plastocyanin. Proceedings of the National Academy of Sciences USA 88, 1325-1329.
29. CHEN, I.-P., PATHIS, P., KOEPKE, J. & MICHEL, H. (2000). Uphill electron transfer in the tetraheme cytochrome subunit of the Rhodopseudomonas viridis photosynthetic reaction center: evidence from site directed mutagenesis. Biochemistry 39, 3592-3602.
30. CHURG, A. K. & WARSHEL, A. (1986). Control of the redox potential of cytochrome c and microscopic dielectric effects in proteins. Biochemistry 25, 1675-1681.
31. CLOSS, G. L. & MILLER, J. R. (1988). Intramolecular long-distance electron transfer in organic molecules. Science 240, 440-447.
32. CRANE, B. R., DI BILIO, A. J., WINKLER, J. R. & GRAY, H. B. (2001). Electron tunneling in single crystals of Pseudomonas aeruginosa azurins. Journal of the American Chemical Society 123, 11623-11631.
33. CREUTZ, C. & SUTIN, N. (1977). Vestiges of the 'inverted region' for highly exergonic electron-transfer reactions. Journal of the American Chemical Society 99, 241-243.
34. DAVIS, W. B., RATNER, M. A. & WASIELEWSKI, M. R. (2002). Dependence of electron transfer dynamics in wire-like bridge molecules on donor-bridge energetics and electronic interactions. Chemical Physics 281, 333-346.
35. DE VAULT, D. & CHANCE, B. (1966). Studies of photosynthesis using a pulsed laser. I. Temperature dependence of cytochrome oxidaton rate in chromatium. Evidence for tunneling. Biophysical Journal 6, 825-846.
36. DE VAULT, D., PARKES, J. H. & CHANCE, B. (1967). Electron tunnelling in cytochromes. Nature 215, 642-644.
37. DEFELIPPIS, M. R., MURTHY, C. P., FARAGGI, M. & KLAPPER, M. H. (1989). Pulse radiolytic measurement of redox potentials: the tyrosine and tryptophan radicals. Biochemistry 28, 4847-4853.
38. DEISENHOFER, J., EPP, O., MIKI, K., HUBER, R. & MICHEL, H. (1985). Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318, 618-624.
39. DEISENHOFER, J., EPP, O., SINNING, I. & MICHEL, H. (1995). Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction center from Rhodopseudomonas viridis. Journal of Molecular Biology 246, 429-457.
40. DI BILIO, A. J., HILL, M. G., BONANDER, N., KARLSSON, B. G., VILLAHERMOSA, R. M., MALMSTRÖM, B. G., WINKLER, J. R. & GRAY, H. B. (1997). Reorganization energy of blue copper: effects of temperature and driving force on the rates of electron transfer in ruthenium- and osmium-modified azurins. Journal of the American Chemical Society 119, 9921-9922.
41. DICK, L. A., MALFANT, I., KUILA, D., NEBOLSKY, S., NOCEK, J. M., HOFFMAN, B. M. & RATNER, M. A. (1998). Cryogenic electron tunneling within mixed-metal hemoglobin hybrids: protein glassing and electron-transfer energetics. Journal of the American Chemical Society 120, 11401-11407.
42. 5 to cytochrome c. Journal of Bioenergetics and Biomembranes 27, 331-340.
43. 5(histidine-33) derivative. Journal of the American Chemical Society 110, 429-434.
44. EVANS, M. G. & GERGELY, J. (1949). A discussion of the possibility of bands of energy levels in proteins. Electronic interactions in non bonded systems. Biochimica et Biophysica Acta 3, 188-197.
45. EVENSON, J. W. & KARPLUS, M. (1993). Effective coupling in biological electron transfer: exponential or complex distance dependence? Science 262, 1247-1249.
46. FOX, L. S., KOZIK, M., WINKLER, J. R. & GRAY, H. B. (1990). Gaussian free-energy dependence of electron-transfer rates in iridium complexes. Science 247, 1069-1071.
47. FRANZEN, S., GOLDSTEIN, R. F. & BOXER, S. G. (1993). Distance dependence of electron-transfer reactions in organized systems: the role of superexchange and non-condon effects in photosynthetic reaction centers. Journal of Physical Chemistry 97, 3040-3053.
48. FREED, K. F. (1983). Role of intramolecular vibrational relaxation on electron transfer rates - application to pentaammineruthenium(III)(histidine-33)-ferricytochrome c. Chemical Physics Letters 97, 489-493.
49. A-type centers: ligand-field control of ground-state properties related to electron transfer. Journal of the American Chemical Society 120, 5246-5263.
50. A by X-ray absorption spectroscopy: comparison to plastocyanin and relevance to electron transfer. Journal of the American Chemical Society 123, 5757-5767.
51. GEREN, L. M., BEASLEY, J. R., FINE, B. R., SAUNDERS, A. J., HIBDON, S., PIELAK, G. J., DURHAM, B. & MILLETT, F. (1995). Design of a ruthenium-cytochrome c derivative to measure electron transfer to the initial acceptor in cytochrome c oxidase. Journal of Biological Chemistry 270, 2466-2472.
52. GRAY, H. B., MALMSTRRÖM, B. G. & WILLIAMS, R. J. P. (2000). Copper coordination in blue proteins. Journal of Biological Inorganic Chemistry 5, 551-559.
53. GRAY, H. B. & WINKLER, J. R. (1996). Electron transfer in proteins. Annual Review of Biochemistry 65, 537-561.
54. GRAY, H. B. & WINKLER, J. R. (2001). Electron transfer in biological systems. In Electron Transfer in Chemistry, vol. III (ed. V. Balzani), pp. 1-175. Weinheim: Wiley-VCH.
55. GRAY, H. B. & WINKLER, J. R. (2003). Heme protein dynamics: electron tunneling and redox triggered folding. In The Porphyrin Handbook - Bioinorganic and Bioorganic Chemistry, vol. 11. The Porphyrin Handbook (eds. K. M. Kadish, K. M. Smith & R. Guilard), pp. 51-73. San Diego, CA: Academic Press.
56. GUNNER, M. R. & HONIG, B. (1991). Electrostatic control of midpoint potentials in the cytochrome subunit of the Rhodopseudomonas viridis reaction center. Proceedings of the National Academy of Sciences USA 88, 9151-9155.
57. GUNNER, M. R., NICHOLLS, A. & HONIG, B. (1996). Electrostatic potentials in Rhodopseudomonas viridis reaction centers: implications for the driving force and directionality of electron transfer. Journal of Physical Chemistry 100, 4277-4291.
58. A site and the oxidized bacteriochlorophyll dimer. Journal of Phyical Chemistry 90, 3783-3795.
59. HARRIMAN, A. (1987). Further comments on the redox potentials of tryptophan and tyrosine. Journal of Physical Chemistry 91, 6102-6104.
60. HEITELE, H., MICHEL-BEYERLE, M. E. & FINCKH, P. (1987). Electron transfer through intramolecular bridges in donor/acceptor systems. Chemical Physics Letters 134, 273-278.
61. HERZ, T., OTTO, P. & CLARK, T. (2000). On the band gap in peptide α-helices. International Journal of Quantum Chemistry 79, 120-124.
62. D®. Proceedings of the National Academy of Sciences USA 98, 6623-6628.
63. HOFFMAN, B. M. & RATNER, M. A. (1987). Gated electron transfer: when are observed rates controlled by conformational interconversion? Journal of the American Chemical Society 109, 6237-6243.
64. HOPFIELD, J. J. (1974). Electron transfer between biological molecules by thermally activated tunneling. Proceedings of the National Academy of Sciences USA 71, 3640-3644.
65. IGUCHI, K. (1997). Semiconductivity of protein: the Saxon-Hutner-Luttinger Theorem in biopolymers. International Journal of Modern Physics (B) 11, 2941-2960.
66. IWATA, S., OSTERMEIER, C., LUDWIG, B. & MICHEL, H. (1995). Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376, 660-669.
67. JORTNER, J., BIXON, M., LANGENBACHER, T. L. & MICHEL-BEYERLE, M. E. (1998). Charge transfer and transport in DNA. Proceedings of the National Academy of Sciences USA 95, 12759-12765.
68. JOVANlC, S. V., HARRIMAN, A. & SIMIC, M. G. (1986). Electron-transfer reactions of tryptophan and tyrosine derivatives. Journal of Physical Chemistry 90, 1935-1939.
69. KARPISHIN, T. B., GRINSTAFF, M. W., KOMAR-PANICUCCI, S., MCLENDON, G. & GRAY, H. B. (1994). Electron transfer in cytochrome c depends upon the structure of the intervening medium. Structure 2, 415-422.
70. KIRMAIER, C. & HOLTEN, D. (1987). Primary photochemistry of reaction centers from the photosynthetic bacteria. Photosynthesis Research 13, 225-260.
71. KOMIYA, H., YEATES, T. O., REES D. C., ALLEN, J. P. & FEHER, G. (1988). Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1 - symmetry relations and sequence comparisons between different species. Proceedings of The National Academy of Sciences USA 85, 9012-9016.
72. KUILA, D., BAXTER, W. W., NATAN, M. J. & HOFFMAN, B. M. (1991). Temperature-independent electron transfer in mixed-metal hemoglobin hybrids. Journal of Physical Chemistry 95, 1-3.
73. KUKI, A. & WOLYNES, P. G. (1987). Electron tunneling paths in proteins. Science 236, 1647-1652.
74. KUMAR, K., KURNIKOV, I. V., BERATAN, D. N., WALDECK, D. H. & ZIMMT, M. B. (1998). Use of modern electron transfer theories to determine the electronic coupling matrix elements in intramolecular systems. Journal of Physical Chemistry (A) 102, 5529-5541.
75. KUZNETSOV, A. M. & ULSTRUP, J. (1998). Electron Transfer in Chemistry and Biology: An Introduction to the Theory. Hoboken, NJ: John Wiley & Sons, Inc.
76. LANGEN, R. (1995). Electron transfer in proteins: theory and experiment. Ph.D. thesis, California Institute of Technology.
77. LANGEN, R., CHANG, I.-J., GERMANAS, J. P., RICHARDS, J. H., WINKLER, J. R. & GRAY, H. B. (1995). Electron tunneling in proteins: coupling through a β-strand. Science 268, 1733-1735.
78. LANGEN, R., COLÓN, J. L., CASIMIRO, D. R., KARPISHIN, T. B., WINKLER, J. R. & GRAY, H. B. (1996). Electron tunneling in proteins. Role of the intervening medium. Journal of Biological Inorganic Chemistry 1, 221-225.
79. LAWSON, J. M., CRAIG, D. C., PADDON-ROW, M. N., KROON, J. & VERHOEVFN, J. W. (1989). Through-bond modulation of intramolecular electron transfer in rigidly linked donor-acceptor systems. Chemical Physics Letters 164, 120-125.
80. LIANG, C. & NEWTON, M. D. (1992). Ab initio studies of electron transfer: pathway analysis of effective transfer integrals. Journal of Physical Chemistry 96, 2855-2866.
81. LIN, X., MURCHISON, H. A., NAGARAJAN, V., PARSON, W. W., ALLEN, J. P. & WILLLAMS, J. C. (1994a). Specific alteration of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Proceedings of the National Academy of Sciences USA 91, 10265-10269.
82. 2 to the reaction center in Rhodobacter sphaeroides. Biochemistry 33, 13517-13523.
83. LO CONTE, L., CHOTHIA, C. & JANIN, J. (1999). The atomic structure of protein-protein recognition sites. Journal of Molecular Biology 285, 2177-2198.
84. MARCUS, R. A. (1956). On the theory of oxidation-reduction reactions involving electron transfer. I. Journal of Chemical Physics 24, 966-978.
85. MARCUS, R. A. & SUTIN, N. (1975). Electron-transfer reactions with unusual activation parameters. A treatment of reactions accompanied by large entropy decreases. Inorganic Chemistry 14, 213-216.
86. MARCUS, R. A. & SUTIN, N. (1985). Electron transfers in chemistry and biology. Biochimica et Biophysica Acta 811, 265-322.
87. 5. Journal of Bioenergetics and Biomembranes 27, 311-330.
88. MAUK, A. G., SCOTT, R. A. & GRAY, H. B. (1980). Distances of electron transfer to and from metalloprotein redox sites in reactions with inorganic complexes. Journal of the American Chemical Society 102, 4360-4363.
89. 5 and cytochrome c. Biochemistry 21, 1843-1846.
90. MCCLESKEY, T. M., WINKLER, J. R. & GRAY, H. B. (1992). Driving-force effects on the rates of bimolecular electron-transfer reactions. Journal of the American Chemical Society 114, 6935-6937.
91. MCCONNELL, H. M. (1961). Intramolecular charge transfer in aromatic free radicals. Journal of Chemical Physics 35, 508-515.
92. MCGOURTY, J. L., BLOUGH, N. V. & HOFFMAN, B. M. (1983). Electron transfer at crystallographically known long distances (25-Å) in [Zn(II),Fe(III)] hybrid hemoglobin. Journal of the American Chemical Society 105, 4470-4472.
93. MCLENDON, G. & HAKE, R. (1992). Interprotein electron transfer. Chemical Reviews 92, 481-490.
94. 5 couple. Journal of the American Chemical Society 107, 7811-7816.
95. MCLENDON, G., ZHANG, Q., WALLIN, S. A., MILLER, R. M., BILLSTONE, V., SPEARS, K. G. & HOFFMAN, B. M. (1993). Thermodynamic and kinetic aspects of binding in the cytochrome c/cytochrome c peroxidase complex. Journal of the American Chemical Society 115, 3665-3669.
96. MEADE, T. J., GRAY, H. B. & WINKLER, J. R. (1989). Driving-force effects on the rate of long-range electron transfer in ruthenium-modified cytochrome c. Journal of the American Chemical Society 111, 4353-4356.
97. MEDVEDEV, D. M., DAIZADEH, I. & STUCHEBRUKHOV, A. A. (2000). Electron transfer tunneling pathways in bovine heart cytochrome c oxidase. Journal of the American Chemical Society 122, 6571-6582.
98. 5-cytochrome c complex. Biochemistry 32, 622-627.
99. MILLER, J. R., BEITZ, J. V. & HUDDLESTON, R. K. (1984). Effect of free energy on rates of electron transfer between molecules. Journal of the American Chemical Society 106, 5057-5068.
100. MINES, G. A., BJERRUM, M. J., HILL, M. G., CASIMIRO, D. R., CHANG, I.-J., WINKLER, J. R. & GRAY, H. B. (1996). Rates of heme oxidation and reduction in Ru(His33)cytochrome c at very high driving forces. Journal of the American Chemical Society 118, 1961-1965.
101. MOORE, G. R. & PETTIGREW, G. W. (1990). Cytochromes c: Evolutionary, Structural, and Physicochemical Aspects. New York: Springer-Verlag.
102. MOSER, C. C., KESKE, J. M., WARNCKE, K., FARID, R. S. & DUTTON, P. L. (1992). Nature of biological electron transfer. Nature 355, 796-802.
103. NEWTON, M. D. (1988). Electronic structure analysis of electron-transfer matrix elements for transition metal redox pairs. Journal of Physical Chemistry 92, 3049-3056.
104. NOCEK, J. M., ZHOU, J. S., DEFOREST, S., PRIYADARSHY, S., BERATAN, D. N., ONUCHIC, J. N. & HOFFMAN, B. M. (1996). Theory and practice of electron transfer within protein-protein complexes: application to the multi-domain binding of cytochrome c by cytochrome c peroxidase. Chemical Reviews 96, 2459-2489.
105. ONUCHIC, J. N. & BERATAN, D. N. (1990). A predictive theoretical model for electron tunneling pathways in proteins. Journal of Chemical Physics 92, 722-733.
106. ONUCHIC, J. N., BERATAN, D. N., WINKLER, J. R. & GRAY, H. B. (1992). Pathway analysis of protein electron transfer reactions. Annual Review of Biophysics and Biomolecular Structure 21, 349-377.
107. ORTEGA, J. M. & MATHIS, P. (1993). Electron transfer from the tetraheme cytochrome to the special pair in isolated reaction centers of Rhodopseudomonas viridis. Biochemistry 32, 1141-1151.
108. OVERFIELD, R. E., SCHERZ, A., KAUFMANN, K. J. & WASIELEWSKI, M. R. (1983). Photoinduced electron-transfer reactions in a chlorophyllide-pheophorbide cyclophane. A model for photosynthetic reaction centers. Journal of the American Chemical Society 105, 5747-5752.
109. PADDON-ROW, M. N. (2003). Superexchange-mediated charge separation and charge recombination in covalently linked donor-bridge-acceptor systems. Australian Journal of Chemistry 56, 729-748.
110. PAGE, C. C., MOSER, C. C., CHEN, X. & DUTTON, P. L. (1999). Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47-52.
111. PAN, L. P., HIBDON, S., LIU, R.-Q., DURHAM, B. & MILLETT, F. (1993). Intracomplex electron transfer between ruthenium-cytochrome c derivatives and cytochrome c oxidase. Biochemistry 32, 8492-8498.
112. PASCHER, T., CHESICK, J. P., WINKLER, J. R. & GRAY, H. B. (1996). Protein folding triggered by electron transfer. Science 271, 1558-1560.
113. PASCHER, T., KARLSSON, B. G., NORDLING, M., MALMSTRÖM, B. G. & VANNGARD, T. (1993). Reduction potentials and their pH dependence in site-directed mutant forms of azurin from Pseudomonas aeruginosa. European Journal of Biochemistry 212, 289-296.
114. PASMAN, P., KOPER, N. W. & VERHOEVEN, J. W. (1982). Photoinduced long-range electron transfer in rigid bichromophoric molecules. Recueil des Travaux Chimiques des Pays-Bas [Journal of the Royal Netherlands Chemical Society] 101, 363-364.
115. PELLETIER, H. & KRAUT, J. (1992). Crystal structure of a complex between electron-transfer partners, cytochrome c peroxidase and cytochrome c. Science 258, 1748-1755.
116. III]hemoglobin hybrids. Journal of the American Chemical Society 108, 1739-1746.
117. PLETNEVA, E. V., FULTON, D. B., KOHZUMA, T. & KOSTIC, N. M. (2000). Protein docking and gated electron-transfer reactions between zinc cytochrome c and the new plastocyanin from the fern Dryopteris crassirhizoma. Direct kinetic evidence for multiple binary complexes. Journal of the American Chemical Society 122, 1034-1046.
118. 2+ (tpy=2,2′:6,2″-terpyridine) by ferric ion in aqueous glasses at 77 K. Journal of the American Chemical Society 122, 8187-8191.
119. POULOS, T. L. & KRAUT, J. (1980). A hypothetical model of the cytochrome c peroxidase ® cytochrome c electron transfer complex. Journal of Biological Chemistry 255, 10322-10330.
120. 5 surface mutants and cytochrome c. Molecular Crystals and Liquid Crystals 194, 311-316.
121. RAMIREZ, B. E., MALMSTRÖM, B. G., WINKLER, J. R. & GRAY, H. B. (1995). The currents of life: the terminal electron-transfer complex of respiration. Proceedings of the National Academy of Sciences USA 92, 11949-11951.
122. REGAN, J. J., DI BILIO, A. J., LANGEN, R., SKOV, L. K., WINKLER, J. R., GRAY, H. B. & ONUCHIC, J. N. (1995). Electron tunneling in azurin: coupling across a β sheet. Chemistry and Biology 2, 489-496.
123. REGAN, J. J. & ONUCHIC, J. N. (1999). Electron-transfer tubes. Advances in Chemical Physics 107, 497-553.
124. REGAN, J. J., RAMIREZ, B. E., WINKLER, J. R., GRAY, H. B. & MALMSTÖM, B. G. (1998). Pathways for electron tunneling in cytochrome c oxidase. Journal of Bioenergetics and Biomembranes 30, 35-39.
125. REHM, D. & WELLER, A. (1970). Kinetics of fluorescence quenching by electron and H-atom transfer. Israel Journal of Chemistry 8, 259-271.
126. ROBERTS, V. A. & PIQUE, M. E. (1999). Definition of the interaction domain for cytochrome c on cytochrome c oxidase. III. Prediction of the docked complex by a complete systematic search. Journal of Biological Chemistry 274, 38051-38060.
127. SABAHI, A. & WITTUNG-STAFSHEDE, P. (2002). Unfolding the unique c-type heme protein, Chlamydomonas reinhardtii cytochrome f. Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology 1596, 163-171.
128. 5. Journal of Molecular Biology 102, 563-568.
129. SCOTT, R. A. & MAUK, A. G. (1996). Cytochrome c - A Multidisciplinary Approach, pp. 738. Sausalito, CA: University Science Books.
130. SHEU, S.-Y., YANG, D.-Y., SELZLE, H. L. & SCHLAG, E. W. (2002). Charge transport in a polypeptide chain. European Physiol Journal (D) 20, 557-563.
131. SHOPES, R. J., LEVINE, L. M. A., HOLTEN, D. & WRAIGHT, C. A. (1987). Kinetics of oxidation of the bound cytochromes in reaction centers from Rhodopseudomonas viridis. Photosynthesis Research 12, 165-180.
132. III(CN). Journal of the American Chemical Society 106, 5012-5013.
133. SIMONSON, T. (2002). Gaussian fluctuations and linear response in an electron transfer protein. Proceedings of the National Academy of Sciences USA 99, 6544-6549.
134. SKOURTIS, S. S. & BERATAN, D. N. (1997). High and low resolution theories of protein electron transfer. Journal of Biological Inorganic Chemistry 2, 378-386.
135. SKOURTIS, S. S. & BERATAN, D. N. (1998). Electron transfer mechanisms. Current Opinion in Chemical Biology 2, 235-243.
136. 2(im)(His83)-modified azurin increase below 220 K. Journal of the American Chemical Society 120, 1102-1103.
137. SMALLEY, J. F., FELDBERG, S. W., CHIDSEY, C. E. D., LINFORD, M. R., NEWTON, M. D. & LIU, Y.-P. (1995). The kinetics of electron transfer through ferrocene-terminated alkanethiol monolayers on gold. Journal of Physical Chemistry 99, 13141-13149.
138. SMALLEY, J. F., FINKLEA, H. O., CHIDSEY, C. E. D., LINFORD, M. R., CREAGER, S. E., FERRARIS, J. P., CHALFANT, K., ZAWODZINSK, T., FELDBERG, S. W. & NEWTON, M. D. (2003). Heterogeneous electron-transfer kinetics for ruthenium and ferrocene redox moieties through alkanethiol monolayers on gold. Journal of the American Chemical Society 125, 2004-2013.
139. 562 redox variants: strategies for modulating redox potential revealed using a library approach. Biochemistry 41, 4321-4328.
140. STEMP, E. D. A. & HOFFMAN, B. M. (1993). Cytochrome c peroxidase binds two molecules of cytochrome c: evidence for a low-affinity, electron-transfer-active site on cytochrome c peroxidase. Biochemistry 32, 10848-10865.
141. STUBBE, J., NOCERA, D. G., YEE, C. S. & CHANG, M. C. Y. (2003). Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer? Chemical Reviews 103, 2167-2201.
142. STUBBE, J. & VAN DER DONK, W. A. (1998). Protein radicals in enzyme catalysis. Chemical Reviews 98, 705-762.
143. STUCHEBRUKHOV, A. A. (1996). Tunneling currents in electron-transfer reactions in proteins. 2. Calculation of electronic superexchange matrix element and tunneling currents using nonorthogonal basis sets. Journal of Chemical Physics 105, 10819-10829.
144. STUCHEBRUKHOV, A. A. (2001). Toward ab initio theory of long-distance electron tunneling in proteins: tunneling currents approach. Advances in Chemical Physics 118, 1-44.
145. SUCHETA, A., SZUNDI, I. & EINARSDOTTIR, O. (1998). Intermediates in the reaction of fully reduced cytochrome c oxidase with dioxygen. Biochemistry 37, 17905-17914.
146. SZENT-GYÖRGYI, A. (1941). Towards a new biochemistry? Science 93, 609-611.
147. TEZCAN, F. A., CRANE, B. R., WINKLER, J. R. & GRAY, H. B. (2001). Electron tunneling in protein crystals. Proceedings of the National Academy of Sciences USA 98, 5002-5006.
148. TEZCAN, F. A., WINKLER, J. R. & GRAY, H. B. (1998). Effects of ligation and folding on reduction potentials of heme proteins. Journal of the American Chemical Society 120, 13383-13388.
149. TOMMOS, C., SKALICKY, J. J., PILOUD, D. L., WAND, A. J. & DUTTON, P. L. (1999). De novo proteins as models of radical enzymes. Biochemistry 38, 9495-9507.
150. TSUKIHARA, T., AOYAMA, H., YAMASHITA, E., TOMIZAKI, T., YAMAGUCHI, H., SHINZAWA-ITOH, K., NAKASHIMA, R., YAONO, R. & YOSHIKAWA, S. (1995). Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 269, 1071-1074.
151. VARADARAJAN, R., ZEWERT, T. E., GRAY, H. B. & BOXER, S. G. (1989). Effects of buried ionizable amino acids on the reduction potential of recombinant myoglobin. Science 243, 69-72.
152. 2 to the photosynthetic reaction center of the purple bacterium from Rhodobacter sphaeroides. Biophysical Journal 74, 3226-3240.
153. VERHOEVEN, J. W. (1999). From close contact to long-range intramolecular electron transfer. Advances in Chemical Physics 106, 603-644.
154. WASIELEWSKI, M. R. (1992). Photoinduced electron transfer in supramolecular systems for artificial photosynthesis. Chemical Reviews 92, 435-461.
155. A site of cytochrome c oxidase. Journal of the American Chemical Society 119, 613-614.
156. WINKLER, J. R. (2000). Electron tunneling pathways in proteins. Current Opinion in Chemical Biology 4, 192-198.
157. WINKLER, J. R., DI BILIO, A., FARROW, N. A., RICHARDS, J. H. & GRAY, H. B. (1999). Electron tunneling in biological molecules. Pure and Applied Chemistry 71, 1753-1764.
158. WINKLER, J. R. & GRAY, H. B. (1992). Electron transfer in ruthenium-modified proteins. Chemical Reviews 92, 369-379.
159. WINKLER, J. R., NOCERA, D. G., YOCOM, K. M., BORDIGNON, E. & GRAY, H. B. (1982). Electron-transfer kinetics of pentaammineruthenium(III)(histidine-33)-ferricytochrome c. Measurement of the rate of intramolecular electron transfer between redox centers separated by 15 Å in a protein. Journal of the American Chemical Society 104, 5798-5800.
160. WINKLER, J. R., WITTUNG-STAFSHEDE, P., LECKNER, J., MALMSTRÖM, B. G. & GRAY, H. B. (1997). Effects of folding on metalloprotein active sites. Proceedings of the National Academy of Sciences USA 94, 4246-4249.
161. WUTTKE, D. S., BJERRUM, M. J., WINKLER, J. R. & GRAY, H. B. (1992). Electron-tunneling pathways in cytochrome c. Science 256, 1007-1009.
162. YE, Y.-J. & LADIK, J. (1994). Theory of hopping conductivity of proteins. International Journal of Quantum Chemistry 52, 491-506.
163. YOCOM, K. M., SHELTON, J. B., SHELTON, J. R., SCHROEDER, W. E., WOROSILA, G., ISIED, S. S., BORDIGNON, E. & GRAY, H. B. (1982). Preparation and characterization of a pentammineruthenium(III) derivative of horse heart ferricytochrome c. Proceedings of the National Academy of Sciences USA 79, 7052-7055.
164. YOSHIKAWA, S., SHINZAWA-ITOH, K., NAKASHIMA, R., YAONO, R., YAMASHITA, E., INOUE, N., YAO, M., FEI, J. M., LIBEU, C. P., MIZUSHIMA, T., YAMAGUCHI, H., TOMIZAKI, T. & TSUKIHARA, T. (1998). Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280, 1723-1729.