Distance-independent charge recombination kinetics in cytochrome c-cytochrome c peroxidase complexes: Compensating changes in the electronic coupling and reorganization energies

Journal of Physical Chemistry B

Volumn 117, Issue 31, 2013, Pages 9129-9141

  Jiang, Nan ^a   Kuznetsov, Aleksey ^a   Nocek, Judith M ^b   Hoffman, Brian M ^b   Crane, Brian R ^c   Hu, Xiangqian ^a   Beratan, David N ^a,d  

^a DUKE UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c Department of Molecular Biology and Genetics   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHARGE RECOMBINATION KINETICS; CHARGE RECOMBINATIONS; CONFORMATIONAL DIFFERENCES; DONOR-ACCEPTOR DISTANCE; ELECTRONIC COUPLING; RECOMBINATION KINETICS; RECOMBINATION REACTIONS; REORGANIZATION ENERGIES;

KINETICS; PROTEINS; RATE CONSTANTS;

TUNGSTEN COMPOUNDS;

EID: 84881430037     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp401551t     Document Type: Article

References (117)

1. Bendall, D. S. Protein Electron Transfer; Bios Scientific Publishers: Oxford, U.K., 1996.
2. Lippard, S. J.; Berg, J. M. Principles of Bioinorganic Chemistry; University Science Books: Mill Valley, CA, 1994.
3. Bertini, I.; Gray, H. B.; Stiefel, E.; Valentine, J. S. Biological Inorganic Chemistry; University Science Books: Mill Valley, CA, 2007.
4. Balzani, V., Ed. Electron Transfer in Chemistry; Wiley-VCH: New York, 2001.
5. Gray, H. B.; Winkler, J. R. Electron Tunneling through Proteins Q. Rev. Biophys. 2003, 36, 341-372
6. Beratan, D. N.; Skourtis, S. S. Electron Transfer Mechanisms Curr. Opin. Chem. Biol. 1998, 2, 235-243
7. Beratan, D. N.; Skourtis, S. S.; Balabin, I. A.; Balaeff, A.; Keinan, S.; Venkatramani, R.; Xiao, D. Q. Steering Electrons on Moving Pathways Acc. Chem. Res. 2009, 42, 1669-1678
8. Skourtis, S. S.; Waldeck, D. H.; Beratan, D. N. Fluctuations in Biological and Bioinspired Electron-Transfer Reactions Annu. Rev. Phys. Chem. 2010, 61, 461-485
9. Kang, S. A.; Crane, B. R. Effects of Interface Mutations on Association Modes and Electron-Transfer Rates between Proteins Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 15465-15470
10. Pletneva, E. V.; Fulton, D. B.; Kohzuma, T.; Kostic, N. M. 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 J. Am. Chem. Soc. 2000, 122, 1034-1046
11. Nocek, J. M.; Zhou, J. S.; DeForest, S.; Priyadarshy, S.; Beratan, D. N.; Onuchic, J. N.; Hoffman, B. M. Theory and Practice of Electron Transfer within Protein-Protein Complexes: Application to the Multidomain Binding of Cytochrome c by Cytochrome c Peroxidase Chem. Rev. 1996, 96, 2459-2489
12. Mei, H. K.; Wang, K. F.; Peffer, N.; Weatherly, G.; Cohen, D. S.; Miller, M.; Pielak, G.; Durham, B.; Millett, F. Role of Configurational Gating in Intracomplex Electron Transfer from Cytochrome c to the Radical Cation in Cytochrome c Peroxidase Biochemistry 1999, 38, 6846-6854
13. 5 and a Suite of Myoglobin Surface-Charge Mutants. Introduction of a Functional-Docking Algorithm for Protein-Protein Complexes J. Am. Chem. Soc. 2004, 126, 2785-2798
14. Hoffman, B. M.; Celis, L. M.; Cull, D. A.; Patel, A. D.; Seifert, J. L.; Wheeler, K. E.; Wang, J. Y.; Yao, J.; Kurnikov, I. V.; Nocek, J. M. Differential Influence of Dynamic Processes on Forward and Reverse Electron Transfer across a Protein-Protein Interface Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 3564-3569
15. 5 Complex with a Redesigned Interface Science 2010, 330, 1075-1078
16. 6 from Chlamydomonas Reinhardtii J. Am. Chem. Soc. 2003, 125, 10598-10607
17. 5 J. Am. Chem. Soc. 1993, 115, 5516-5521
18. Everest, A. M.; Wallin, S. A.; Stemp, E. D. A.; Nocek, J. M.; Mauk, A. G.; Hoffman, B. M. Aromatic Hole Superexchange through Position-82 of Cytochrome c Is Not Required for Intracomplex Electron-Transfer to Zinc Cytochrome- c Peroxidase J. Am. Chem. Soc. 1991, 113, 4337-4338
19. Niki, K.; Hardy, W. R.; Hill, M. G.; Li, H.; Sprinkle, J. R.; Margoliash, E.; Fujita, K.; Tanimura, R.; Nakamura, N.; Ohno, H. Coupling to Lysine-13 Promotes Electron Tunneling through Carboxylate-Terminated Alkanethiol Self-Assembled Monolayers to Cytochrome c J. Phys. Chem. B 2003, 107, 9947-9949
20. 5 and Cytochrome c Biochemistry 2004, 43, 3527-3536
21. Zhou, J. S.; Tran, S. T.; McLendon, G.; Hoffman, B. M. Photoinduced Electron Transfer between Cytochrome c Peroxidase (D37K) and Zn-Substituted Cytochrome c: Probing the Two-Domain Binding and Reactivity of the Peroxidase J. Am. Chem. Soc. 1997, 119, 269-277
22. Davidson, V. L. What Controls the Rates of Interprotein Electron-Transfer Reactions Acc. Chem. Res. 2000, 33, 87-93
23. Davidson, V. L. Protein Control of True, Gated, and Coupled Electron Transfer Reactions Acc. Chem. Res. 2008, 41, 730-738
24. Pelletier, H.; Kraut, J. Crystal-Structure of a Complex between Electron-Transfer Partners, Cytochrome c Peroxidase and Cytochrome c Science 1992, 258, 1748-1755
25. Erman, J. E.; Vitello, L. B. Yeast Cytochrome c Peroxidase: Mechanistic Studies Via Protein Engineering Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 2002, 1597, 193-220
26. Volkov, A. N.; Nicholls, P.; Worrall, J. A. R. The Complex of Cytochrome c and Cytochrome c Peroxidase: The End of the Road? Biochim. Biophys. Acta, Bioenerg. 2011, 1807, 1482-1503
27. Battistuzzi, G.; Bellei, M.; Bortolotti, C. A.; Sola, M. Redox Properties of Heme Peroxidases Arch. Biochem. Biophys. 2010, 500, 21-36
28. Gray, H. B.; Winkler, J. R. Long-Range Electron Transfer Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 3534-3539
29. 2+ (Tpy=2,2′:6,2″-Terpyridine) by Ferric Ions in Aqueous Glasses at 77 K J. Am. Chem. Soc. 2000, 122, 8187-8191
30. Hopfield, J. J. Electron-Transfer between Biological Molecules by Thermally Activated Tunneling Proc. Natl. Acad. Sci. U.S.A. 1974, 71, 3640-3644
31. Kang, S. A.; Marjavaara, P. J.; Crane, B. R. Electron Transfer between Cytochrome c and Cytochome c Peroxidase in Single Crystals J. Am. Chem. Soc. 2004, 126, 10836-10837
32. Sancar, A. Structure and Function of DNA Photolyase and Cryptochrome Blue-Light Photoreceptors Chem. Rev. 2003, 103, 2203-2237
33. Noy, D.; Moser, C. C.; Dutton, P. L. Design and Engineering of Photosynthetic Light-Harvesting and Electron Transfer Using Length, Time, and Energy Scales Biochim. Biophys. Acta, Bioenerg. 2006, 1757, 90-105
34. Wei, C. C.; Crane, B. R.; Stuehr, D. J. Tetrahydrobiopterin Radical Enzymology Chem. Rev. 2003, 103, 2365-2383
35. Stubbe, J.; Nocera, D. G.; Yee, C. S.; Chang, M. C. Y. Radical Initiation in the Class I Ribonucleotide Reductase: Long-Range Proton-Coupled Electron Transfer? Chem. Rev. 2003, 103, 2167-2201
36. Seyedsayamdost, M. R.; Reece, S. Y.; Nocera, D. G.; Stubbe, J. Mono-, Di-, Tri-, and Tetra-Substituted Fluorotyrosines: New Probes for Enzymes That Use Tyrosyl Radicals in Catalysis J. Am. Chem. Soc. 2006, 128, 1569-1579
37. Liang, N.; Mauk, A. G.; Pielak, G. J.; Johnson, J. A.; Smith, M.; Hoffman, B. M. Regulation of Interprotein Electron-Transfer by Residue-82 of Yeast Cytochrome c Science 1988, 240, 311-313
38. Di Bilio, A. J.; Crane, B. R.; Wehbi, W. A.; Kiser, C. N.; Abu-Omar, M. M.; Carlos, R. M.; Richards, J. H.; Winkler, J. R.; Gray, H. B. Properties of Photogenerated Tryptophan and Tyrosyl Radicals in Structurally Characterized Proteins Containing Rhenium(I) Tricarbonyl Diimines J. Am. Chem. Soc. 2001, 123, 3181-3182
39. Shih, C.; Museth, A. K.; Abrahamsson, M.; Blanco-Rodriguez, A. M.; Di Bilio, A. J.; Sudhamsu, J.; Crane, B. R.; Ronayne, K. L.; Towrie, M.; Vlcek, A. Tryptophan-Accelerated Electron Flow through Proteins Science 2008, 320, 1760-1762
40. Seifert, J. L.; Pfister, T. D.; Nocek, J. M.; Lu, Y.; Hoffman, B. M. Hopping in the Electron-Transfer Photocycle of the 1: 1 Complex of Zn-Cytochrome c Peroxidase with Cytochrome c J. Am. Chem. Soc. 2005, 127, 5750-5751
41. Debler, E. W.; Kaufmann, G. F.; Meijler, M. M.; Heine, A.; Mee, J. M.; Pljevaljcic, G.; Di Bilio, A. J.; Schultz, P. G.; Millar, D. P.; Janda, K. D. Deeply Inverted Electron-Hole Recombination in a Luminescent Antibody-Stilbene Complex Science 2008, 319, 1232-1235
42. Blumberger, J.; Klein, M. L. Reorganization Free Energies for Long-Range Electron Transfer in a Porphyrin-Binding Four-Helix Bundle Protein J. Am. Chem. Soc. 2006, 128, 13854-13867
43. Treutlein, H.; Schulten, K.; Brunger, A. T.; Karplus, M.; Deisenhofer, J.; Michel, H. Chromophore Protein Interactions and the Function of the Photosynthetic Reaction Center-a Molecular-Dynamics Study Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 75-79
44. Parson, W. W.; Chu, Z. T.; Warshel, A. Reorganization Energy of the Initial Electron-Transfer Step in Photosynthetic Bacterial Reaction Centers Biophys. J. 1998, 74, 182-191
45. Zeng, X. C.; Hu, H.; Hu, X. Q.; Cohen, A. J.; Yang, W. T. Ab Initio Quantum Mechanical/Molecular Mechanical Simulation of Electron Transfer Process: Fractional Electron Approach. J. Chem. Phys. 2008, 128.
46. Cascella, M.; Magistrato, A.; Tavernelli, I.; Carloni, P.; Rothlisberger, U. Role of Protein Frame and Solvent for the Redox Properties of Azurin from Pseudomonas Aeruginosa Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 19641-19646
47. Petruk, A. A.; Bartesaghi, S.; Trujillo, M.; Estrin, D. A.; Murgida, D.; Kalyanaraman, B.; Marti, M. A.; Radi, R. Molecular Basis of Intramolecular Electron Transfer in Proteins During Radical-Mediated Oxidations: Computer Simulation Studies in Model Tyrosine-Cysteine Peptides in Solution Arch. Biochem. Biophys. 2012, 525, 82-91
48. Alvarez-Paggi, D.; Martin, D. F.; DeBiase, P. M.; Hildebrandt, P.; Marti, M. A.; Murgida, D. H. Molecular Basis of Coupled Protein and Electron Transfer Dynamics of Cytochrome c in Biomimetic Complexes J. Am. Chem. Soc. 2010, 132, 5769-5778
49. Kobayashi, C.; Baldridge, K.; Onuchic, J. N. Multiple Versus Single Pathways in Electron Transfer in Proteins: Influence of Protein Dynamics and Hydrogen Bonds J. Chem. Phys. 2003, 119, 3550-3558
50. Kurnikov, I. V.; Beratan, D. N. Ab Initio Based Effective Hamiltonians for Long-Range Electron Transfer: Hartree-Fock Analysis J. Chem. Phys. 1996, 105, 9561-9573
51. Liang, C. X.; Newton, M. D. Ab Initio Studies of Electron-Transfer- Pathway Analysis of Effective Transfer Integrals J. Phys. Chem. 1992, 96, 2855-2866
52. Newton, M. D. Thermal and Optical Electron Transfer Involving Transition Metal Complexes: Insights from Theory and Computation Coord. Chem. Rev. 2003, 238, 167-185
53. Onuchic, J. N.; Beratan, D. N.; Hopfield, J. J. Some Aspects of Electron-Transfer Reaction Dynamics J. Phys. Chem. 1986, 90, 3707-3721
54. Regan, J. J.; Di Bilio, A. J.; Langen, R.; Skov, L. K.; Winkler, J. R.; Gray, H. B.; Onuchic, J. N. Electron-Tunneling in Azurin-the Coupling across a Beta-Sheet Chem. Biol. 1995, 2, 489-496
55. Wolfgang, J.; Risser, S. M.; Priyadarshy, S.; Beratan, D. N. Secondary Structure Conformations and Long Range Electronic Interactions in Oligopeptides J. Phys. Chem. B 1997, 101, 2986-2991
56. Jones, M. L.; Kurnikov, I. V.; Beratan, D. N. The Nature of Tunneling Pathway and Average Packing Density Models for Protein-Mediated Electron Transfer J. Phys. Chem. A 2002, 106, 2002-2006
57. Regan, J. J.; Onuchic, J. N. Electron-Transfer Tubes Adv. Chem. Phys. 1999, 107, 497-553
58. Skourtis, S. S.; Regan, J. J.; Onuchic, J. N. Electron-Transfer in Proteins-a Novel-Approach for the Description of Donor-Acceptor Coupling J. Phys. Chem. 1994, 98, 3379-3388
59. Stuchebrukhov, A. A. Tunneling Currents in Long-Distance Electron Transfer Reactions. V. Effective One Electron Approximation J. Chem. Phys. 2003, 118, 7898-7906
60. Zhang, L. Y.; Friesner, R. A.; Murphy, R. B. Ab Initio Quantum Chemical Calculation of Electron Transfer Matrix Elements for Large Molecules J. Chem. Phys. 1997, 107, 450-459
61. Zheng, X. H.; Stuchebrukhov, A. A. Electron Tunneling in the His(126) Ru-Modified Azurin: Tunneling Jumps between Protein Strands Via Hydrogen Bonds J. Phys. Chem. B 2003, 107, 9579-9584
62. Balabin, I. A.; Beratan, D. N.; Skourtis, S. S. Persistence of Structure over Fluctuations in Biological Electron-Transfer Reactions. Phys. Rev. Lett. 2008.
63. Hatcher, E.; Balaeff, A.; Keinan, S.; Venkatramani, R.; Beratan, D. N. PNA Versus DNA: Effects of Structural Fluctuations on Electronic Structure and Hole-Transport Mechanisms J. Am. Chem. Soc. 2008, 130, 11752-11761
64. Prytkova, T. R.; Beratan, D. N.; Skourtis, S. S. Photoselected Electron Transfer Pathways in DNA Photolyase Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 802-807
65. Prytkova, T. R.; Kurnikov, I. V.; Beratan, D. N. Ab Initio Based Calculations of Electron-Transfer Rates in Metalloproteins J. Phys. Chem. B 2005, 109, 1618-1625
66. Skourtis, S. S.; Beratan, D. N. Theories of Structure-Function Relationships for Bridge-Mediated Electron Transfer Reactions Adv. Chem. Phys. 1999, 106, 377-452
67. Beratan, D. N.; Betts, J. N.; Onuchic, J. N. Protein Electron-Transfer Rates Set by the Bridging Secondary and Tertiary Structure Science 1991, 252, 1285-1288
68. Ridley, J.; Zerner, M. Intermediate Neglect of Differential Overlap Technique for Spectroscopy-Pyrrole and Azines Theor. Chim. Acta 1973, 32, 111-134
69. Cave, R. J.; Newton, M. D. Generalization of the Mulliken-Hush Treatment for the Calculation of Electron Transfer Matrix Elements Chem. Phys. Lett. 1996, 249, 15-19
70. Cave, R. J.; Newton, M. D. Calculation of Electronic Coupling Matrix Elements for Ground and Excited State Electron Transfer Reactions: Comparison of the Generalized Mulliken-Hush and Block Diagonalization Methods J. Chem. Phys. 1997, 106, 9213-9226
71. Marcus, R. A.; Sutin, N. Electron Transfers in Chemistry and Biology Biochim. Biophys. Acta 1985, 811, 265-322
72. Fox, L. S.; Kozik, M.; Winkler, J. R.; Gray, H. B. Gaussian Free-Energy Dependence of Electron-Transfer Rates in Iridium Complexes Science 1990, 247, 1069-1071
73. A Site and the Oxidized Bacteriochlorophyll Dimer J. Phys. Chem. 1986, 90, 3783-3795
74. Gould, I. R.; Ege, D.; Moser, J. E.; Farid, S. Efficiencies of Photoinduced Electron-Transfer Reactions-Role of the Marcus Inverted Region in Return Electron-Transfer within Geminate Radical-Ion Pairs J. Am. Chem. Soc. 1990, 112, 4290-4301
75. Sharp, K. A. Calculation of Electron Transfer Reorganization Energies Using the Finite Difference Poisson-Boltzmann Model Biophys. J. 1998, 74, 1241-1250
76. Humphrey, W.; Dalke, A.; Schulten, K. Vmd: Visual Molecular Dynamics J. Mol. Graph. Model. 1996, 14, 33-38
77. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with Namd J. Comput. Chem. 2005, 26, 1781-1802
78. MacKerell, A. D.; Bashford, D.; Bellott, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
79. Mackerell, A. D.; Feig, M.; Brooks, C. L. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-Phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
80. Stote, R. H.; Karplus, M. Zinc-Binding in Proteins and Solution-a Simple but Accurate Nonbonded Representation Proteins 1995, 23, 12-31
81. Balabin, I. A.; Hu, X. Q.; Beratan, D. N. Exploring Biological Electron Transfer Pathway Dynamics with the Pathways Plugin for VMD J. Comput. Chem. 2012, 33, 906-910
82. Hoffman, B. M. Triplet-State Electron-Paramagnetic Resonance Studies of Zinc Porphyrins and Zinc-Substituted Hemoglobins and Myoglobins J. Am. Chem. Soc. 1975, 97, 1688-1694
83. Jordan, K. D.; Paddon-Row, M. N. Analysis of the Interactions Responsible for Long-Range through-Bond-Mediated Electronic Coupling between Remote Chromophores Attached to Rigid Polynorbornyl Bridges Chem. Rev. 1992, 92, 395-410
84. Frisch, M. J.; Gaussian 03, revision D.02; Gaussian, Inc.: Wallingford, CT, 2003.
85. Becke, A. D. Density-Functional Exchange-Energy Approximation with Correct Asymptotic-Behavior Phys. Rev. A 1988, 38, 3098-3100
86. Becke, A. D. Density-Functional Thermochemistry. 3. The Role of Exact Exchange J. Chem. Phys. 1993, 98, 5648-5652
87. Binning, R. C.; Curtiss, L. A. Compact Contracted Basis-Sets for 3rd-Row Atoms-Ga-Kr J. Comput. Chem. 1990, 11, 1206-1216
88. Blaudeau, J. P.; McGrath, M. P.; Curtiss, L. A.; Radom, L. Extension of Gaussian-2 (G2) Theory to Molecules Containing Third-Row Atoms K and Ca J. Chem. Phys. 1997, 107, 5016-5021
89. Ditchfield, R.; Hehre, W. J.; Pople, J. A. Self-Consistent Molecular-Orbital Methods 9. Extended Gaussian-Type Basis for Molecular-Orbital Studies of Organic Molecules J. Chem. Phys. 1971, 54, 724-728
90. Francl, M. M.; Pietro, W. J.; Hehre, W. J.; Binkley, J. S.; Gordon, M. S.; Defrees, D. J.; Pople, J. A. Self-Consistent Molecular-Orbital Methods. 23. A Polarization-Type Basis Set for 2nd-Row Elements J. Chem. Phys. 1982, 77, 3654-3665
91. Gordon, M. S. The Isomers of Silacyclopropane Chem. Phys. Lett. 1980, 76, 163-168
92. Hariharan, P. C.; Pople, J. A. Influence of Polarization Functions on Molecular-Orbital Hydrogenation Energies Theor. Chim. Acta 1973, 28, 213-222
93. Hehre, W. J.; Ditchfield, R.; Pople, J. A. Self-Consistent Molecular-Orbital Methods 0.12. Further Extensions of Gaussian-Type Basis Sets for Use in Molecular-Orbital Studies of Organic-Molecules J. Chem. Phys. 1972, 56, 2257-2261
94. Lee, C. T.; Yang, W. T.; Parr, R. G. Development of the Colle-Salvetti Correlation-Energy Formula into a Functional of the Electron-Density Phys. Rev. B 1988, 37, 785-789
95. Petersson, G. A.; Bennett, A.; Tensfeldt, T. G.; Allaham, M. A.; Shirley, W. A.; Mantzaris, J. A Complete Basis Set Model Chemistry. 1. The Total Energies of Closed-Shell Atoms and Hydrides of the 1st-Row Elements J. Chem. Phys. 1988, 89, 2193-2218
96. Rassolov, V. A.; Pople, J. A.; Ratner, M. A.; Windus, T. L. 6-31g* Basis Set for Atoms K through Zn J. Chem. Phys. 1998, 109, 1223-1229
97. Rassolov, V. A.; Ratner, M. A.; Pople, J. A.; Redfern, P. C.; Curtiss, L. A. 6-31g*Basis Set for Third-Row Atoms J. Comput. Chem. 2001, 22, 976-984
98. Nicholls, A.; Honig, B. A Rapid Finite-Difference Algorithm, Utilizing Successive over-Relaxation to Solve the Poisson-Boltzmann Equation J. Comput. Chem. 1991, 12, 435-445
99. Rocchia, W.; Alexov, E.; Honig, B. Extending the Applicability of the Nonlinear Poisson-Boltzmann Equation: Multiple Dielectric Constants and Multivalent Ions J. Phys. Chem. B 2001, 105, 6507-6514
100. Rocchia, W.; Sridharan, S.; Nicholls, A.; Alexov, E.; Chiabrera, A.; Honig, B. Rapid Grid-Based Construction of the Molecular Surface and the Use of Induced Surface Charge to Calculate Reaction Field Energies: Applications to the Molecular Systems and Geometric Objects J. Comput. Chem. 2002, 23, 128-137
101. Sharp, K. A. Electrostatic Interactions in Macromolecules Curr. Opin. Struct. Biol. 1994, 4, 234-239
102. Frisch, M. J.; Gaussian 09, revision A.1; Gaussian, Inc.: Wallingford, CT, 2009.
103. Huyett, J. E.; Doan, P. E.; Gurbiel, R.; Houseman, A. L. P.; Sivaraja, M.; Goodin, D. B.; Hoffman, B. M. Compound ES of Cytochrome-c Peroxidase Contains a Trp Pi-Cation Radical-Characterization by CW and Pulsed Q-Band ENDOR Spectroscopy J. Am. Chem. Soc. 1995, 117, 9033-9041
104. 8 Bimetallic System J. Am. Chem. Soc. 1997, 119, 5690-5700
105. Warshel, A. Dynamics of Reactions in Polar-Solvents-Semi-Classical Trajectory Studies of Electron-Transfer and Proton-Transfer Reactions J. Phys. Chem. 1982, 86, 2218-2224
106. Hwang, J. K.; Warshel, A. Microscopic Examination of Free-Energy Relationships for Electron-Transfer in Polar-Solvents J. Am. Chem. Soc. 1987, 109, 715-720
107. Churg, A. K.; Warshel, A. Control of the Redox Potential of Cytochrome c and Microscopic Dielectric Effects in Proteins Biochemistry 1986, 25, 1675-1681
108. Warshel, A.; Parson, W. W. Computer-Simulations of Electron-Transfer Reactions in Solution and in Photosynthetic Reaction Centers Annu. Rev. Phys. Chem. 1991, 42, 279-309
109. Muegge, I.; Qi, P. X.; Wand, A. J.; Chu, Z. T.; Warshel, A. The Reorganization Energy of Cytochrome c Revisited J. Phys. Chem. B 1997, 101, 825-836
110. Blumberger, J.; Lamoureux, G. Reorganization Free Energies and Quantum Corrections for a Model Electron Self-Exchange Reaction: Comparison of Polarizable and Non-Polarizable Solvent Models Mol. Phys. 2008, 106, 1597-1611
111. Tipmanee, V.; Oberhofer, H.; Park, M.; Kim, K. S.; Blumberger, J. Prediction of Reorganization Free Energies for Biological Electron Transfer: A Comparative Study of Ru-Modified Cytochromes and a 4-Helix Bundle Protein J. Am. Chem. Soc. 2010, 132, 17032-17040
112. 3+ Self-Exchange Electron Transfer J. Chem. Theory Comput. 2012, 8, 4960-4967
113. Heck, A.; Woiczikowski, P. B.; Kubar, T.; Giese, B.; Elstner, M.; Steinbrecher, T. B. Charge Transfer in Model Peptides: Obtaining Marcus Parameters from Molecular Simulation J. Phys. Chem. B 2012, 116, 2284-2293
114. Mines, G. A.; Bjerrum, M. J.; Hill, M. G.; Casimiro, D. R.; Chang, I. J.; Winkler, J. R.; Gray, H. B. Rates of Heme Oxidation and Reduction in Ru(His33)Cytochrome c at Very High Driving Forces J. Am. Chem. Soc. 1996, 118, 1961-1965
115. Rafferty, S. P.; Pearce, L. L.; Barker, P. D.; Guillemette, J. G.; Kay, C. M.; Smith, M.; Mauk, A. G. Electrochemical, Kinetic, and Circular Dichroic Consequences of Mutations at Position-82 of Yeast Iso-1-Cytochrome c Biochemistry 1990, 29, 9365-9369
116. Ho, P. S.; Sutoris, C.; Liang, N.; Margoliash, E.; Hoffman, B. M. Species Specificity of Long-Range Electron-Transfer within the Complex between Zinc-Substituted Cytochrome c Peroxidase and Cytochrome c J. Am. Chem. Soc. 1985, 107, 1070-1071
117. Venkatramani, R.; Keinan, S.; Balaeff, A.; Beratan, D. N. Nucleic Acid Charge Transfer: Black, White and Gray Coord. Chem. Rev. 2011, 255, 635-648