The medium reorganization energy for the charge transfer reactions in proteins

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1807, Issue 11, 2011, Pages 1444-1456

  Krishtalik, Lev I ^a  

^a FRUMKIN INSTITUTE OF PHYSICAL CHEMISTRY AND ELECTROCHEMISTRY   (Russian Federation)

Author keywords

Azurin; Cytochrome c; Cytochrome c oxidase; Ferredoxin; Interprotein electron transfer; Protein reorganization energy

Indexed keywords

AMICYANIN; AMINE DEHYDROGENASE; AZURIN; CHYMOTRYPSIN A; CYTOCHROME C; CYTOCHROME C OXIDASE; FERREDOXIN; PROTEIN;

ALGORITHM; ARTICLE; ELECTRON TRANSPORT; ENERGY; PRIORITY JOURNAL; PROTEIN REORGANIZATION ENERGY; PROTON TRANSPORT;

ALGORITHMS; ELECTRONS; PROTEINS; PROTONS; THERMODYNAMICS;

EID: 80052769847     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2011.07.002     Document Type: Article

References (107)

1. R.R. Dogonadze, and A.M. Kuznetsov Theory of charge transfer kinetics at solid-polar liquid interfaces Prog. Surf. Sci. 6 1975 1 42
2. J. Ulstrup Lecture Notes in Chemistry 1979 Springer-Verlag Berlin
3. R.R. Dogonadze, and A.M. Kuznetsov Quantum electrochemical kinetics B.E. Conway, Bockris JO'M, E. Yeager, S.U.M. Khan, R.E. White, Comprehensive Treatise of Electrochemistry 7 1983 Plenum Press New York 1 40
4. M.D. Newton, and N. Sutin Electron-transfer reactions in condensed phases Annu. Rev. Phys. Chem. 35 1984 437 480
5. R.A. Marcus, and N. Sutin Electron transfer in chemistry and biology Biochim. Biophys. Acta 811 1985 265 322
6. L.I. Krishtalik Charge Transfer Reactions in Electrochemical and Chemical Processes 1986 Plenum New York
7. A.M. Kuznetsov Charge Transfer in Physics 1995 Chemistry and Biology Physical Mechanisms of Elementary Processes and an Introduction to the Theory, Gordon and Breach, Reading
8. R.A. Marcus Electron transfer reactions in chemistry. Theory and experiment D.S. Bendall, Protein Electron Transfer 1996 BIOS Scientific Publishers Ltd. Oxford 249 272
9. A.M. Kuznetsov, and J. Ulstrup Electron Transfer in Chemistry and Biology 1998 John Wiley and Sons Chichester
10. R.I. Cukier, and D.G. Nocera Proton-coupled electron transfer Annu. Rev. Phys. Chem. 49 1998 337 369 (Pubitemid 128436894)
11. A.M. Kuznetsov Stochastic and Dynamic Views of Chemical Reaction Kinetics in Solutions 1999 Press Polytechniques etUniversitaires Romandes Lausanne
12. L.I. Krishtalik The mechanism of the proton transfer: an outline Biochim. Biophys. Acta. 1458 2000 6 27 (Pubitemid 30254248)
13. L.I. Krishtalik Energetics of multielectron reactions. Photosynthetic oxygen evolution Biochim. Biophys. Acta 849 1986 162 171
14. R.A. Marcus On the theory of oxidation-reduction reactions involving electron transfer. I J. Chem. Phys. 24 1956 966 978
15. L.I. Krishtalik The globule size and activation energy of an enzymatic process Mol. Biol. (Mosc.) 13 1979 577 581
16. L.I. Krishtalik Catalytic acceleration of reactions by enzymes. Effect of screening of a polar medium by a protein globule J. Theor. Biol. 86 1980 757 771
17. L.I. Krishtalik The specific features of enzyme as a polar medium and their role in the mechanism of enzymatic process Molekulyarnaya Biologiya (Mosc.) 8 1974 91 99
18. A. Yadav, R.M. Jackson, J.J. Holbrook, and A. Warshel Role of solvent reorganization energies in the catalytic activity of enzymes J. Am. Chem. Soc. 113 1991 4800 4805
19. I. Muegge, P.X. Qi, A.J. Wand, Z.T. Chu, and A. Warshel The reorganization energy of cytochrome c revisited J. Phys. Chem. B 101 1997 825 836 (Pubitemid 127627952)
20. T. Simonson Gaussian fluctuations and linear response in an electron transfer protein PNAS 99 2002 6544 6549 (Pubitemid 34526169)
21. V. Tipmanee, H. Oberhofer, M. Park, K.S. Kim, and J. Blumberger 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. 132 2010 17032 17040
22. Yu.I. Kharkatz, and L.I. Krishtalik Medium reorganization energy and enzymatic reaction activation energy J. Theor. Biol. 112 1985 221 249 (Pubitemid 15160991)
23. L.I. Krishtalik, and V.V. Topolev Effects of medium polarization and pre-existing field on activation energy of enzymatic charge-transfer reactions Biochim. Biophys. Acta 1459 2000 88 105 (Pubitemid 30484007)
24. L.I. Krishtalik Effective activation energy of enzymatic and nonenzymatic reactions. Evolution imposed requirements to enzyme structure J. Theor. Biol. 112 1985 251 264 (Pubitemid 15160992)
25. L.I. Krishtalik Dynamic and solvation effects of a polar medium in enzymatic charge transfer reactions J. Mol. Catal. 47 1988 211 218
26. K.A. Sharp, and B. Honig Electrostatic interactions in macromolecules: theory and applications Annu. Rev. Biophys. Biophys. Chem. 19 1990 301 332 (Pubitemid 20205627)
27. D. Bashford Electrostatic effects in biological molecules Curr. Opin. Struct. Biol. 1 1991 175 184 (Pubitemid 121002519)
28. M. Gunner, M. Saleh, E. Cross, A. ud-Doula, and M. Wise Backbone dipoles generate positive potentials in all proteins: origins and implications of the effect Biophys. J. 78 2000 1126 1144 (Pubitemid 30141542)
29. P. Voigt, and E.-W. Knapp Tuning heme redox potentials in the cytochrome c subunit of photosynthetic reaction centers J. Biol. Chem. 278 2003 51993 52001 (Pubitemid 38035784)
30. C.N. Schutz, and A. Warshel What are the dielectric "constants" of proteins and how to validate electrostatic models? Proteins Struct. Funct. Genet. 44 2001 400 417 (Pubitemid 32768578)
31. G. King, F. Lee, and A. Warshel Microscopic simulations of macroscopic dielectric constants of solvated proteins J. Chem. Phys. 95 1991 4366 4377
32. L.I. Krishtalik, A.M. Kuznetsov, and E.L. Mertz Electrostatics of proteins: description in terms of two dielectric constants simultaneously Proteins Struct. Funct. Genet. 28 1997 174 182 (Pubitemid 27276304)
33. T. Simonson, G. Archontis, and M. Karplus A Poisson-Boltzmann study of charge insertion in an enzyme active site: the effect of dielectric relaxation J. Phys. Chem. B 103 1999 6142 6156 (Pubitemid 129616291)
34. L.I. Krishtalik Continuum electrostatics of proteins. Experimental test with model solvents and the method of the proteins pK calculations Chem. Phys. 319 2005 316 329 (Pubitemid 41750498)
35. V.V. Ptushenko, D.A. Cherepanov, L.I. Krishtalik, and A.Yu. Semenov Semi-continuum electrostatic calculations of redox potentials in photosystem I Photosynth. Res. 97 2008 55 74
36. A.M. Kuznetsov, E.M. Zueva, A.N. Masliy, and L.I. Krishtalik Redox potential of the Rieske iron-sulfur protein. Quantum-chemical and electrostatic study Biochim. Biophys. Acta 1797 2010 347 359
37. R.A. Marcus Free energy of nonequilibrium polarization systems. 4. A formalism based on the nonequilibrium dielectric displacement J. Phys. Chem. 98 1994 7170 7174
38. L.I. Krishtalik Fast electron transfers in photosynthetic reaction centre: effect of the time-evolution of dielectric response Biochim. Biophys. Acta 1228 1995 58 66
39. L.I. Krishtalik Intramembrane electron transfer: processes in photosynthetic reaction center Biochim. Biophys. Acta 1273 1996 139 149 (Pubitemid 26071258)
40. E.L. Mertz, E.D. German, and A.M. Kuznetsov Calculation of the solvent reorganization free energy in the dielectric cavity model Chem. Phys. 215 1997 355 370
41. A. Nicholls, and B. Honig A rapid finite-difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation J. Comput. Chem. 12 1991 435 445
42. M.K. Gilson, and B.H. Honig The dielectric constant of a folded protein Biopolymers 25 1986 2097 2119
43. H. Nakamura, T. Sakamoto, and A. Wada A theoretical study of the dielectric constant of protein Protein Eng. 2 1988 177 181
44. T. Simonson, D. Perahia, and G. Bricogne Intramolecular dielectric screening in proteins J. Mol. Biol. 218 1991 859 886 (Pubitemid 121003382)
45. T. Simonson, D. Perahia, and A.T. Brünger Microscopic theory of the dielectric properties of proteins Biophys. J. 59 1991 670 690
46. P.E. Smith, R.M. Brunne, A.E. Mark, and W.F. van Gunsteren Dielectric properties of trypsin inhibitor and lysozyme calculated from molecular dynamics simulations J. Phys. Chem. 97 1993 2009 2014
47. T. Simonson, and D. Perahia Microscopic dielectric properties of cytochrome c from molecular dynamics simulations in aqueous solution J. Am. Chem. Soc. 117 1995 7987 8000
48. E.L. Mertz, and L.I. Krishtalik Low dielectric response in enzyme active site Proc. Natl. Acad. Sci. U.S.A. 97 2000 2081 2086 (Pubitemid 30134025)
49. G.M. Ullmann The coupling of protonation and reduction in proteins with multiple redox centers: theory, computational method, and application to cytochrome c J. Phys. Chem. B 104 2000 6293 6301
50. L.I. Krishtalik, G.-S. Tae, D.A. Cherepanov, and W.A. Cramer The redox properties of cytochromes b imposed by the membrane electrostatic environment Biophys. J. 65 1993 184 195 (Pubitemid 23206052)
51. G.M. Soriano, W.A. Cramer, and L.I. Krishtalik Electrostatic effects on electron-transfer kinetics in the cytochrome f-plastocyanin complex Biophys. J. 73 1997 3265 3276 (Pubitemid 27525789)
52. H.X. Zhou Effects of mutations and complex formation on the reduction potentials of cytochrome c and cytochrome c peroxidase J. Am. Chem. Soc. 116 1994 10362 10378
53. Yu.I. Kharkats, and J. Ulstrup Dielectric image effects in environmental reorganization free energies and inter-reactant work terms of metalloprotein electron transfer reactions Chem. Phys. 141 1990 117 129
54. Y.-P. Liu, and M.D. Newton Reorganization energy for electron transfer at film-modified electrode surfaces: a dielectric continuum model J. Phys. Chem. 98 1994 7162 7169
55. S. Terrettaz, J. Cheng, C.J. Miller, and R.D. Guiles Kinetic parameters for cytochrome c via insulated electrode voltammetry J. Am. Chem. Soc. 118 1996 7857 7858 (Pubitemid 26285145)
56. J.I. Blankman, N. Shahzad, B. Dangi, C.J. Miller, and R.D. Guiles Voltammetric probes of cytochrome electroreactivity: the effect of the protein matrix on outer-sphere reorganization energy and electronic coupling probed through comparisons with the behavior of porphyrin complexes Biochemistry 39 2000 14799 14805
57. L.A. Khanova, and L.I. Krishtalik Long-range electron transfer: what is rate-determining - the geometric distance or the pathway? Electrochim. Acta 50 2005 1085 1099
58. K. Niki, W.R. Hardy, M.G. Hill, H. Li, J.R. Sprinkle, E. Margoliash, K. Fujita, R. Tanimura, N. Nakamura, H. Ohno, J.H. Richards, and H.B. Gray Coupling to Lysine-13 promotes electron tunneling through carboxylate-terminated alkanethiol self-assembled monolayers to cytochrome c J. Phys. Chem. B 107 2003 9947 9949
59. E. Sigfridsson, M.H.M. Olsson, and U. Ryde A comparison of the inner-sphere reorganization energies of cytochromes, iron-sulfur clusters, and blue copper proteins J. Phys. Chem. B 105 2001 5546 5552 (Pubitemid 35372599)
60. A.M. Berghuis, and G.D. Brayer Oxidation state-dependent conformational changes in cytochrome c J. Mol. Biol. 223 1992 959 976
61. A.M. Berghuis, J.G. Guillemette, G. McLendon, F. Sherman, M. Smith, and G.D. Brayer The role of a conserved internal water molecule and its associated hydrogen bond network in cytochrome c J. Mol. Biol. 236 1994 786 799
62. P.X. Qi, R.A. Beckman, and A.J. Wand Solution structure of horse heart ferricytochrome c and detection of redox-related structural changes by high-resolution 1H NMR Biochemistry 35 1996 12275 12286 (Pubitemid 26331249)
63. I. Bertini, C. Dalvit, J.G. Huber, C. Luchinat, and M. Piccioli ePHOGSY experiments on a paramagnetic protein: location of the catalytic water molecule in the heme crevice of the oxidized form of horse heart cytochrome c FEBS Lett. 415 1997 45 48 (Pubitemid 27402046)
64. I. Bertini, J.G. Huber, C. Luchinat, and M. Piccioli Protein hydration and location of water molecules in oxidized horse heart cytochrome c by 1H NMR J. Magn. Reson. 147 2000 1 8
65. A.K. Churg, R.M. Welss, A. Warshel, and T. Takano On the action of cytochrome c: correlating geometry changes upon oxidation with energies of electron transfer J. Phys. Chem. 87 1983 1683 1694
66. H.B. Gray, and J.R. Winkler Electron transfer in proteins Annu. Rev. Biochem. 65 1996 537 561 (Pubitemid 26250619)
67. H.B. Gray, and J.R. Winkler Electron tunneling through proteins Q. Rev. Biophys. 36 2003 341 372 (Pubitemid 38268661)
68. T.J. Meade, H.B. Gray, and J.R. Winkler Driving-force effects on the rate of long-range electron transfer in ruthenium-modified cytochrome c J. Am. Chem. Soc. 111 1989 4353 4356
69. 4] Inorg. Chem. 10 1971 2304 2308
70. M. Maruyama, and Y. Kaizu Role of the inner-sphere reorganization in the photoinduced electron transfer reaction of Ru(I1) complexes containing imine C N or Azo NN double bonds in the ligands J. Phys. Chem. 99 1995 6152 6162
71. X. Amashukeli, N.E. Gruhn, D.L. Lichtenberger, J.Y.R. Winkler, and H.B. Gray Inner-sphere electron-transfer reorganization energies of zinc porphyrins J. Am. Chem. Soc. 126 2004 15566 15571 (Pubitemid 39577493)
72. G.A. Mines, M.J. Bjerrum, M.G. Hill, D.R. Casimiro, I.-J. Chang, J.R. Winkler, and H.B. Gray Rates of heme oxidation and reduction in Ru(His33)cytochrome c at very high driving forces J. Am. Chem. Soc. 118 1996 1961 1965 (Pubitemid 26100205)
73. O. Farver, and I. Pecht Blue copper proteins as a model for investigating electron transfer processes within polypeptide matrices Biophys. Chem. 50 1994 203 216 (Pubitemid 24130964)
74. M.H.M. Olsson, U. Ryde, and B.O. Roos Quantum chemical calculations of the reorganization energy of blue-copper proteins Protein Sci. 7 1998 2659 2668 (Pubitemid 28565708)
75. D.R. Gamelin, D.W. Randall, M.T. Hay, R.P. Houser, T.C. Mulder, G.W. Canters, S. de Vries, W.B. Tolman, Yi Lu, and E.I. Solomon Spectroscopy of mixed-valence CuA-type centers: ligand-field. Control of ground-state properties related to electron transfer J. Am. Chem. Soc. 120 1998 5246 5263 (Pubitemid 28328888)
76. R. Kümmerle, J. Gaillard, P. Kyritsis, and J.-M. Moulis Intramolecular electron transfer in [4Fe - 4S] proteins: estimates of the reorganization energy and electronic coupling in Chromatium vinosum ferredoxin J. Biol. Inorg. Chem. 6 2001 446 451 (Pubitemid 32822135)
77. R.A. Torres, T. Lovell, L. Noodleman, and D.A. Case Density functional and reduction potential calculations of Fe4S4 clusters J. Am. Chem. Soc. 125 2003 1923 1936 (Pubitemid 36236149)
78. E. Sigfridsson, M.H.M. Olsson, and U. Ryde Inner-sphere reorganization energy of iron-sulfur clusters studied with theoretical methods Inorg. Chem. 40 2001 2509 2519 (Pubitemid 32880557)
79. C.H. Chang, and K. Kim Density functional theory calculation of bonding and charge parameters for molecular dynamics studies on [FeFe] hydrogenases J. Chem. Theory Comput. 5 2009 1137 1145
80. Y. Jia, T.J. DiMagno, C.-K. Chan, Z. Wang, M. Du, D.K. Hanson, M. Schiffer, J.R. Norris, G.R. Fleming, and M.S. Popov Primary charge separation in mutant reaction centers of Rhodobacter capsulatus J. Phys. Chem. 97 1993 13180 13191
81. Z. Wang, R.M. Pearlstein, Y. Jia, G.R. Fleming, and J.R. Norris Inhomogeneous electron transfer kinetics in reaction centers of bacterial photosynthesis Chem. Phys. 176 1993 421 425
82. L.I. Krishtalik Activationless electron transfer in the reaction centre of photosynthesis Biochim. Biophys. Acta 977 1989 200 206
83. S.M. Dracheva, L.A. Drachev, A.A. Konstantinov, A.Y. Semenov, V.P. Skulachev, A.M. Arutjunjan, V.A. Shuvalov, and S.M. Zaberezhnaya Electrogenic steps in the redox reactions catalyzed by photosynthetic reaction-center complex from Rhodopseudomonas-viridis Eur J. Biochem. 174 1988 253 264
84. M.H. Vos, C. Rischel, M.R. Jones, and J.-L. Martin Electrochromic detection of a coherent component in the formation of the charge pair P+ HL- in bacterial reaction centers Biochemistry 39 2000 8353 8361 (Pubitemid 30489932)
85. V.A. Shuvalov, and A.G. Yakovlev Coupling of nuclear wavepacket motion and charge separation in bacterial reaction centers FEBS Lett. 540 2003 26 34 (Pubitemid 36398028)
86. A. Jasaitis, F. Rappaport, E. Pilet, U. Liebl, and M.H. Vos Activationless electron transfer through the hydrophobic core of cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 102 2005 10882 10886 (Pubitemid 41105961)
87. V.R.I. Kailaa, M.P. Johansson, D. Sundholm, and M. Wikström Interheme electron tunneling in cytochrome c oxidase Proc. Natl. Acad. Sci. U.S.A. 107 2010 21470 21475
88. B.E. Ramirez, B.G. Malmstrom, J.R. Winkler, and H.B. Gray The currents of life: the terminal electron-transfer complex of respiration Proc. Natl. Acad. Sci. U.S.A. 92 1995 11949 11951 (Pubitemid 26013987)
89. P. Brzezinski Internal electron-transfer reactions in cytochrome c oxidase Biochemistry 35 1996 5611 5615 (Pubitemid 26143655)
90. M.H.M. Olsson, and U. Ryde Geometry, reduction potential, and reorganization energy of the binuclear CuA site, studied by density functional theory J. Am. Chem. Soc. 123 2001 7866 7876 (Pubitemid 32899351)
91. D.R. Gamelin, D.W. Randall, M.T. Hay, R.P. Houser, T.C. Mulder, G.W. Canters, S. de Vries, W.B. Tolman, Yi Lu, and E.I. Solomon Spectroscopy of mixed-valence CuA-type centers: ligand-field control of ground-state properties related to electron transfer J. Am. Chem. Soc. 120 1998 5246 5263 (Pubitemid 28328888)
92. G. McLendon, and R. Hake Interprotein electron transfer Chem. Rev. 92 1992 481 490
93. S.J. Takayama, K. Irie, H. Tai, T. Kawahara, S. Hirota, T. Takabe, L.A. Alcaraz, A. Donaire, and Y. Yamamoto Electron transfer from cytochrome c to cupredoxins J. Biol. Inorg. Chem. 14 2009 821 828
94. V.L. Davidson Electron transfer in quinoproteins Arch. Biochem. Biophys. 428 2004 32 40 (Pubitemid 38844907)
95. G. Soriano, W.A. Cramer, and L.I. Krishtalik Electrostatic effects on electron-transfer kinetics in the cytochrome f-plastocyanin complex Biophys. J. 73 1997 3265 3276 (Pubitemid 27525789)
96. A.A. Kossiakoff, and S.A. Spencer Direct determination of the protonation states of aspartic acid-102 and histidine-57 in the tetrahedral intermediate of the serine proteases: neutron structure of trypsin Biochemistry 20 1981 6462 6474
97. J.P. Elrod, J.L. Hogg, D.M. Quinn, K.S. Venkatasubban, and R.L. Schowen Protonic reorganization and substrate structure in catalysis by serine proteases J. Am. Chem. Soc. 102 1980 3917 3922
98. M. Fujinaga, A.R. Sielecki, R.J. Read, W. Ardelt, M. Laskowski Jr., and M.N.G. James Crystal and molecular structures of the complex of α-chymotrypsin with its inhibitor Turkey ovomucoid third domain at 1.8 Å resolution J. Mol. Biol. 195 1987 397 418 (Pubitemid 17106696)
99. M. Strajbl, J. Florian, and A. Warshel Ab initio evaluation of the potential surface for general base-catalyzed methanolysis of formamide: a reference solution reaction for studies of serine proteases J. Am. Chem. Soc. 122 2000 5354 5366 (Pubitemid 30395267)
100. D.E. Khoshtariya, V.V. Topolev, and L.I. Krishtalik Investigation of the proton transfer in enzymatic-hydrolysis by the method of the kinetic isotope effect temperature-dependence. 1. Alpha-chymotrypsin catalyzed hydrolysis of N-acetyl and N-benzoyl-l-tyrosine ethyl esters Bioorg. Khim. 4 1978 1341 1351
101. D.E. Khoshtariya Investigation of the proton transfer in enzymatic-hydrolysis by the method of the kinetic isotope effect temperature-dependence. 2. Beta-trypsin catalyzed-hydrolysis of Bz-Arg-Oet Bioorg. Khim. 4 1978 1673 1677
102. D.E. Khoshtariya, V.V. Topolev, L.I. Krishtalik, I.L. Reyzer, and V.P. Torchilin Investigation of the proton-transfer in enzymatic-hydrolysis by the method of kinetic isotope effect temperature-dependence.3. Hydrolysis of n-acetyl-l-tyrosine and n-benzoyl-l-tyrosine ethyl-esters by alpha-chymotrypsin immobilized on soluble dextran Bioorg. Khim. 5 1979 1243 1247
103. M.H.M. Olsson, W.W. Parson, and A. Warshel Dynamical contributions to enzyme catalysis: critical tests of a popular hypothesis Chem. Rev. 106 2006 1737 1756 (Pubitemid 43792778)
104. D.E. Khoshtariya, and L.I. Krishtalik Mechanism of the elementary event in the formation and decomposition of the tetrahedral adduct in the hydrolysis of esters Bull. Acad. Sci. USSR Div. Chem. Sci. 33 1984 1579 1585
105. A. Warshel, F. Sussman, and J.-K. Hwang Evaluation of catalytic free energies in genetically modified proteins J. Mol. Biol. 201 1988 139 159
106. A. Warshel, G. Naray-Szabo, F. Sussman, and J.-K. Hwang How do serine proteases really work? Biochemistry 28 1989 3629 3637 (Pubitemid 19125405)
107. A. Shurki, and A. Warshel Structure/function correlations of proteins using MM, QM/MM, and related approaches: methods, concepts, pitfalls, and current progress Adv. Protein Chem. 66 2003 249 313 (Pubitemid 37392318)