Design and fine-tuning redox potentials of metalloproteins involved in electron transfer in bioenergetics

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1857, Issue 5, 2016, Pages 557-581

  Hosseinzadeh, Parisa ^a   Lu, Yi ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cupredoxin; Cytochromes; Iron sulfur proteins; Metalloenzymes; Non covalent interactions; Secondary coordination sphere

Indexed keywords

AMINO ACID; AZURIN; COPPER PROTEIN; CUPREDOXIN; CYTOCHROME; CYTOCHROME C PEROXIDASE; HEME; HEME B; HEMOPROTEIN; IRON SULFUR PROTEIN; IRON SUPEROXIDE DISMUTASE; LIGAND; MANGANESE IRON SUPEROXIDE DISMUTASE; MANGANESE SUPEROXIDE DISMUTASE; METAL ION; METALLOPROTEIN; MYOGLOBIN; PROTEIN KINASE FES; SOLVENT; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; MULTIENZYME COMPLEX;

ARTICLE; BIOENERGY; ELECTRON TRANSPORT; HYDROGEN BOND; HYDROPHOBICITY; LIGAND BINDING; MITOCHONDRIAL RESPIRATION; OXIDATION REDUCTION POTENTIAL; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; SURFACE CHARGE; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; ENERGY METABOLISM; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; OXIDATION REDUCTION REACTION; PROCEDURES;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; ELECTRON TRANSPORT; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENERGY METABOLISM; HUMANS; METALLOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEIN ENGINEERING;

EID: 84941661864     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.08.006     Document Type: Article

References (312)

1. O. Farver, and I. Pecht Electron transfer processes of blue copper proteins Met. Ions Biol. Syst. 3 1981 151 192
2. T.H. Stevens, C.T. Martin, H. Wang, G.W. Brudvig, C.P. Scholes, and S.I. Chan The nature of copperA in cytochrome c oxidase J. Biol. Chem. 257 1982 12106 12113
3. C. Dennison, and G.W. Canters The CuA site of cytochrome c oxidase Recl. Trav. Chim. Pays-Bas 115 1996 345 351
4. G. Battistuzzi, M. Borsari, L. Loschi, F. Righi, and M. Sola Redox thermodynamics of blue copper proteins J. Am. Chem. Soc. 121 1999 501 506
5. F. De Rienzo, R.R. Gabdoulline, M.C. Menziani, and R.C. Wade Blue copper proteins: a comparative analysis of their molecular interaction properties Protein Sci. 9 2000 1439 1454
6. H.B. Gray, B.G. Malmstrom, and R.J. Williams Copper coordination in blue proteins J. Biol. Inorg. Chem. 5 2000 551 559
7. Y. Lu Electron transfer: cupredoxins J.L. Que, W.B. Tolman, Biocoordination Chemistry 2004 Elsevier Oxford, UK 91 122
8. D.B. Rorabacher Electron transfer by copper centers Chem. Rev. 104 2004 651 698
9. T.D. Wilson, Y. Yu, and Y. Lu Understanding copper-thiolate containing electron transfer centers by incorporation of unnatural amino acids and the CuA center into the type 1 copper protein azurin Coord. Chem. Rev. 257 2012 260 276
10. J. Liu, S. Chakraborty, P. Hosseinzadeh, Y. Yu, S. Tian, I. Petrik, A. Bhagi, and Y. Lu Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers Chem. Rev. 114 2014 4366 4469
11. D. Keilin, and E.F. Hartree Cytochrome and cytochrome oxidase Proc. R. Soc. London, Ser. B 127 1939 167 191
12. R. Lember, and J. Barrett Cytochromes 1973 Academic Press London
13. G. Vonjagow, and W. Sebald B-type cytochromes Annu. Rev. Biochem. 49 1980 281 314
14. T.E. Meyer, and M.D. Kamen New perspectives on C-type cytochromes Adv. Protein Chem. 35 1982 105 212
15. G.W. Pettigrew, and G.R. Moore Cytochromes C: Biological Aspects 1987 Springer Berlin
16. I.B. Coutinho, and A.V. Xavier Tetraheme cytochromes Methods Enzymol. 243 1994 119 140
17. K.R. Rodgers, and G.S. Lukat-Rodgers Electron transfer cytochromes J. McCleverty, T.J. Meyer, Comprehensive Coordination Chemistry II 2004 Pergamon Oxford 17 60
18. J.C.M. Tsibris, and R.W. Woody Structural studies of iron-sulfur proteins Coord. Chem. Rev. 5 1970 417 458
19. H. Beinert, R.H. Holm, and E. Munck Iron-sulfur clusters: nature's modular, multipurpose structures Science 277 1997 653 659
20. H. Sticht, and P. Rosch The structure of iron-sulfur proteins Prog. Biophys. Mol. Biol. 70 1998 95 136
21. B.N. Anand Iron sulfur proteins and their synthetic analogs: structure, reactivity and redox properties Resonance 3 1998 52 61
22. R. Kummerle, P. Kyritsis, J. Gaillard, and J.-M. Moulis Electron transfer properties of iron-sulfur proteins J. Inorg. Biochem. 79 2000 83 91
23. J. Meyer Iron-sulfur protein folds, iron-sulfur chemistry, and evolution J. Biol. Inorg. Chem. 13 2008 157 170
24. R. Lill Function and biogenesis of iron-sulfur proteins Nature 460 2009 831 838
25. P. Zanello Inorganic electrochemistry: theory, practice and application 2013 Royal Society of Chemistry, Padstow Cornwall, UK
26. R.A. Marcus Electron-transfer reactions in chemistry: theory and experiment (Nobel lecture) Angew. Chem. 105 1993 1161 1172 (See also, Angew. Chem., Int. Ed. Engl., 1993, 1132(1168), 1111-1121)
27. D. Noy, C.C. Moser, and P.L. Dutton Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales Biochim. Biophys. Acta 1757 2006 90 105
28. M.D. Kärkäs, O. Verho, E.V. Johnston, and B. Akermark Artificial photosynthesis: molecular systems for catalytic water oxidation Chem. Rev. 114 2014 11863 12001
29. N. Nelson, and A. Ben-Shem The complex architecture of oxygenic photosynthesis Nat. Rev. Mol. Cell Biol. 5 2004 971 982
30. J. Barber, and P.D. Tran From natural to artificial photosynthesis J. R. Soc. Interface 10 2013 20120984
31. C.C. Moser, and P.L. Dutton Engineering protein structure for electron transfer function in photosynthetic reaction centers Biochim. Biophys. Acta 1101 1992 171 176
32. R.E. Blankenship Origin and early evolution of photosynthesis Photosynth. Res. 33 1992 91 111
33. C.A. Wraight Chance and design - proton transfer in water, channels and bioenergetic proteins Biochim. Biophys. Acta 1757 2006 886 912
34. G. Lenaz, and M.L. Genova Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject Antioxid. Redox Signal. 12 2010 961 1008
35. H.J. Kim, O. Khalimonchuk, P.M. Smith, and D.R. Winge Structure, function, and assembly of heme centers in mitochondrial respiratory complexes Biochim. Biophys. Acta 1823 2012 1604 1616
36. M.R. Gunner, M. Amin, X. Zhu, and J. Lu Molecular mechanisms for generating transmembrane proton gradients Biochim. Biophys. Acta 1827 2013 892 913
37. S. Yoshikawa, and A. Shimada Reaction mechanism of cytochrome c oxidase Chem. Rev. 115 2015 1936 1989
38. R.I. Murray, M.T. Fisher, P.G. Debrunner, and S.G. Sligar Structure and chemistry of cytochrome P-450 Top. Mol. Struct. Biol. 6 1985 157 206
39. S.G. Sligar Nature's universal oxygenases: the cytochromes P450 Essays Biochem. 34 1999 71 83
40. M.J. Coon Cytochrome P450: nature's most versatile biological catalyst Annu. Rev. Pharmacol. Toxicol. 45 2005 1 25
41. I.G. Denisov, T.M. Makris, S.G. Sligar, and I. Schlichting Structure and chemistry of cytochrome P 450 Chem. Rev. 105 2005 2253 2277
42. M.A. Schuler, and S.G. Sligar Diversities and similarities in P450 systems: an introduction Met. Ions Life Sci. 3 2007 1 26
43. I.G. Denisov, and S.G. Sligar Cytochrome P450 enzymes K.M. Kadish, K.M. Smith, R. Guilard, Handbook of Porphyrin Science 2010 World Scientific Publishing Co. Pte. Ltd 165 201
44. S.T. Jung, R. Lauchli, and F.H. Arnold Cytochrome P 450: taming a wild type enzyme Curr. Opin. Biotechnol. 22 2011 809 817
45. T.L. Poulos Heme enzyme structure and function Chem. Rev. 114 2014 3919 3962
46. T.A. Link The role of the 'Rieske' iron sulfur protein in the hydroquinone oxidation (Q(P)) site of the cytochrome bc1 complex. The 'proton-gated affinity change' mechanism FEBS Lett. 412 1997 257 264
47. T.A. Link The Structures of Rieske and Rieske-Type Proteins A.G. Sykes, Adv. Inorg. Chem. 1999 Academic Press 83 157
48. K.L. Hsueh, M. Tonelli, K. Cai, W.M. Westler, and J.L. Markley Electron transfer mechanism of the Rieske protein from Thermus thermophilus from solution nuclear magnetic resonance investigations Biochemistry 52 2013 2862 2873
49. P. De, R. Antonio, I. Jelesarov, F. Ackermann, W.H. Koppenol, M. Hirasawa, D.B. Knaff, and H.R. Bosshard Binding of ferredoxin to ferredoxin:NADP + oxidoreductase: the role of carboxyl groups, electrostatic surface potential, and molecular dipole moment Protein Sci. 2 1993 1126 1135
50. T. Hase, P. Schurmann, and D.B. Knaff The interaction of ferredoxin with ferredoxin-dependent enzymes Adv. Photosynth. Respir. 24 2006 477 498
51. Y. Lu, N. Yeung, N. Sieracki, and N.M. Marshall Design of functional metalloproteins Nature 460 2009 855 862
52. Y. Lu, S. Chakraborty, K.D. Miner, T.D. Wilson, A. Mukherjee, Y. Yu, J. Liu, and N.M. Marshall 3.19 - metalloprotein design J.R. Poeppelmeier, Comprehensive Inorganic Chemistry II Second Edition 2013 Elsevier Amsterdam 565 593
53. N.M. Marshall, K.D. Miner, T.D. Wilson, and Y. Lu Rational design of protein cages for alternative enzymatic functions Coordination Chemistry in Protein Cages 2013 John Wiley & Sons, Inc. 111 147
54. F. Yu, V.M. Cangelosi, M.L. Zastrow, M. Tegoni, J.S. Plegaria, A.G. Tebo, C.S. Mocny, L. Ruckthong, H. Qayyum, and V.L. Pecoraro Protein design: toward functional metalloenzymes Chem. Rev. 114 2014 3495 3578
55. S. Chakraborty, P. Hosseinzadeh, and Y. Lu Metalloprotein Design and Engineering, in: Encyclopedia of Inorganic and Bioinorganic Chemistry 2014 John Wiley & Sons Ltd
56. W. Maret, H. Dietrich, H.H. Ruf, and M. Zeppezauer Active site-specific reconstituted copper(II) horse liver alcohol dehydrogenase: a biological model for type 1 Cu2 + and its changes upon ligand binding and conformational transitions J. Inorg. Biochem. 12 1980 241 252
57. W. Maret, M. Zeppezauer, A. Desideri, L. Morpurgo, and G. Rotilio Ligand binding to the blue copper center of horse liver alcohol dehydrogenase FEBS Lett. 136 1981 72 74
58. W. Maret, A.K. Shiemke, W.D. Wheeler, T.M. Loehr, and J. Sanders-Loehr Resonance Raman spectroscopy of blue copper proteins: ligand and coenzyme effects in copper(II)-substituted liver alcohol dehydrogenase J. Am. Chem. Soc. 108 1986 6351 6359
59. W. Maret, and H. Kozlowski Electronic absorption and EPR spectroscopy of copper alcohol dehydrogenase: pink, violet and green forms of a type 1 copper center analog Biochim. Biophys. Acta 912 1987 329 337
60. M.L. Brader, and M.F. Dunn Insulin stabilizes copper(II)-thiolate ligation that models blue copper proteins J. Am. Chem. Soc. 112 1990 4585 4587
61. M.L. Brader, D. Borchardt, and M.F. Dunn Ligand effects on the blue copper site. Spectroscopic studies of an insulin-stabilized copper(II) chromophore incorporating an exogenous thiolate ligand J. Am. Chem. Soc. 114 1992 4480 4486
62. M.L. Brader, D. Borchardt, and M.F. Dunn The T to R transition in the copper(II)-substituted insulin hexamer. Anion complexes of the R-state species exhibiting type 1 and type 2 spectral characteristics Biochemistry 31 1992 4691 4696
63. D. Shiga, D. Nakane, T. Inomata, Y. Funahashi, H. Masuda, A. Kikuchi, M. Oda, M. Noda, S. Uchiyama, K. Fukui, K. Kanaori, K. Tajima, Y. Takano, H. Nakamura, and T. Tanaka Creation of a type 1 blue copper site within a de novo coiled-coil protein scaffold J. Am. Chem. Soc. 132 2010 18191 18198
64. Y. Lu, E.B. Gralla, J.A. Roe, and J.S. Valentine The redesign of a type 2 into a type 1 copper protein: construction and characterization of yeast copper, zinc superoxide dismutase mutants J. Am. Chem. Soc. 114 1992 3560 3562
65. Y. Lu, J. Roe, E. Gralla, and J. Valentine Metalloprotein ligand redesign: characterization of copper-cysteinate proteins derived from yeast copper-zinc superoxide dismutase K. Karlin, Z. Tyeklár, Bioinorganic Chemistry of Copper 1993 Springer Netherlands 64 77
66. Y. Lu, J.A. Roe, C.J. Bender, J. Peisach, L. Banci, I. Bertini, E.B. Gralla, and J.S. Valentine New type 2 copper-cysteinate proteins. Copper site histidine-to-cysteine mutants of yeast copper-zinc superoxide dismutase Inorg. Chem. 35 1996 1692 1700
67. Y. Lu, L.B. LaCroix, M.D. Lowery, E.I. Solomon, C.J. Bender, J. Peisach, J.A. Roe, E.B. Gralla, and J.S. Valentine Construction of a blue copper site at the native zinc site of yeast copper-zinc superoxide dismutase J. Am. Chem. Soc. 115 1993 5907 5918
68. K.M. Clark, Y. Yu, N.M. Marshall, N.A. Sieracki, M.J. Nilges, N.J. Blackburn, W.A. van der Donk, and Y. Lu Transforming a blue copper into a red copper protein: engineering cysteine and homocysteine into the axial position of azurin using site-directed mutagenesis and expressed protein ligation J. Am. Chem. Soc. 132 2010 10093 10101
69. K.M. Clark, Y. Yu, W.A. van der Donk, N. Blackburn, and Y. Lu Modulating the copper-sulfur interaction in type 1 blue copper azurin by replacing Cys112 with nonproteinogenic homocysteine Inorg. Chem. Front. 1 2014 153 158
70. H. Robinson, M.C. Ang, Y.G. Gao, M.T. Hay, Y. Lu, and A.H. Wang Structural basis of electron transfer modulation in the purple CuA center Biochemistry 38 1999 5677 5683
71. A center in purple azurin: impact of the mixed valence-to-trapped valence state transition J. Phys. Chem. B 111 2007 6690 6694
72. X. Xie, S.I. Gorelsky, R. Sarangi, D.K. Garner, H.J. Hwang, K.O. Hodgson, B. Hedman, Y. Lu, and E.I. Solomon Perturbations to the geometric and electronic structure of the CuA site: factors that influence delocalization and their contributions to electron transfer J. Am. Chem. Soc. 130 2008 5194 5205
73. T.D. Wilson, M.G. Savelieff, M.J. Nilges, N.M. Marshall, and Y. Lu Kinetics of copper incorporation into a biosynthetic purple Cu(A) azurin: characterization of red, blue, and a new intermediate species J. Am. Chem. Soc. 133 2011 20778 20792
74. M.T. Hay, M.C. Ang, D.R. Gamelin, E.I. Solomon, W.E. Antholine, M. Ralle, N.J. Blackburn, P.D. Massey, X. Wang, A.H. Kwon, and Y. Lu Spectroscopic characterization of an engineered purple CuA center in Azurin Inorg. Chem. 37 1998 191 198
75. C. Dennison, E. Vijgenboom, S. de Vries, J. van der Oost, and G.W. Canters Introduction of a CuA site into the blue copper protein amicyanin from Thiobacillus versutus FEBS Lett. 365 1995 92 94
76. M. Hay, J.H. Richards, and Y. Lu Construction and characterization of an azurin analog for the purple copper site in cytochrome c oxidase Proc. Natl. Acad. Sci. U. S. A. 93 1996 461 464
77. D. Shiga, Y. Funahashi, H. Masuda, A. Kikuchi, M. Noda, S. Uchiyama, K. Fukui, K. Kanaori, K. Tajima, Y. Takano, H. Nakamura, M. Kamei, and T. Tanaka Creation of a binuclear purple copper site within a de novo coiled-coil protein Biochemistry 51 2012 7901 7907
78. D.E. Robertson, R.S. Farid, C.C. Moser, J.L. Urbauer, S.E. Mulholland, R. Pidikiti, J.D. Lear, A.J. Wand, W.F. DeGrado, and P.L. Dutton Design and synthesis of multi-haem proteins Nature 368 1994 425 432
79. W.A. Kalsbeck, D.E. Robertson, R.K. Pandey, K.M. Smith, P.L. Dutton, and D.F. Bocian Structural and electronic properties of the heme cofactors in a multi-heme synthetic cytochrome Biochemistry 35 1996 3429 3438
80. B.R. Gibney, Y. Isogai, F. Rabanal, K.S. Reddy, A.M. Grosset, C.C. Moser, and P.L. Dutton Self-assembly of heme a and heme b in a designed four-helix bundle: implications for a cytochrome c oxidase maquette Biochemistry 39 2000 11041 11049
81. J.M. Shifman, B.R. Gibney, R.E. Sharp, and P.L. Dutton Heme redox potential control in de novo designed four-alpha-helix bundle proteins Biochemistry 39 2000 14813 14821
82. M. Ishida, N. Dohmae, Y. Shiro, T. Oku, T. Iizuka, and Y. Isogai Design and synthesis of de novo cytochromes c Biochemistry 43 2004 9823 9833
83. J.L. Anderson, C.T. Armstrong, G. Kodali, B.R. Lichtenstein, D.W. Watkins, J.A. Mancini, A.L. Boyle, T.A. Farid, M.P. Crump, C.C. Moser, and P.L. Dutton Constructing a man-made c-type cytochrome maquette: electron transfer, oxygen transport and conversion to a photoactive light harvesting maquette Chem. Sci. 5 2014 507 514
84. S.S. Huang, R.L. Koder, M. Lewis, A.J. Wand, and P.L. Dutton The HP-1 maquette: from an apoprotein structure to a structured hemoprotein designed to promote redox-coupled proton exchange Proc. Natl. Acad. Sci. U. S. A. 101 2004 5536 5541
85. B.M. Discher, D. Noy, J. Strzalka, S. Ye, C.C. Moser, J.D. Lear, J.K. Blasie, and P.L. Dutton Design of amphiphilic protein maquettes: controlling assembly, membrane insertion, and cofactor interactions Biochemistry 44 2005 12329 12343
86. A.R. Reddi, C.J. Reedy, S. Mui, and B.R. Gibney Thermodynamic investigation into the mechanisms of proton-coupled electron transfer events in heme protein maquettes Biochemistry 46 2007 291 305
87. X. Jiang, H. Farid, E. Pistor, and R.S. Farid A new approach to the design of uniquely folded thermally stable proteins Protein Sci. 9 2000 403 416
88. Z. Xu, and R.S. Farid Design, synthesis, and characterization of a novel hemoprotein Protein Sci. 10 2001 236 249
89. Y. Isogai, M. Ota, T. Fujisawa, H. Izuno, M. Mukai, H. Nakamura, T. Iizuka, and K. Nishikawa Design and synthesis of a globin fold Biochemistry 38 1999 7431 7443
90. Y. Isogai, A. Ishii, T. Fujisawa, M. Ota, and K. Nishikawa Redesign of artificial globins: effects of residue replacements at hydrophobic sites on the structural properties Biochemistry 39 2000 5683 5690
91. N.R. Rojas, S. Kamtekar, C.T. Simons, J.E. McLean, K.M. Vogel, T.G. Spiro, R.S. Farid, and M.H. Hecht De novo heme proteins from designed combinatorial libraries Protein Sci. 6 1997 2512 2524
92. H.K. Rau, and W. Haehnel Design, synthesis, and properties of a novel cytochrome b model J. Am. Chem. Soc. 120 1998 468 476
93. H.K. Rau, N. DeJonge, and W. Haehnel Combinatorial synthesis of four-helix bundle hemoproteins for tuning of cofactor properties Angew. Chem. Int. Ed. Engl. 39 2000 250 253
94. Y. Wei, T. Liu, S.L. Sazinsky, D.A. Moffet, I. Pelczer, and M.H. Hecht Stably folded de novo proteins from a designed combinatorial library Protein Sci. 12 2003 92 102
95. D.A. Moffet, J. Foley, and M.H. Hecht Midpoint reduction potentials and heme binding stoichiometries of de novo proteins from designed combinatorial libraries Biophys. Chem. 105 2003 231 239
96. A. Das, S.A. Trammell, and M.H. Hecht Electrochemical and ligand binding studies of a de novo heme protein Biophys. Chem. 123 2006 102 112
97. T. Albrecht, W. Li, J. Ulstrup, W. Haehnel, and P. Hildebrandt Electrochemical and spectroscopic investigations of immobilized de novo designed heme proteins on metal electrodes ChemPhysChem 6 2005 961 970
98. T. Albrecht, W.W. Li, W. Haehnel, P. Hildebrandt, and J. Ulstrup Voltammetry and in situ scanning tunnelling microscopy of de novo designed heme protein monolayers on Au(111)-electrode surfaces Bioelectrochemistry 69 2006 193 200
99. F. Nastri, A. Lombardi, G. Morelli, O. Maglio, G. D'Auria, C. Pedone, and V. Pavone Hemoprotein models based on a covalent helix-heme-helix sandwich: 1. Design, synthesis, and characterization Chem. Eur. J. 3 1997 340 349
100. D.R. Benson, B.R. Hart, X. Zhu, and M.B. Doughty Design, synthesis, and circular dichroism investigation of a peptide-sandwiched mesoheme J. Am. Chem. Soc. 117 1995 8502 8510
101. P.A. Arnold, D.R. Benson, D.J. Brink, M.P. Hendrich, G.S. Jas, M.L. Kennedy, D.T. Petasis, and M. Wang Helix induction and springboard strain in peptide-sandwiched mesohemes1 Inorg. Chem. 36 1997 5306 5315
102. P.A. Arnold, W.R. Shelton, and D.R. Benson Peptide helix induction in a self-assembling hemoprotein model J. Am. Chem. Soc. 119 1997 3181 3182
103. D.L. Huffman, M.M. Rosenblatt, and K.S. Suslick Synthetic heme-peptide complexes J. Am. Chem. Soc. 120 1998 6183 6184
104. D.L. Huffman, and K.S. Suslick Hydrophobic interactions in metalloporphyrin-peptide complexes Inorg. Chem. 39 2000 5418 5419
105. M.M. Rosenblatt, D.L. Huffman, X. Wang, H.A. Remmer, and K.S. Suslick Cyclic and hairpin peptide complexes of heme J. Am. Chem. Soc. 124 2002 12394 12395
106. M.M. Rosenblatt, J. Wang, and K.S. Suslick De novo designed cyclic-peptide heme complexes Proc. Natl. Acad. Sci. U. S. A. 100 2003 13140 13145
107. D. Liu, D.A. Williamson, M.L. Kennedy, T.D. Williams, M.M. Morton, and D.R. Benson Aromatic side chain-porphyrin interactions in designed hemoproteins J. Am. Chem. Soc. 121 1999 11798 11812
108. 1H NMR study of the solution molecular and electronic structure of engineered distal myoglobin His64(E7) Val/Val68(E11) His double mutant. Coordination of His64(E11) at the sixth position in both low-spin and high-spin states J. Biol. Chem. 269 1994 1083 1090
109. E. Lloyd, D.P. Hildebrand, K.M. Tu, and A.G. Mauk Conversion of myoglobin into a reversible electron transfer protein that maintains bishistidine axial ligation J. Am. Chem. Soc. 117 1995 6434 6438
110. Y. Dou, S.J. Admiraal, M. Ikeda-Saito, S. Krzywda, A.J. Wilkinson, T. Li, J.S. Olson, R.C. Prince, I.J. Pickering, and G.N. George Alteration of axial coordination by protein engineering in myoglobin. Bisimidazole ligation in the His64 - > Val/Val68 - > His double mutant J. Biol. Chem. 270 1995 15993 16001
111. J.R. Wilson, D.J. Caruana, and G. Gilardi Engineering redox functions in a nucleic acid binding protein Chem. Commun. 356-357 2003
112. J.M. Cordova, P.L. Noack, S.A. Hilcove, J.D. Lear, and G. Ghirlanda Design of a functional membrane protein by engineering a heme-binding site in glycophorin A J. Am. Chem. Soc. 129 2007 512 518
113. G. Di Nardo, A. Di Venere, G. Mei, S.J. Sadeghi, J.R. Wilson, and G. Gilardi Engineering heme binding sites in monomeric rop J. Biol. Inorg. Chem. 14 2009 497 505
114. S. Shinde, J.M. Cordova, B.W. Woodrum, and G. Ghirlanda Modulation of function in a minimalist heme-binding membrane protein J. Biol. Inorg. Chem. 17 2012 557 564
115. P.D. Barker, J.C. Ferrer, M. Mylrajan, T.M. Loehr, R. Feng, Y. Konishi, W.D. Funk, R.T. MacGillivray, and A.G. Mauk Transmutation of a heme protein Proc. Natl. Acad. Sci. U. S. A. 90 1993 6542 6546
116. P.D. Barker, E.P. Nerou, S.M. Freund, and I.M. Fearnley Conversion of cytochrome b562 to c-type cytochromes Biochemistry 34 1995 15191 15203
117. E.J. Tomlinson, and S.J. Ferguson Loss of either of the two heme-binding cysteines from a class I c-type cytochrome has a surprisingly small effect on physicochemical properties J. Biol. Chem. 275 2000 32530 32534
118. E.J. Tomlinson, and S.J. Ferguson Conversion of a c type cytochrome to a b type that spontaneously forms in vitro from apo protein and heme: implications for c type cytochrome biogenesis and folding Proc. Natl. Acad. Sci. U. S. A. 97 2000 5156 5160
119. S.M. Ibrahim, H. Nakajima, T. Ohta, K. Ramanathan, N. Takatani, Y. Naruta, and Y. Watanabe Cytochrome c(552) from Thermus thermophilus engineered for facile substitution of prosthetic group Biochemistry 50 2011 9826 9835
120. R. Wain, C. Redfield, S.J. Ferguson, and L.J. Smith NMR analysis shows that a b-type variant of Hydrogenobacter thermophilus cytochrome c552 retains its native structure J. Biol. Chem. 279 2004 15177 15182
121. G.L. Anderson, and J.B. Howard Reactions with the oxidized iron protein of Azotobacter vinelandii nitrogenase: formation of a 2Fe center Biochemistry 23 1984 2118 2122
122. W.G. Fu, T.V. Morgan, L.E. Mortenson, and M.K. Johnson Resonance Raman studies of the [4Fe-4S] to [2Fe-2S] cluster conversion in the iron protein of nitrogenase FEBS Lett. 284 1991 165 168
123. E. Mulliez, S. Ollagnier-de Choudens, C. Meier, M. Cremonini, C. Luchinat, A.X. Trautwein, and M. Fontecave Iron-sulfur interconversions in the anaerobic ribonucleotide reductase from Escherichia coli J. Biol. Inorg. Chem. 4 1999 614 620
124. J. Yang, S.G. Naik, D.O. Ortillo, R. Garcia-Serres, M. Li, W.E. Broderick, B.H. Huynh, and J.B. Broderick The iron-sulfur cluster of pyruvate formate-lyase activating enzyme in whole cells: cluster interconversion and a valence-localized [4Fe-4S]2 + state Biochemistry 48 2009 9234 9241
125. 2: [4Fe-4S] to [2Fe-2S] conversion with loss of biological activity Proc. Natl. Acad. Sci. U. S. A. 94 1997 6087 6092
126. J.C. Crack, J. Green, N.E. Le Brun, and A.J. Thomson Detection of sulfide release from the oxygen-sensing [4Fe-4S] cluster of FNR J. Biol. Chem. 281 2006 18909 18913
127. B. Zhang, J.C. Crack, S. Subramanian, J. Green, A.J. Thomson, N.E. Le Brun, and M.K. Johnson Reversible cycling between cysteine persulfide-ligated [2Fe-2S] and cysteine-ligated [4Fe-4S] clusters in the FNR regulatory protein Proc. Natl. Acad. Sci. U. S. A. 109 2012 15734 15739
128. Y. Nicolet, R. Rohac, L. Martin, and J.C. Fontecilla-Camps X-ray snapshots of possible intermediates in the time course of synthesis and degradation of protein-bound Fe4S4 clusters Proc. Natl. Acad. Sci. U. S. A. 110 2013 7188 7192
129. T.A. Kent, J.L. Dreyer, M.C. Kennedy, B.H. Huynh, M.H. Emptage, H. Beinert, and E. Munck Mossbauer studies of beef heart aconitase: evidence for facile interconversions of iron-sulfur clusters Proc. Natl. Acad. Sci. U. S. A. 79 1982 1096 1100
130. M.C. Kennedy, T.A. Kent, M. Emptage, H. Merkle, H. Beinert, and E. Munck Evidence for the formation of a linear [3Fe-4S] cluster in partially unfolded aconitase J. Biol. Chem. 259 1984 14463 14471
131. M.J. Ryle, W.N. Lanzilotta, L.C. Seefeldt, R.C. Scarrow, and G.M. Jensen Circular dichroism and x-ray spectroscopies of Azotobacter vinelandii nitrogenase iron protein. MgATP and MgADP induced protein conformational changes affecting the [4Fe-4S] cluster and characterization of a [2Fe-2S] form J. Biol. Chem. 271 1996 1551 1557
132. M. Guergova-Kuras, R. Kuras, N. Ugulava, I. Hadad, and A.R. Crofts Specific mutagenesis of the Rieske iron-sulfur protein in Rhodobacter sphaeroides shows that both the thermodynamic gradient and the pK of the oxidized form determine the rate of quinol oxidation by the bc1 complex † Biochemistry 39 2000 7436 7444
133. N. Akira, and U. Norikazu Importance of Peptide Sequence in Electron-Transfer Reactions of Iron-Sulfur Clusters Metal Clusters in Proteins American Chemical Society 1988 292 301
134. M.L. Antonkine, M.S. Koay, B. Epel, C. Breitenstein, O. Gopta, W. Gartner, E. Bill, and W. Lubitz Synthesis and characterization of de novo designed peptides modelling the binding sites of [4Fe-4S] clusters in photosystem I Biochim. Biophys. Acta 1787 2009 995 1008
135. B.R. Gibney, S.E. Mulholland, F. Rabanal, and P.L. Dutton Ferredoxin and ferredoxin-heme maquettes Proc. Natl. Acad. Sci. U. S. A. 93 1996 15041 15046
136. J. Grzyb, F. Xu, V. Nanda, R. Luczkowska, E. Reijerse, W. Lubitz, and D. Noy Empirical and computational design of iron-sulfur cluster proteins Biochim. Biophys. Acta 1817 2012 1256 1262
137. V. Nanda, M.M. Rosenblatt, A. Osyczka, H. Kono, Z. Getahun, P.L. Dutton, J.G. Saven, and W.F. Degrado De novo design of a redox-active minimal rubredoxin mimic J. Am. Chem. Soc. 127 2005 5804 5805
138. J. Grzyb, F. Xu, L. Weiner, E.J. Reijerse, W. Lubitz, V. Nanda, and D. Noy De novo design of a non-natural fold for an iron-sulfur protein: alpha-helical coiled-coil with a four-iron four-sulfur cluster binding site in its central core Biochim. Biophys. Acta 1797 2010 406 413
139. W. Ma, and Y.T. Long Quinone/hydroquinone-functionalized biointerfaces for biological applications from the macro- to nano-scale Chem. Soc. Rev. 43 2014 30 41
140. S.C. Feifel, A. Kapp, R. Ludwig, and F. Lisdat Nanobiomolecular multiprotein clusters on electrodes for the formation of a switchable cascadic reaction scheme Angew. Chem. Int. Ed. Engl. 53 2014 5676 5679
141. B.M. Discher, R.L. Koder, C.C. Moser, and P.L. Dutton Hydrophilic to amphiphilic design in redox protein maquettes Curr. Opin. Chem. Biol. 7 2003 741 748
142. Y. Lv, T. Tan, and F. Svec Molecular imprinting of proteins in polymers attached to the surface of nanomaterials for selective recognition of biomacromolecules Biotechnol. Adv. 31 2013 1172 1186
143. G.A. Hudalla, T. Sun, J.Z. Gasiorowski, H. Han, Y.F. Tian, A.S. Chong, and J.H. Collier Gradated assembly of multiple proteins into supramolecular nanomaterials Nat. Mater. 13 2014 829 836
144. A.R. Arnold, and J.K. Barton DNA protection by the bacterial ferritin Dps via DNA charge transport J. Am. Chem. Soc. 135 2013 15726 15729
145. M.A. Grodick, H.M. Segal, T.J. Zwang, and J.K. Barton DNA-mediated signaling by proteins with 4Fe-4S clusters is necessary for genomic integrity J. Am. Chem. Soc. 136 2014 6470 6478
146. A. Kuzyk, K.T. Laitinen, and P. Torma DNA origami as a nanoscale template for protein assembly Nanotechnology 20 2009 235305
147. N.Y. Wong, C. Zhang, L.H. Tan, and Y. Lu Site-specific attachment of proteins onto a 3D DNA tetrahedron through backbone-modified phosphorothioate DNA Small 7 2011 1427 1430
148. B.S. Goodman, and S.L. Reck-Peterson Engineering defined motor ensembles with DNA origami Methods Enzymol. 540 2014 169 188
149. T. Kortemme, and D. Baker Computational design of protein-protein interactions Curr. Opin. Chem. Biol. 8 2004 91 97
150. P.S. Huang, J.J. Love, and S.L. Mayo A de novo designed protein protein interface Protein Sci. 16 2007 2770 2774
151. D.J. Mandell, and T. Kortemme Computer-aided design of functional protein interactions Nat. Chem. Biol. 5 2009 797 807
152. J. Karanicolas, J.E. Corn, I. Chen, L.A. Joachimiak, O. Dym, S.H. Peck, S. Albeck, T. Unger, W. Hu, G. Liu, S. Delbecq, G.T. Montelione, C.P. Spiegel, D.R. Liu, and D. Baker A de novo protein binding pair by computational design and directed evolution Mol. Cell 42 2011 250 260
153. S.J. Fleishman, T.A. Whitehead, E.M. Strauch, J.E. Corn, S. Qin, H.X. Zhou, J.C. Mitchell, O.N. Demerdash, M. Takeda-Shitaka, G. Terashi, I.H. Moal, X. Li, P.A. Bates, M. Zacharias, H. Park, J.S. Ko, H. Lee, C. Seok, T. Bourquard, J. Bernauer, A. Poupon, J. Aze, S. Soner, S.K. Ovali, P. Ozbek, N.B. Tal, T. Haliloglu, H. Hwang, T. Vreven, B.G. Pierce, Z. Weng, L. Perez-Cano, C. Pons, J. Fernandez-Recio, F. Jiang, F. Yang, X. Gong, L. Cao, X. Xu, B. Liu, P. Wang, C. Li, C. Wang, C.H. Robert, M. Guharoy, S. Liu, Y. Huang, L. Li, D. Guo, Y. Chen, Y. Xiao, N. London, Z. Itzhaki, O. Schueler-Furman, Y. Inbar, V. Potapov, M. Cohen, G. Schreiber, Y. Tsuchiya, E. Kanamori, D.M. Standley, H. Nakamura, K. Kinoshita, C.M. Driggers, R.G. Hall, J.L. Morgan, V.L. Hsu, J. Zhan, Y. Yang, Y. Zhou, P.L. Kastritis, A.M. Bonvin, W. Zhang, C.J. Camacho, K.P. Kilambi, A. Sircar, J.J. Gray, M. Ohue, N. Uchikoga, Y. Matsuzaki, T. Ishida, Y. Akiyama, R. Khashan, S. Bush, D. Fouches, A. Tropsha, J. Esquivel-Rodriguez, D. Kihara, P.B. Stranges, R. Jacak, B. Kuhlman, S.Y. Huang, X. Zou, S.J. Wodak, J. Janin, and D. Baker Community-wide assessment of protein-interface modeling suggests improvements to design methodology J. Mol. Biol. 414 2011 289 302
154. P.B. Stranges, and B. Kuhlman A comparison of successful and failed protein interface designs highlights the challenges of designing buried hydrogen bonds Protein Sci. 22 2013 74 82
155. T.M. Jacobs, and B. Kuhlman Using anchoring motifs for the computational design of protein-protein interactions Biochem. Soc. Trans. 41 2013 1141 1145
156. P. Xiong, J.M. Nocek, J. Vura-Weis, J.V. Lockard, M.R. Wasielewski, and B.M. Hoffman Faster interprotein electron transfer in a [myoglobin, b(5)] complex with a redesigned interface Science 330 2010 1075 1078
157. E.N. Trana, J.M. Nocek, A.K. Knutson, and B.M. Hoffman Evolving the [myoglobin, cytochrome b5] complex from dynamic toward simple docking: charging the electron transfer reactive patch Biochemistry 51 2012 8542 8553
158. C.M. Agapakis, and P.A. Silver Modular electron transfer circuits for synthetic biology: insulation of an engineered biohydrogen pathway Bioeng. Bugs 1 2010 413 418
159. R. Langen, G.M. Jensen, U. Jacob, P.J. Stephens, and A. Warshel Protein control of iron-sulfur cluster redox potentials J. Biol. Chem. 267 1992 25625 25627
160. J.A. Cowan, and S.M. Lui Structure-function correlations in high-potential iron proteins Adv. Inorg. Chem. 45 1998 313 350
161. R.P. Venkateswara, and R.H. Holm Synthetic analogues of the active sites of iron-sulfur proteins Chem. Rev. 104 2004 527 559
162. C.W. Carter High potential iron sulfur proteins Handbook of Metalloproteins 2006 John Wiley & Sons, Ltd
163. H.M. Holden, B.L. Jacobson, J.K. Hurley, G. Tollin, B.H. Oh, L. Skjeldal, Y.K. Chae, H. Cheng, B. Xia, and J.L. Markley Structure-function studies of [2Fe-2S] ferredoxins J. Bioenerg. Biomembr. 26 1994 67 88
164. J. Meyer Ferredoxins of the third kind FEBS Lett. 509 2001 1 5
165. J. Meyer, S.L. Andrade, and O. Einsle Thioredoxin-like [2Fe-2S] ferredoxin Handbook of Metalloproteins 2006 John Wiley & Sons, Ltd
166. C. Binda, and A. Aliverti The [2Fe-2S] ferredoxins Encyclopedia of Inorganic and Bioinorganic Chemistry 2011 John Wiley & Sons, Ltd
167. J.-S. Park, T. Ohmura, K. Kano, T. Sagara, K. Niki, Y. Kyogoku, and H. Akutsu Regulation of the redox order of four hemes by pH in cytochrome C3 from D. vulgaris Miyazaki F Biochim. Biophys. Acta 1293 1996 45 54
168. S. Chapman, S. Daff, and A. Munro Heme: the most versatile redox centre in biology? H.A.O. Hill, P.J. Sadler, A.J. Thomson, Metal Sites in Proteins and Models 1997 Springer Berlin Heidelberg 39 70
169. P.J. Martel, C.M. Soares, A.M. Baptista, M. Fuxreiter, G. Náray-Szabó, R.O. Louro, and M.A. Carrondo Comparative redox and pK a calculations on cytochrome c 3 from several Desulfovibrio species using continuum electrostatic methods J. Biol. Inorg. Chem. 4 1999 73 86
170. H. Santos, J.J.G. Moura, I. Moura, J. LeGall, and A.V. Xavier NMR studies of electron transfer mechanisms in a protein with interacting redox centres: Desulfovibrio gigas cytochrome c3 Eur. J. Biochem. 141 1984 283 296
171. K.J. Fan, H. Akutsu, Y. Kyogoku, and K. Niki Estimation of microscopic redox potentials of a tetraheme protein, cytochrome c3 of Desulfovibrio vulgaris, Miyazaki F, and partial assignments of heme groups Biochemistry 29 1990 2257 2263
172. M. Coletta, T. Catarino, J. LeGall, and A.V. Xavier A thermodynamic model for the cooperative functional properties of the tetraheme cytochrome c3 from Desulfovibrio gigas Eur. J. Biochem. 202 1991 1101 1106
173. 3 Bull. Chem. Soc. Jpn. 84 2011 1096 1101
174. S.G. Sligar, K.D. Egeberg, J.T. Sage, D. Morikis, and P.M. Champion Alteration of heme axial ligands by site-directed mutagenesis: a cytochrome becomes a catalytic demethylase J. Am. Chem. Soc. 109 1987 7896 7897
175. I.C. Gunsalus, J.R. Meeks, J.D. Lipscomb, P. Debrunner, and E. Muenck Bacterial monooxygenases. P 450 cytochrome system Molecular Mechanism of Oxygen Activation 1974 Academic 559 613
176. K.D. Bewley, K.E. Ellis, M.A. Firer-Sherwood, and S.J. Elliott Multi-heme proteins: nature's electronic multi-purpose tool Biochim. Biophys. Acta 1827 2013 938 948
177. Y. Lu Electron transfer: cupredoxins J.A. McCleverty, T.J. Meyer, Comprehensive Coordination Chemistry II 2003 Elsevier Pergamon: Oxford 91 122
178. G. Battistuzzi, M. Bellei, C.A. Bortolotti, and M. Sola Redox properties of heme peroxidases Arch. Biochem. Biophys. 500 2010 21 36
179. R.J.P. Williams Heme proteins and oxygen A. Jacobs, M. Warwood, Iron in Biochemistry and Medicine 1974 Academic 183 219
180. S.-i. Adachi, S. Nagano, Y. Watanabe, K. Ishimori, and I. Morishima Alteration of human myoglobin proximal histidine to cysteine or tyrosine by site-directed mutagenesis: characterization and their catalytic activities Biochem. Biophys. Res. Commun. 180 1991 138 144
181. C.J. Reedy, M.M. Elvekrog, and B.R. Gibney Development of a heme protein structure-electrochemical function database Nucleic Acids Res. 36 2008 D307 D313
182. Z. Zheng, and M.R. Gunner Analysis of the electrochemistry of hemes with E(m)s spanning 800 mV Proteins 75 2009 719 734
183. K. Piontek, T. Glumoff, and K. Winterhalter Low pH crystal structure of glycosylated lignin peroxidase from Phanerochaete chrysosporium at 2.5 A resolution FEBS Lett. 315 1993 119 124
184. L. Banci Structural properties of peroxidases J. Biotechnol. 53 1997 253 263
185. J. Balk, and R. Lill The cell's cookbook for iron-sulfur clusters: recipes for fool's gold? ChemBioChem 5 2004 1044 1049
186. M.T. Werth, G. Cecchini, A. Manodori, B.A. Ackrell, I. Schröder, R.P. Gunsalus, and M.K. Johnson Site-directed mutagenesis of conserved cysteine residues in Escherichia coli fumarate reductase: modification of the spectroscopic and electrochemical properties of the [2Fe-2S] cluster Proc. Natl. Acad. Sci. U. S. A. 87 1990 8965 8969
187. S.E. Iismaa, A.E. Vazquez, G.M. Jensen, P.J. Stephens, J.N. Butt, F.A. Armstrong, and B.K. Burgess Site-directed mutagenesis of Azotobacter vinelandii ferredoxin I. Changes in [4Fe-4S] cluster reduction potential and reactivity J. Biol. Chem. 266 1991 21563 21571
188. H. Cheng, B. Xia, G.H. Reed, and J.L. Markley Optical, EPR, and 1H NMR spectroscopy of serine-ligated [2Fe-2S] ferredoxins produced by site-directed mutagenesis of cysteine residues in recombinant Anabaena 7120 vegetative ferredoxin Biochemistry 33 1994 3155 3164
189. A.L. Raphael, and H.B. Gray Axial ligand replacement in horse heart cytochrome c by semisynthesis Proteins Struct. Funct. Bioinf. 6 1989 338 340
190. G.T. Miller, B. Zhang, J.K. Hardman, and R. Timkovich Converting a c-type to a b-type cytochrome: Met61 to His61 mutant of Pseudomonas cytochrome c-551 Biochemistry 39 2000 9010 9017
191. S. Hay, and T. Wydrzynski Conversion of the Escherichia coli cytochrome b562 to an archetype cytochrome b: a mutant with bis-histidine ligation of heme iron † Biochemistry 44 2004 431 439
192. A. Dolla, L. Florens, P. Bianco, J. Haladjian, G. Voordouw, E. Forest, J. Wall, F. Guerlesquin, and M. Bruschi Characterization and oxidoreduction properties of cytochrome c3 after heme axial ligand replacements J. Biol. Chem. 269 1994 6340 6346
193. F.A. Tezcan, J.R. Winkler, and H.B. Gray Effects of ligation and folding on reduction potentials of heme proteins J. Am. Chem. Soc. 120 1998 13383 13388
194. W.D. Funk, T.P. Lo, M.R. Mauk, G.D. Brayer, R.T. MacGillivray, and A.G. Mauk Mutagenic, electrochemical, and crystallographic investigation of the cytochrome b5 oxidation-reduction equilibrium: involvement of asparagine-57, serine-64, and heme propionate-7 Biochemistry 29 1990 5500 5508
195. S.L. Springs, S.E. Bass, and G.L. McLendon Cytochrome b562 variants: a library for examining redox potential evolution Biochemistry 39 2000 6075 6082
196. R.H. Holm, P. Kennepohl, and E.I. Solomon Structural and functional aspects of metal sites in biology Chem. Rev. 96 1996 2239 2314
197. M.O. Senge Exercises in molecular gymnastics - bending, stretching and twisting porphyrins Chem. Commun. 243-256 2006
198. B. Roder, M. Buchner, I. Ruckmann, and M.O. Senge Correlation of photophysical parameters with macrocycle distortion in porphyrins with graded degree of saddle distortion Photochem. Photobiol. Sci. 9 2010 1152 1158
199. M.O. Senge New trends in photobiology: the conformational flexibility of tetrapyrroles - current model studies and photobiological relevance J. Photochem. Photobiol. B Biol. 16 1992 3 36
200. J. Hobbs, and J. Shelnutt Conserved nonplanar heme distortions in cytochromesc J. Protein Chem. 14 1995 19 25
201. W. Jentzen, J.-G. Ma, and J.A. Shelnutt Conservation of the conformation of the porphyrin macrocycle in hemoproteins Biophys. J. 74 1998 753 763
202. J.G. Ma, M. Laberge, X.Z. Song, W. Jentzen, S.L. Jia, J. Zhang, J.M. Vanderkooi, and J.A. Shelnutt Protein-induced changes in nonplanarity of the porphyrin in nickel cytochrome c probed by resonance Raman spectroscopy Biochemistry 37 1998 5118 5128
203. L.N. Todd, and M. Zimmer Moderating influence of proteins on nonplanar tetrapyrrole deformations: coenzyme F430 in methyl-coenzyme-M reductase Inorg. Chem. 41 2002 6831 6837
204. C. Olea Jr., J. Kuriyan, and M.A. Marletta Modulating heme redox potential through protein-induced porphyrin distortion J. Am. Chem. Soc. 132 2010 12794 12795
205. M. Can, G. Zoppellaro, K.K. Andersson, and K.L. Bren Modulation of ligand-field parameters by heme ruffling in cytochromes c revealed by EPR spectroscopy Inorg. Chem. 50 2011 12018 12024
206. G. Backes, Y. Mino, T.M. Loehr, T.E. Meyer, M.A. Cusanovich, W.V. Sweeney, E.T. Adman, and J. Sanders-Loehr The environment of Fe4S4 clusters in ferredoxins and high-potential iron proteins. New information from x-ray crystallography and resonance Raman spectroscopy J. Am. Chem. Soc. 113 1991 2055 2064
207. E.D. Duee, E. Fanchon, J. Vicat, L.C. Sieker, J. Meyer, and J.M. Moulis Refined crystal structure of the 2[4Fe-4S] ferredoxin from Clostridium acidurici at 1.84 Å resolution J. Mol. Biol. 243 1994 683 695
208. Z. Dauter, K.S. Wilson, L.C. Sieker, J. Meyer, and J.M. Moulis Atomic resolution (0.94 Å) structure of Clostridium acidurici ferredoxin. Detailed geometry of [4Fe-4S] clusters in a protein Biochemistry 36 1997 16065 16073
209. C.D. Stout, E.A. Stura, and D.E. McRee Structure of Azotobacter vinelandii 7Fe ferredoxin at 1.35 Å resolution and determination of the [Fe-S] bonds with 0.01 Å accuracy J. Mol. Biol. 278 1998 629 639
210. T.A. Link, W.R. Hagen, A.J. Pierik, C. Assmann, and G. Von Jagow Determination of the redox properties of the Rieske [2Fe-2S] cluster of bovine heart bc1 complex by direct electrochemistry of a water-soluble fragment Eur. J. Biochem. 208 1992 685 691
211. R. Cammack, K.K. Rao, C.P. Bargeron, K.G. Hutson, P.W. Andrew, and L.J. Rogers Midpoint redox potentials of plant and algal ferredoxins Biochem. J. 168 1977 205 209
212. M. Choi, and V.L. Davidson Cupredoxins - a study of how proteins may evolve to use metals for bioenergetic processes Metallomics 3 2011 140 151
213. A.J. Vila, and C.O. Fernandez Copper in electron transfer proteins I. Bertini, A. Sigel, H. Sigel, Handbook on Metalloproteins 2001 Marcel Dekker New York, NY 813
214. E.I. Solomon, R.K. Szilagyi, S. DeBeer George, and L. Basumallick Electronic structures of metal sites in proteins and models: contributions to function in blue copper proteins Chem. Rev. 104 2004 419 458
215. C. Dennison Investigating the structure and function of cupredoxins Coord. Chem. Rev. 249 2005 3025 3054
216. R.J. Kassner Effects of nonpolar environments on the redox potentials of heme complexes Proc. Natl. Acad. Sci. U. S. A. 69 1972 2263 2267
217. E. Stellwagen Haem exposure as the determinate of oxidation-reduction potential of haem proteins Nature 275 1978 73 74
218. A.K. Churg, and A. Warshel Control of the redox potential of cytochrome c and microscopic dielectric effects in proteins Biochemistry 25 1986 1675 1681
219. M. Rivera, R. Seetharaman, D. Girdhar, M. Wirtz, X. Zhang, X. Wang, and S. White The reduction potential of cytochrome b5 is modulated by its exposed heme edge Biochemistry 37 1998 1485 1494
220. A. Fantuzzi, S. Sadeghi, F. Valetti, G.L. Rossi, and G. Gilardi Tuning the reduction potential of engineered cytochrome c-553 Biochemistry 41 2002 8718 8724
221. G. Battistuzzi, M. Borsari, J.A. Cowan, A. Ranieri, and M. Sola Control of cytochrome C redox potential: axial ligation and protein environment effects J. Am. Chem. Soc. 124 2002 5315 5324
222. M. Paoli, J. Marles-Wright, and A. Smith Structure-function relationships in heme-proteins DNA Cell Biol. 21 2002 271 280
223. K.K. Rodgers, and S.G. Sligar Surface electrostatics, reduction potentials, and the internal dielectric constant of proteins J. Am. Chem. Soc. 113 1991 9419 9421
224. C.M. DiCarlo, L.B. Vitello, and J.E. Erman Reduction potential shifts due to active site and surface mutations of yeast cytochrome c peroxidase ECS Trans. 6 2007 27 45
225. G.M. Jensen, A. Warshel, and P.J. Stephens Calculation of the redox potentials of iron-sulfur proteins: the 2-/3-couple of [Fe4S∗4Cys4] clusters in Peptococcus aerogenes ferredoxin, Azotobacter vinelandii ferredoxin I, and Chromatium vinosum high-potential iron protein Biochemistry 33 1994 10911 10924
226. L. Banci, I. Bertini, S. Ciurli, C. Luchinat, and R. Pierattelli Rationalization of the reduction potentials within the series of the high potential iron-sulfur proteins Inorg. Chim. Acta 240 1995 251 256
227. A. Romero, C.W. Hoitink, H. Nar, R. Huber, A. Messerschmidt, and G.W. Canters X-ray analysis and spectroscopic characterization of M121Q azurin. A copper site model for stellacyanin J. Mol. Biol. 229 1993 1007 1021
228. T. Pascher, B.G. Karlsson, M. Nordling, B.G. Malmstrom, and T. Vanngard Reduction potentials and their pH dependence in site-directed-mutant forms of azurin from Pseudomonas aeruginosa Eur. J. Biochem. 212 1993 289 296
229. S. Yanagisawa, and C. Dennison Reduction potential tuning at a type 1 copper site does not compromise electron transfer reactivity J. Am. Chem. Soc. 127 2005 16453 16459
230. G.J. Davies, and V. Ducros Laccases A. Messerschmidt, R. Huber, T. Poulos, K. Wieghardt, Handbook of Metalloproteins 2001 Wiley Chichester 1359
231. M.D. Lowery, and E.I. Solomon Axial ligand bonding in blue copper proteins Inorg. Chim. Acta 198-200 1992 233 243
232. H. Nar, A. Messerschmidt, R. Huber, M. van de Kamp, and G.W. Canters Crystal structure analysis of oxidized Pseudomonas aeruginosa azurin at pH 5.5 and pH 9.0. A pH-induced conformational transition involves a peptide bond flip J. Mol. Biol. 221 1991 765 772
233. S. Yanagisawa, M.J. Banfield, and C. Dennison The role of hydrogen bonding at the active site of a cupredoxin: the Phe114Pro azurin variant Biochemistry 45 2006 8812 8822
234. L.D. Kanbi, S. Antonyuk, M.A. Hough, J.F. Hall, F.E. Dodd, and S.S. Hasnain Crystal structures of the Met148Leu and Ser86Asp mutants of rusticyanin from Thiobacillus ferrooxidans: insights into the structural relationship with the cupredoxins and the multi copper proteins J. Mol. Biol. 320 2002 263 275
235. N.M. Marshall, D.K. Garner, T.D. Wilson, Y.-G. Gao, H. Robinson, M.J. Nilges, and Y. Lu Rationally tuning the reduction potential of a single cupredoxin beyond the natural range Nature 462 2009 113 116
236. T.L. Poulos Heme enzyme crystal structures Adv. Inorg. Biochem. 7 1988 1 36
237. J.H. Dawson Probing structure-function relations in heme-containing oxygenases and peroxidases Science 240 1988 433 439
238. T.L. Poulos, and J. Kraut The stereochemistry of peroxidase catalysis J. Biol. Chem. 255 1980 8199 8205
239. L. Banci, I. Bertini, P. Turano, M. Tien, and T.K. Kirk Proton NMR investigation into the basis for the relatively high redox potential of lignin peroxidase Proc. Natl. Acad. Sci. U. S. A. 88 1991 6956 6960
240. S.E. Bowman, and K.L. Bren Variation and analysis of second-sphere interactions and axial histidinate character in c-type cytochromes Inorg. Chem. 49 2010 7890 7897
241. A.M. Berghuis, and G.D. Brayer Oxidation state-dependent conformational changes in cytochrome c J. Mol. Biol. 223 1992 959 976
242. A.M. Berghuis, J.G. Guillemette, M. Smith, and G.D. Brayer Mutation of tyrosine-67 to phenylalanine in cytochrome c significantly alters the local heme environment J. Mol. Biol. 235 1994 1326 1341
243. C.W. Conroy, P. Tyma, P.H. Daum, and J.E. Erman Oxidation-reduction potential measurements of cytochrome c peroxidase and pH dependent spectral transitions in the ferrous enzyme Biochim. Biophys. Acta, Protein Struct. 537 1978 62 69
244. K. Chen, G.J. Tilley, V. Sridhar, G.S. Prasad, C.D. Stout, F.A. Armstrong, and B.K. Burgess Alteration of the reduction potential of the [4Fe-4S](2 +/+) cluster of Azotobacter vinelandii ferredoxin I J. Biol. Chem. 274 1999 36479 36487
245. E. Adman, K.D. Watenpaugh, and L.H. Jensen NH-S hydrogen bonds in Peptococcus aerogenes ferredoxin, Clostridium pasteurianum rubredoxin, and Chromatium high potential iron protein Proc. Natl. Acad. Sci. U. S. A. 72 1975 4854 4858
246. T. Ichiye Computational studies o redox properties of electron transfer proteins AIP Conf. Proc. 492 1999
247. L. Noodleman, M.E. Pique, and V.A. Roberts Iron-Sulfur Clusters: Properties and Functions 2009 John Wiley & Sons, Inc. 458 468
248. E.N. Brown, R. Friemann, A. Karlsson, J.V. Parales, M.M. Couture, L.D. Eltis, and S. Ramaswamy Determining Rieske cluster reduction potentials J. Biol. Inorg. Chem. 13 2008 1301 1313
249. E. Denke, T. Merbitz-Zahradnik, O.M. Hatzfeld, C.H. Snyder, T.A. Link, and B.L. Trumpower Alteration of the midpoint potential and catalytic activity of the rieske iron-sulfur protein by changes of amino acids forming hydrogen bonds to the iron-sulfur cluster J. Biol. Chem. 273 1998 9085 9093
250. J.R. Mason, and R. Cammack The electron-transport proteins of hydroxylating bacterial dioxygenases Annu. Rev. Microbiol. 46 1992 277 305
251. T.A. Link The structures of Rieske and Rieske-type proteins Adv. Inorg. Chem. 47 1999 83 157
252. S.M. Berry, M.H. Baker, and N.J. Reardon Reduction potential variations in azurin through secondary coordination sphere phenylalanine incorporations J. Inorg. Biochem. 104 2010 1071 1078
253. B. Shen, D.R. Jollie, C.D. Stout, T.C. Diller, F.A. Armstrong, C.M. Gorst, G.N. La Mar, P.J. Stephens, and B.K. Burgess Azotobacter vinelandii ferredoxin I. Alteration of individual surface charges and the [4FE-4S]2 +/+ cluster reduction potential J. Biol. Chem. 269 1994 8564 8575
254. A. Dey, F.E. Jenney Jr., M.W. Adams, E. Babini, Y. Takahashi, K. Fukuyama, K.O. Hodgson, B. Hedman, and E.I. Solomon Solvent tuning of electrochemical potentials in the active sites of HiPIP versus ferredoxin Science 318 2007 1464 1468
255. J.A.R. Worrall, B.G. Schlarb-Ridley, T. Reda, M.J. Marcaida, R.J. Moorlen, J. Wastl, J. Hirst, D.S. Bendall, B.F. Luisi, and C.J. Howe Modulation of heme redox potential in the cytochrome c6 family J. Am. Chem. Soc. 129 2007 9468 9475
256. C.M. Lett, and J.G. Guillemette Increasing the redox potential of isoform 1 of yeast cytochrome c through the modification of select haem interactions Biochem. J. 362 2002 281 287
257. R. Varadarajan, T.E. Zewert, H.B. Gray, and S.G. Boxer Effects of buried ionizable amino acids on the reduction potential of recombinant myoglobin Science 243 1989 69 72
258. D.F. Wilson, M. Erecinska, and E.S. Brocklehurst Chemical properties of cytochrome c oxidase in intact mitochondria Arch. Biochem. Biophys. 151 1972 180 187
259. A. Soriano, D. Li, S. Bian, A. Agarwal, and J.A. Cowan Factors influencing redox thermodynamics and electron self-exchange for the [Fe4S4] cluster in Chromatium vinosum high potential iron protein: the role of core aromatic residues in defining cluster redox chemistry Biochemistry 35 1996 12479 12486
260. J. Vondrasek, L. Bendova, V. Klusak, and P. Hobza Unexpectedly strong energy stabilization inside the hydrophobic core of small protein rubredoxin mediated by aromatic residues: correlated ab initio quantum chemical calculations J. Am. Chem. Soc. 127 2005 2615 2619
261. K.E. Riley, and K.M. Merz Jr. Role of solvation in the energy stabilization inside the hydrophobic core of the protein rubredoxin J. Phys. Chem. B 110 2006 15650 15653
262. K. Ozawa, Y. Takayama, F. Yasukawa, T. Ohmura, M.A. Cusanovich, Y. Tomimoto, H. Ogata, Y. Higuchi, and H. Akutsu Role of the aromatic ring of Tyr43 in tetraheme cytochrome c3 from Desulfovibrio vulgaris Miyazaki F Biophys. J. 85 2003 3367 3374
263. M.V. Ponamarev, B.G. Schlarb, C.J. Howe, C.J. Carrell, J.L. Smith, D.S. Bendall, and W.A. Cramer Tryptophan-heme pi-electrostatic interactions in cytochrome f of oxygenic photosynthesis Biochemistry 39 2000 5971 5976
264. C. Dennison, E. Vijgenboom, W.R. Hagen, and G.W. Canters Loop-directed mutagenesis converts amicyanin from Thiobacillus versutus into a novel blue copper protein J. Am. Chem. Soc. 118 1996 7406 7407
265. C. Buning, G.W. Canters, P. Comba, C. Dennison, L. Jeuken, M. Melter, and J. Sanders-Loehr Loop-directed mutagenesis of the blue copper protein amicyanin from Paracoccus versutus and its effect on the structure and the activity of the type-1 copper Site J. Am. Chem. Soc. 122 1999 204 211
266. R. Remenyi, L.J. Jeuken, P. Comba, and G.W. Canters An amicyanin C-terminal loop mutant where the active-site histidine donor cannot be protonated J. Biol. Inorg. Chem. 6 2001 23 26
267. G. Battistuzzi, M. Borsari, G.W. Canters, G. di Rocco, E. de Waal, Y. Arendsen, A. Leonardi, A. Ranieri, and M. Sola Ligand loop effects on the free energy change of redox and pH-dependent equilibria in cupredoxins probed on amicyanin variants Biochemistry 44 2005 9944 9949
268. S. Yanagisawa, and C. Dennison Loop-contraction mutagenesis of type 1 copper sites J. Am. Chem. Soc. 126 2004 15711 15719
269. D.K. Garner, M.D. Vaughan, H.J. Hwang, M.G. Savelieff, S.M. Berry, J.F. Honek, and Y. Lu Reduction potential tuning of the blue copper center in Pseudomonas aeruginosa azurin by the axial methionine as probed by unnatural amino acids J. Am. Chem. Soc. 128 2006 15608 15617
270. X. Liu, Y. Yu, C. Hu, W. Zhang, Y. Lu, and J. Wang Significant increase of oxidase activity through the genetic incorporation of a tyrosine-histidine cross-link in a myoglobin model of heme-copper oxidase Angew. Chem. Int. Ed. Engl. 51 2012 4312 4316
271. Y. Yu, X. Lv, J. Li, Q. Zhou, C. Cui, P. Hosseinzadeh, A. Mukherjee, M.J. Nilges, J. Wang, and Y. Lu Defining the role of tyrosine and rational tuning of oxidase activity by genetic incorporation of unnatural tyrosine analogs J. Am. Chem. Soc. 137 2015 4594 4597
272. Y. Yu, Q. Zhou, L. Wang, X. Liu, W. Zhang, M. Hu, J. Dong, J. Li, X. Lv, H. Ouyang, H. Li, F. Gao, W. Gong, Y. Lu, and J. Wang Significant improvement of oxidase activity through the genetic incorporation of a redox-active unnatural amino acid Chem. Sci. 6 2015 3881 3885
273. D.W. Low, and M.G. Hill Backbone-engineered high-potential iron proteins: effects of active-site hydrogen bonding on reduction potential J. Am. Chem. Soc. 122 2000 11039 11040
274. 2 reduction rates in a designed oxidase in myoglobin J. Am. Chem. Soc. 136 2014 11882 11885
275. B. He, R. Sinclair, B.R. Copeland, R. Makino, L.S. Powers, and I. Yamazaki The structure-function relationship and reduction potentials of high oxidation states of myoglobin and peroxidase Biochemistry 35 1996 2413 2420
276. O. Farver, and I. Pecht Long-range intramolecular electron transfer in azurins Proc. Natl. Acad. Sci. U. S. A. 86 1989 6968 6972
277. T.J. Mizoguchi, A.J. Di Bilio, H.B. Gray, and J.H. Richards Blue to type 2 binding. Copper(II) and cobalt(II) derivatives of a Cys112Asp mutant of Pseudomonas aeruginosa azurin J. Am. Chem. Soc. 114 1992 10076 10078
278. B.G. Karlsson, M. Nordling, T. Pascher, L.-C. Tsai, L. Sjolin, and L.G. Lundberg Cassette mutagenesis of Met121 in azurin from Pseudomonas aeruginosa Protein Eng. 4 1991 343 349
279. T. Den Blaauwen, and G.W. Canters Creation of type-1 and type-2 copper sites by addition of exogenous ligands to the Pseudomonas aeruginosa azurin His117Gly mutant J. Am. Chem. Soc. 115 1993 1121 1129
280. A. Messerschmidt, L. Prade, S.J. Kroes, J. Sanders-Loehr, R. Huber, and G.W. Canters Rack-induced metal binding vs. flexibility: Met121His azurin crystal structures at different pH Proc. Natl. Acad. Sci. U. S. A. 95 1998 3443 3448
281. L.K. Skov, T. Pascher, J.R. Winkler, and H.B. Gray Rates of intramolecular electron transfer in Ru(bpy)2(im)(His83)-modified azurin increase below 220 K J. Am. Chem. Soc. 120 1998 1102 1103
282. E.N. Baker, B.F. Anderson, K.E. Blackwell, R.L. Kingston, G.E. Norris, and W.E.B. Shepard The relative rigidity of the type 1 copper site in azurin, as seen in high resolution X-ray analyses of various forms of the protein J. Inorg. Biochem. 43 1991 162
283. M.J. Bjerrum, D.R. Casimiro, I.J. Chang, A.J. Di Bilio, H.B. Gray, M.G. Hill, R. Langen, G.A. Mines, L.K. Skov, J.R. Winkler, and et al. Electron transfer in ruthenium-modified proteins J. Bioenerg. Biomembr. 27 1995 295 302
284. S.M. Berry, M.D. Gieselman, M.J. Nilges, W.A. van der Donk, and Y. Lu An engineered azurin variant containing a selenocysteine copper ligand J. Am. Chem. Soc. 124 2002 2084 2085
285. O. Farver, G.W. Canters, I. van Amsterdam, and I. Pecht Intramolecular electron transfer in a covalently linked mutated azurin dimer J. Phys. Chem. A 107 2003 6757 6760
286. S.M. Berry, M. Ralle, D.W. Low, N.J. Blackburn, and Y. Lu Probing the role of axial methionine in the blue copper center of azurin with unnatural amino acids J. Am. Chem. Soc. 125 2003 8760 8768
287. M. Cascella, A. Magistrato, I. Tavernelli, P. Carloni, and U. Rothlisberger Role of protein frame and solvent for the redox properties of azurin from Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U. S. A. 103 2006 19641 19646
288. K.M. Lancaster, S. Sproules, J.H. Palmer, J.H. Richards, and H.B. Gray Outer-sphere effects on reduction potentials of copper sites in proteins: the curious case of high potential type 2 C112D/M121E Pseudomonas aeruginosa azurin J. Am. Chem. Soc. 132 2010 14590
289. T. Pascher, B.G. Karlsson, M. Nordling, B.G. MalmstrÖM, and T. VÄNngÅRd Reduction potentials and their pH dependence in site-directed-mutant forms of azurin from Pseudomonas aeruginosa Eur. J. Biochem. 212 1993 289 296
290. R.G. Hadt, N. Sun, N.M. Marshall, K.O. Hodgson, B. Hedman, Y. Lu, and E.I. Solomon Spectroscopic and DFT studies of second-sphere variants of the type 1 copper site in azurin: covalent and nonlocal electrostatic contributions to reduction potentials J. Am. Chem. Soc. 134 2012 16701 16716
291. O. Farver, N.M. Marshall, S. Wherland, Y. Lu, and I. Pecht Designed azurins show lower reorganization free energies for intraprotein electron transfer Proc. Natl. Acad. Sci. U. S. A. 110 2013 10536 10540
292. O. Farver, P. Hosseinzadeh, N.M. Marshall, S. Wherland, Y. Lu, and I. Pecht Long-range electron transfer in engineered azurins exhibits marcus inverted region behavior J. Phys. Chem. Lett. 6 2015 100 105
293. E. Antonini, and M. Brunori Hemoglobin and myoglobin in their reactions with ligands Front. Biol. 21 1971 (North-Holland)
294. M.F. Perutz, P.D. Pulsinelli, and H.M. Ranney Structure and subunit interaction of hemoglobin M Milwaukee Nat. New Biol. 237 1972 259 263
295. Y.W. Lin, N. Yeung, Y.G. Gao, K.D. Miner, S. Tian, H. Robinson, and Y. Lu Roles of glutamates and metal ions in a rationally designed nitric oxide reductase based on myoglobin Proc. Natl. Acad. Sci. U. S. A. 107 2010 8581 8586
296. T. Murakami, I. Morishima, T. Matsui, S.-i. Ozaki, I. Hara, H.-J. Yang, and Y. Watanabe Effects of the arrangement of a distal catalytic residue on regioselectivity and reactivity in the coupled oxidation of sperm whale myoglobin mutants J. Am. Chem. Soc. 121 1999 2007 2011
297. C. Redaelli, E. Monzani, L. Santagostini, L. Casella, A.M. Sanangelantoni, R. Pierattelli, and L. Banci Characterization and peroxidase activity of a myoglobin mutant containing a distal arginine ChemBioChem 3 2002 226 233
298. G. Battistuzzi, M. Bellei, L. Casella, C. Bortolotti, R. Roncone, E. Monzani, and M. Sola Redox reactivity of the heme Fe3 +/Fe2 + couple in native myoglobins and mutants with peroxidase-like activity J. Biol. Inorg. Chem. 12 2007 951 958
299. Y. Shiro, T. Iizuka, K. Marubayashi, T. Ogura, T. Kitagawa, S. Balasubramanian, and S.G. Boxer Spectroscopic study of Ser92 mutants of human myoglobin: hydrogen bonding effect of Ser92 to proximal His93 on structure and property of myoglobin Biochemistry 33 1994 14986 14992
300. C.D. Millis, D.Y. Cai, M.T. Stankovich, and M. Tien Oxidation-reduction potentials and ionization states of extracellular peroxidases from the lignin-degrading fungus Phanerochaete chrysosporium Biochemistry 28 1989 8484 8489
301. D.B. Goodin, and D.E. McRee The Asp-His-iron triad of cytochrome c peroxidase controls the reduction potential electronic structure, and coupling of the tryptophan free radical to the heme Biochemistry 32 1993 3313 3324
302. J.M. Mauro, L.A. Fishel, J.T. Hazzard, T.E. Meyer, G. Tollin, M.A. Cusanovich, and J. Kraut Tryptophan-191 → phenylalanine, a proximal-side mutation in yeast cytochrome c peroxidase that strongly affects the kinetics of ferrocytochrome c oxidation Biochemistry 27 1988 6243 6256
303. J.A. Zuris, D.A. Halim, A.R. Conlan, E.C. Abresch, R. Nechushtai, M.L. Paddock, and P.A. Jennings Engineering the redox potential over a wide range within a new class of FeS proteins J. Am. Chem. Soc. 132 2010 13120 13122
304. A.-F. Miller Superoxide dismutases: ancient enzymes and new insights FEBS Lett. 586 2012 585 595
305. C.K. Vance, and A.F. Miller Simple proposal that can explain the inactivity of metal-substituted superoxide dismutases J. Am. Chem. Soc. 120 1998 461 467
306. A.L. Schwartz, E. Yikilmaz, C.K. Vance, S. Vathyam, R.L. Koder, and A.F. Miller Mutational and spectroscopic studies of the significance of the active site glutamine to metal ion specificity in superoxide dismutase J. Inorg. Biochem. 80 2000 247 256
307. T.A. Jackson, and T.C. Brunold Combined spectroscopic/computational studies on Fe- and Mn-dependent superoxide dismutases: insights into second-sphere tuning of active site properties Acc. Chem. Res. 37 2004 461 470
308. E. Yikilmaz, J. Xie, T.C. Brunold, and A.F. Miller Hydrogen-bond-mediated tuning of the redox potential of the non-heme Fe site of superoxide dismutase J. Am. Chem. Soc. 124 2002 3482 3483
309. E. Yikilmaz, J. Porta, L.E. Grove, A. Vahedi-Faridi, Y. Bronshteyn, T.C. Brunold, G.E. Borgstahl, and A.F. Miller How can a single second sphere amino acid substitution cause reduction midpoint potential changes of hundreds of millivolts? J. Am. Chem. Soc. 129 2007 9927 9940
310. A.F. Miller Redox tuning over almost 1 V in a structurally conserved active site: lessons from Fe-containing superoxide dismutase Acc. Chem. Res. 41 2008 501 510
311. S.Y. New, N.M. Marshall, T.S.A. Hor, F. Xue, and Y. Lu Redox tuning of two biological copper centers through non-covalent interactions: same trend but different magnitude Chem. Commun. 48 2012 4217 4219
312. J. Bujons, A. Dikiy, J.C. Ferrer, L. Banci, and A.G. Mauk Charge reversal of a critical active-site residue of cytochrome-c peroxidase: characterization of the Arg48 - >Glu variant Eur. J. Biochem. 243 1997 72 84