Lessons from Nature: A Bio-Inspired Approach to Molecular Design

Biochemistry

Volumn 54, Issue 27, 2015, Pages 4167-4180

  Cook, Sarah A ^a   Hill, Ethan A ^a   Borovik, A S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

BIO-INSPIRED APPROACH; BIOLOGICAL ACTIVATION; BIOLOGICAL FUNCTIONS; HIGH SELECTIVITY; INTRICATE STRUCTURES; METALLO-PROTEINS; MOLECULAR DESIGN; SPECTROSCOPIC CHARACTERIZATION;

PROTEINS;

CARBON; FERRIC ION; HYDROGEN; METALLOPROTEIN; MYOGLOBIN; OXYGEN; SULFUR; WATER; CYTOCHROME P450; HEMOGLOBIN; PHOTOSYSTEM II; PORPHYRIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; HYDROGEN BOND; HYDROXYLATION; MUTATION; PHOTOSYNTHESIS; PRIORITY JOURNAL; ANIMAL; HUMAN; METABOLISM; PHOTOSYSTEM II; SYNTHETIC BIOLOGY;

ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; HEMOGLOBINS; HUMANS; METALLOPROTEINS; MODELS, MOLECULAR; OXYGEN; PHOTOSYSTEM II PROTEIN COMPLEX; PORPHYRINS; SYNTHETIC BIOLOGY;

EID: 84949550775     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00249     Document Type: Article

References (122)

1. Holm, R. H. and Solomon, E. I. (2014) Introduction: Bioinorganic enzymology II Chem. Rev. 114, 4039-4040
2. Dawson, J. (1988) Probing structure-function relations in heme-containing oxygenases and peroxidases Science 240, 433-439
3. Liu, J., Chakraborty, S., Hosseinzadeh, P., Yu, Y., Tian, S., Petrik, I., Bhagi, A., and Lu, Y. (2014) Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers Chem. Rev. 114, 4366-4469
4. Borovik, A. S. (2005) Bioinspired hydrogen bond motifs in ligand design: The role of noncovalent interactions in metal ion mediated activation of dioxygen Acc. Chem. Res. 38, 54-61
5. Capaldi, R. A. (1990) Structure and function of cytochrome c oxidase Annu. Rev. Biochem. 59, 569-596
6. Peters, J. W., Fisher, K., and Dean, D. R. (1995) Nitrogenase structure and function: A biochemical-genetic perspective Annu. Rev. Microbiol. 49, 335-366
7. Holm, R. H. and Solomon, E. I. (2004) Preface: Biomimetic inorganic chemistry Chem. Rev. 104, 347-348
8. Kendrew, J. C., Bodo, G., Dintzis, H. M., Parrish, R. G., Wyckoff, H., and Phillips, D. C. (1958) A Three-Dimensional Model of the Myoglobin Molecule Obtained by X-ray Analysis Nature 181, 662-666
9. Kendrew, J. C., Dickerson, R. E., Strandberg, B. E., Hart, R. G., Davies, D. R., Phillips, D. C., and Shore, V. C. (1960) Structure of Myoglobin: A Three-Dimensional Fourier Synthesis at 2 Å Resolution Nature 185, 422-427
10. Perutz, M. F., Rossmann, M. G., Cullis, A. F., Muirhead, H., Will, G., and North, A. C. T. (1960) Structure of Hæmoglobin: A Three-Dimensional Fourier Synthesis at 5.5-Å Resolution, Obtained by X-ray Analysis Nature 185, 416-422
11. Cohen, I. A. and Caughey, W. S. (1968) Substituted deuteroporphyrins. IV. Kinetics and mechanism of reactions of iron(II) porphyrins with oxygen Biochemistry 7, 636-641
12. Fleischer, E. B. and Srivastava, T. S. (1969) Structure and properties of μ-oxobis(tetraphenylporphineiron(III)) J. Am. Chem. Soc. 91, 2403-2405
13. Hoffman, A. B., Collins, D. M., Day, V. W., Fleischer, E. B., Srivastava, T. S., and Hoard, J. L. (1972) Crystal structure and moleculsr stereochemistry of μ-oxo-bis[α,β,γ,δ-tetraphenylporphinatoiron(III)] J. Am. Chem. Soc. 94, 3620-3626
14. Chang, C. K. and Traylor, T. G. (1973) Solution behavior of a synthetic myoblobin active site J. Am. Chem. Soc. 95, 5810-5811
15. Anderson, D. L., Weschler, C. J., and Basolo, F. (1974) Reversible reaction of simple ferrous porphyrins with molecular oxygen at low temperatures J. Am. Chem. Soc. 96, 5599-5600
16. Collman, J. P., Gagne, R. R., Halbert, T. R., Marchon, J. C., and Reed, C. A. (1973) Reversible oxygen adduct formation in ferrous complexes derived from a picket fence porphyrin. Model for oxymyoglobin J. Am. Chem. Soc. 95, 7868-7870
17. Collman, J. P., Gagne, R. T., and Reed, C. A. (1974) Paramagnetic dioxygen complex of iron(II) derived from a picket fence porphyrin. Further models for hemoproteins J. Am. Chem. Soc. 96, 2629-2631
18. Pauling, L. (1964) Nature of the Iron-Oxygen Bond in Oxyhæmoglobin Nature 203, 182-183
19. Weiss, J. J. (1964) Nature of the Iron-Oxygen Bond in Oxyhæmoglobin Nature 202, 83-84
20. Griffith, J. S. (1956) On the Magnetic Properties of Some Haemoglobin Complexes Proc. R. Soc. A 235, 23-36
21. Perutz, M. F. (1970) Stereochemistry of Cooperative Effects in Haemoglobin: Haem-Haem Interaction and the Problem of Allostery Nature 228, 726-734
22. Collman, J. P., Brauman, J. I., Doxsee, K. M., Halbert, T. R., and Suslick, K. S. (1978) Model compounds for the T state of hemoglobin Proc. Natl. Acad. Sci. U.S.A. 75, 564-568
23. Yang, J., Kloek, A. P., Goldberg, D. E., and Mathews, F. S. (1995) The structure of Ascaris hemoglobin domain I at 2.2 Å resolution: Molecular features of oxygen avidity Proc. Natl. Acad. Sci. U.S.A. 92, 4224-4228
24. Lacy, D. C., Mukherjee, J., Lucas, R. L., Day, V. W., and Borovik, A. S. (2013) Metal complexes with varying intramolecular hydrogen bonding networks Polyhedron 52, 261-267
25. Nam, E., Alokolaro, P. E., Swartz, R. D., Gleaves, M. C., Pikul, J., and Kovacs, J. A. (2011) Investigation of the mechanism of formation of a thiolate-ligated Fe(III)-OOH Inorg. Chem. 50, 1592-1602
26. Matsumoto, J., Suzuki, T., Kajita, Y., and Masuda, H. (2012) Synthesis and characterization of cobalt(II) complexes with tripodal polypyridine ligand bearing pivalamide groups. Selective formation of six- and seven-coordinate cobalt(II) complexes Dalton Trans. 41, 4107-4117
27. Wada, A., Ogo, S., Nagatomo, S., Kitagawa, T., Watanabe, Y., Jitsukawa, K., and Masuda, H. (2002) Reactivity of Hydroperoxide Bound to a Mononuclear Non-Heme Iron Site Inorg. Chem. 41, 616-618
28. Garner, D. K., Allred, R. A., Tubbs, K. J., Arif, A. M., and Berreau, L. M. (2002) Synthesis and Characterization of Mononuclear Zinc Aryloxide Complexes Supported by Nitrogen/Sulfur Ligands Possessing an Internal Hydrogen Bond Donor Inorg. Chem. 41, 3533-3541
29. Matson, E. M., Bertke, J. A., and Fout, A. R. (2014) Isolation of iron(II) aqua and hydroxyl complexes featuring a tripodal H-bond donor and acceptor ligand Inorg. Chem. 53, 4450-4458
30. Matson, E. M., Park, Y. J., and Fout, A. R. (2014) Facile nitrite reduction in a non-heme iron system: Formation of an iron(III)-oxo J. Am. Chem. Soc. 136, 17398-17401
31. MacBeth, C. E., Gupta, R., Mitchell-Koch, K. R., Young, V. G., Lushington, G. H., Thompson, W. H., Hendrich, M. P., and Borovik, A. S. (2004) Utilization of Hydrogen Bonds To Stabilize M-O(H) Units: Synthesis and Properties of Monomeric Iron and Manganese Complexes with Terminal Oxo and Hydroxo Ligands J. Am. Chem. Soc. 126, 2556-2567
32. 2 Science 289, 938-941
33. Fujimori, D. G., Barr, E. W., Matthews, M. L., Koch, G. M., Yonce, J. R., Walsh, C. T., Bollinger, J. M., Krebs, C., and Riggs-Gelasco, P. J. (2007) Spectroscopic evidence for a high-spin Br-Fe(IV)-oxo intermediate in the α-ketoglutarate-dependent halogenase CytC3 from Streptomyces J. Am. Chem. Soc. 129, 13408-13409
34. Blasiak, L. C., Vaillancourt, F. H., Walsh, C. T., and Drennan, C. L. (2006) Crystal structure of the non-haem iron halogenase SyrB2 in syringomycin biosynthesis Nature 440, 368-371
35. Price, J., Barr, E., Tirupati, B., and Krebs, C. (2003) The first direct characterization of a high-valent iron intermediate in the reaction of an α-ketoglutarate-dependent dioxygenase: A high-spin Fe(IV) complex in taurine/α-ketoglutarate dioxygenase (TauD) Biochemistry 42, 7497-7508
36. Wong, C., Fujimori, D. G., Walsh, C. T., and Drennan, C. L. (2009) Structural analysis of an open active site conformation of nonheme iron halogenase CytC3 J. Am. Chem. Soc. 131, 4872-4879
37. Lacy, D. C., Gupta, R., Stone, K. L., Greaves, J., Ziller, J. W., Hendrich, M. P., and Borovik, A. S. (2010) Formation, structure, and EPR detection of a high spin Fe(IV)-oxo species derived from either an Fe(III)-oxo or Fe(III)-OH complex J. Am. Chem. Soc. 132, 12188-12190
38. Gupta, R., Lacy, D. C., Bominaar, E. L., Borovik, A. S., and Hendrich, M. P. (2012) Electron paramagnetic resonance and Mössbauer spectroscopy and density functional theory analysis of a high-spin Fe(IV)-oxo complex J. Am. Chem. Soc. 134, 9775-9784
39. Ortiz de Montellano, P. R. (2010) Hydrocarbon hydroxylation by cytochrome P450 enzymes Chem. Rev. 110, 932-948
40. Green, M. T. (2009) C-H bond activation in heme proteins: The role of thiolate ligation in cytochrome P450 Curr. Opin. Chem. Biol. 13, 84-88
41. Denisov, I. G., Makris, T. M., Sligar, S. G., and Schlichting, I. (2005) Structure and chemistry of cytochrome P450 Chem. Rev. 105, 2253-2277
42. Newcomb, M., Zhang, R., Chandrasena, R. E. P., Halgrimson, J. A., Horner, J. H., Makris, T. M., and Sligar, S. G. (2006) Cytochrome P450 Compound I J. Am. Chem. Soc. 128, 4580-4581
43. Groves, J. T. and Van der Puy, M. (1974) Stereospecific aliphatic hydroxylation by an iron-based oxidant J. Am. Chem. Soc. 96, 5274-5275
44. Groves, J. T., McClusky, G. A., White, R. E., and Coon, M. J. (1978) Aliphatic hydroxylation by highly purified liver microsomal cytochrome P-450. Evidence for a carbon radical intermediate Biochem. Biophys. Res. Commun. 81, 154-160
45. Groves, J. T. and McClusky, G. A. (1976) Aliphatic hydroxylation via oxygen rebound. Oxygen transfer catalyzed by iron J. Am. Chem. Soc. 98, 859-861
46. Groves, J. T., Haushalter, R. C., Nakamura, M., Nemo, T. E., and Evans, B. J. (1981) High-valent iron-porphyrin complexes related to peroxidase and cytochrome P-450 J. Am. Chem. Soc. 103, 2884-2886
47. White, R. E. and Coon, M. J. (1980) Oxygen activation by cytochrome P-450 Annu. Rev. Biochem. 49, 315-356
48. Hamilton, G. A., Giacin, J. R., Hellman, T. M., Snook, M. E., and Weller, J. W. (1973) Oxenoid Models For Enzymatic Hydroxylations Ann. N.Y. Acad. Sci. 212, 4-12
49. Rutter, R., Hager, L. P., Dhonau, H., Hendrich, M., Valentine, M., and Debrunner, P. (1984) Chloroperoxidase compound I: Electron paramagnetic resonance and Mössbauer studies Biochemistry 23, 6809-6816
50. Groves, J. T., Kruper, W. J., Nemo, T. E., and Myers, R. S. (1980) Hydroxylation and expoxidation reactions catalyzed by synthetic metalloporphyrinates. Models related to the active oxygen species of cytochrome P-450 J. Mol. Catal. 7, 169-177
51. Groves, J. T., Nemo, T. E., and Myers, R. S. (1979) Hydroxylation and epoxidation catalyzed by iron-porphine complexes. Oxygen transfer from iodosylbenzene J. Am. Chem. Soc. 101, 1032-1033
52. Rittle, J. and Green, M. T. (2010) Cytochrome P450 compound I: Capture, characterization, and C-H bond activation kinetics Science 330, 933-937
53. Sligar, S. G. (2010) Chemistry. Glimpsing the critical intermediate in cytochrome P450 oxidations Science 330, 924-925
54. Sheng, X., Horner, J., and Newcomb, M. (2008) Spectra and kinetic studies of the compound I derivative of cytochrome P450 119 J. Am. Chem. Soc. 130, 13310-13320
55. Mayer, J. (1998) Hydrogen atom abstraction by metal-oxo complexes: Understanding the analogy with organic radical reactions Acc. Chem. Res. 31, 441-450
56. Yosca, T. H., Rittle, J., Krest, C. M., Onderko, E. L., Silakov, A., Calixto, J. C., Behan, R. K., and Green, M. T. (2013) Iron(IV)hydroxide pKa and the Role of Thiolate Ligation in C-H Bond Activation by Cytochrome P450 Science 342, 825-829
57. Shirin, Z., Hammes, B. S., Young, V. G., and Borovik, A. S. (2000) Hydrogen Bonding in Metal Oxo Complexes: Synthesis and Structure of a Monomeric Manganese(III)-Oxo Complex and Its Hydroxo Analogue J. Am. Chem. Soc. 122, 1836-1837
58. MacBeth, C. E., Hammes, B. S., Young, V. G., Jr., and Borovik, A. S. (2001) Hydrogen-bonding cavities about metal ions: Synthesis, structure, and physical properties for a series of monomeric M-OH complexes derived from water Inorg. Chem. 40, 4733-4741
59. Sastri, C. V., Lee, J., Oh, K., Lee, Y. J., Lee, J., Jackson, T. A., Ray, K., Hirao, H., Shin, W., Halfen, J. A., Kim, J., Que, L., Shaik, S., and Nam, W. (2007) Axial ligand tuning of a nonheme iron(IV)-oxo unit for hydrogen atom abstraction Proc. Natl. Acad. Sci. U.S.A. 104, 19181-19186
60. Nam, W., Lee, Y.-M., and Fukuzumi, S. (2014) Tuning reactivity and mechanism in oxidation reactions by mononuclear nonheme iron(IV)-oxo complexes Acc. Chem. Res. 47, 1146-1154
61. Usharani, D., Lacy, D. C., Borovik, A. S., and Shaik, S. (2013) Dichotomous Hydrogen Atom Transfer vs. Proton Coupled Electron Transfer During Activation of X-H Bonds (X = C, N,O) by Nonheme Iron-Oxo Complexes of Variable Basicity J. Am. Chem. Soc. 135, 17090-17104
62. III/II complexes with terminal hydroxo and oxo ligands: Probing reactivity via O-H bond dissociation energies J. Am. Chem. Soc. 125, 13234-13242
63. Parsell, T. H., Behan, R. K., Green, M. T., Hendrich, M. P., and Borovik, A. S. (2006) Preparation and properties of a monomeric Mn(IV)-oxo complex J. Am. Chem. Soc. 128, 8728-8729
64. Brintzinger, H., Palmer, G., and Sands, R. H. (1966) On the ligand field of iron in ferredoxin from spinach chloroplasts and related nonheme iron enzymes Proc. Natl. Acad. Sci. U.S.A. 55, 397-404
65. Gibson, J. F., Hall, D. O., Thornley, J. H., and Whatley, F. R. (1966) The iron complex in spinach ferredoxin Proc. Natl. Acad. Sci. U.S.A. 56, 987-990
66. 2+ double cubanes by site-specific reactions: Electron-transfer coupling across sulfur-containing bridges of variable length J. Am. Chem. Soc. 111, 1670-1676
67. 2S] J. Am. Chem. Soc. 112, 2455-2456
68. 2+ analog of iron-sulfur protein clusters J. Am. Chem. Soc. 109, 2546-2547
69. Ogino, H., Inomata, S., and Tobita, H. (1998) Abiological Iron-Sulfur Clusters Chem. Rev. 98, 2093-2122
70. Venkateswara Rao, P. and Holm, R. H. (2004) Synthetic analogues of the active sites of iron-sulfur proteins Chem. Rev. 104, 527-559
71. Lee, S. C., Lo, W., and Holm, R. H. (2014) Developments in the biomimetic chemistry of cubane-type and higher nuclearity iron-sulfur clusters Chem. Rev. 114, 3579-3600
72. Kent, T., Emptage, M., Merkle, H., Kennedy, M., Beinert, H., and Munck, E. (1985) Mossbauer studies of aconitase. Substrate and inhibitor binding, reaction intermediates, and hyperfine interactions of reduced 3Fe and 4Fe clusters J. Biol. Chem. 260, 6871-6881
73. Kent, T. A., Dreyer, J. L., Kennedy, M. C., Huynh, B. H., Emptage, M. H., Beinert, H., and Munck, E. (1982) Mossbauer studies of beef heart aconitase: evidence for facile interconversions of iron-sulfur clusters Proc. Natl. Acad. Sci. U.S.A. 79, 1096-1100
74. 2+ clusters: Synthesis, solution and solid-state structures, and subsite-specific reactions J. Am. Chem. Soc. 110, 2484-2494
75. Moran, J. R., Karbach, S., and Cram, D. J. (1982) Cavitands: Synthetic molecular vessels J. Am. Chem. Soc. 104, 5826-5828
76. Cram, D. J. (1983) Cavitands: Organic hosts with enforced cavities Science 219, 1177-1183
77. Gilmore, C. J., MacNicol, D. D., Murphy, A., and Russell, M. A. (1983) Synthesis of hexakis(aryloxy)benzenes: X-ray analysis of hexakis(phenyloxy)benzene and of the acetonitrile clathrate of hexakis(3,5-dimethylphenyloxy)benzene Tetrahedron Lett. 24, 3269-3272
78. Atwood, J. L., Davies, J. E. D., and MacNicol, D. D., Eds. (1984) Inclusion compounds, 2 nd ed., p 499, Academic, New York.
79. 2+ analog Inorg. Chem. 29, 3745-3760
80. 3- Anion Angew. Chem., Int. Ed. 27, 1353-1355
81. 0 unit structurally and electronically analogous to the reduced three-ion centers in ferredoxins J. Am. Chem. Soc. 114, 2472-2482
82. 2+ cubane-type clusters (M = iron, cobalt, nickel) J. Am. Chem. Soc. 114, 10843-10854
83. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Nature 473, 55-60
84. 2 evolving complex Coord. Chem. Rev. 252, 296-305
85. 2+ Biochemistry 27, 3476-3483
86. 2+ Function in Photosynthetic Oxygen Evolution Studied by Alkali Metal Cations Substitution Biophys. J. 81, 1831-1840
87. 2+ exchange in the photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus J. Biol. Chem. 279, 22809-22819
88. Pecoraro, V. L., Baldwin, M. J., Caudle, M. T., Hsieh, W.-Y., and Law, N. A. (1998) A proposal for water oxidation in photosystem II Pure Appl. Chem. 70, 925-929
89. 2 Formation Biochemistry 40, 7937-7945
90. Brudvig, G. W. (2008) Water oxidation chemistry of photosystem II Philos. Trans. R. Soc., B. 363, 1211-1219
91. 2 evolution Inorg. Chem. 52, 13833-13848
92. Mukhopadhyay, S., Mandal, S. K., Bhaduri, S., and Armstrong, W. H. (2004) Manganese clusters with relevance to photosystem II Chem. Rev. 104, 3981-4026
93. Mishra, A., Wernsdorfer, W., Abboud, K. A., and Christou, G. (2005) The first high oxidation state manganese-calcium cluster: Relevance to the water oxidizing complex of photosynthesis Chem. Commun. 54-56
94. Hewitt, I. J., Tang, J.-K., Madhu, N. T., Clérac, R., Buth, G., Anson, C. E., and Powell, A. K. (2006) A series of new structural models for the OEC in photosystem II Chem. Commun. 2650-2652
95. Mishra, A., Yano, J., Pushkar, Y., Yachandra, V. K., Abboud, K. A., and Christou, G. (2007) Heteronuclear Mn-Ca/Sr complexes, and Ca/Sr EXAFS spectral comparisons with the oxygen-evolving complex of photosystem II Chem. Commun. 1538-1540
96. Kotzabasaki, V., Siczek, M., Lis, T., and Milios, C. J. (2011) The first heterometallic Mn-Ca cluster containing exclusively Mn(III) centers Inorg. Chem. Commun. 14, 213-216
97. 3M(II)Na] complexes (M = Mn, Ca): Structural and functional models for the dioxygen evolving centre of PSII Dalton Trans. 40, 2699-2702
98. Tsui, E. Y., Day, M. W., and Agapie, T. (2011) Trinucleating copper: Synthesis and magnetostructural characterization of complexes supported by a hexapyridyl 1,3,5-triarylbenzene ligand Angew. Chem., Int. Ed. 50, 1668-1672
99. Tsui, E. Y., Kanady, J. S., Day, M. W., and Agapie, T. (2011) Trinuclear first row transition metal complexes of a hexapyridyl, trialkoxy 1,3,5-triarylbenzene ligand Chem. Commun. 47, 4189-4191
100. 3Ca subsite of the oxygen-evolving complex in photosystem II Science 333, 733-736
101. Tsui, E. Y. and Agapie, T. (2013) Reduction potentials of heterometallic manganese-oxido cubane complexes modulated by redox-inactive metals Proc. Natl. Acad. Sci. U.S.A. 110, 10084-10088
102. Tsui, E. Y., Tran, R., Yano, J., and Agapie, T. (2013) Redox-inactive metals modulate the reduction potential in heterometallic manganese-oxido clusters Nat. Chem. 5, 293-299
103. Vogt, L., Vinyard, D. J., Khan, S., and Brudvig, G. W. (2015) Oxygen-evolving complex of Photosystem II: An analysis of second-shell residues and hydrogen-bonding networks Curr. Opin. Chem. Biol. 25, 152-158
104. 2 production Science 333, 863-866
105. DuBois, D. L. (2014) Development of molecular electrocatalysts for energy storage Inorg. Chem. 53, 3935-3960
106. 2 oxidation catalyst performance Angew. Chem., Int. Ed. 53, 6487-6491
107. Yu, F., Cangelosi, V. M., Zastrow, M. L., Tegoni, M., Plegaria, J. S., Tebo, A. G., Mocny, C. S., Ruckthong, L., Qayyum, H., and Pecoraro, V. L. (2014) Protein design: Toward functional metalloenzymes Chem. Rev. 114, 3495-3578
108. Reig, A. J., Pires, M. M., Snyder, R. A., Wu, Y., Jo, H., Kulp, D. W., Butch, S. E., Calhoun, J. R., Szyperski, T., Szyperski, T. G., Solomon, E. I., and DeGrado, W. F. (2012) Alteration of the oxygen-dependent reactivity of de novo Due Ferri proteins Nat. Chem. 4, 900-906
109. Salgado, E. N., Ambroggio, X. I., Brodin, J. D., Lewis, R. A., Kuhlman, B., and Tezcan, F. A. (2010) Metal templated design of protein interfaces Proc. Natl. Acad. Sci. U.S.A. 107, 1827-1832
110. Song, W. J., Sontz, P. A., Ambroggio, X. I., and Tezcan, F. A. (2014) Metals in protein-protein interfaces Annu. Rev. Biophys. 43, 409-431
111. Song, W. J. and Tezcan, F. A. (2014) A designed supramolecular protein assembly with in vivo enzymatic activity Science 346, 1525-1528
112. Wilson, M. E. and Whitesides, G. M. (1978) Conversion of a protein to a homogeneous asymmetric hydrogenation catalyst by site-specific modification with a diphosphinerhodium(I) moiety J. Am. Chem. Soc. 100, 306-307
113. Ward, T. R. (2011) Artificial metalloenzymes based on the biotin-avidin technology: Enantioselective catalysis and beyond Acc. Chem. Res. 44, 47-57
114. Dürrenberger, M. and Ward, T. R. (2014) Recent achievments in the design and engineering of artificial metalloenzymes Curr. Opin. Chem. Biol. 19, 99-106
115. Hyster, T. K., Knörr, L., Ward, T. R., and Rovis, T. (2012) Biotinylated Rh(III) complexes in engineered streptavidin for accelerated asymmetric C-H activation Science 338, 500-503
116. 2 catalysed by a protein-bound iron complex Nat. Chem. 2, 1069-1076
117. Song, L.-C., Yang, Z.-Y., Bian, H.-Z., and Hu, Q.-M. (2004) Novel Single and Double Diiron Oxadithiolates as Models for the Active Site of [Fe]-Only Hydrogenases Organometallics 23, 3082-3084
118. Li, H. and Rauchfuss, T. B. (2002) Iron Carbonyl Sulfides, Formaldehyde, and Amines Condense To Give the Proposed Azadithiolate Cofactor of the Fe-Only Hydrogenases J. Am. Chem. Soc. 124, 726-727
119. 2- J. Am. Chem. Soc. 121, 9736-9737
120. Lyon, E., Georgakaki, I., Reibenspies, J., and Darensbourg, M. (1999) Carbon Monoxide and Cyanide Ligands in a Classical Organometallic Complex Model for Fe-Only Hydrogenase Angew. Chem., Int. Ed. 38, 3178-3180
121. Le Cloirec, A., Davies, S. C., Evans, D. J., Hughes, D. L., Pickett, C. J., Best, S. P., and Borg, S. (1999) A di-iron dithiolate possessing structural elements of the carbonyl/cyanide sub-site of the H-centre of Fe-only hydrogenase Chem. Commun. 2285-2286
122. Berggren, G., Adamska, A., Lambertz, C., Simmons, T. R., Esselborn, J., Atta, M., Gambarelli, S., Mouesca, J.-M., Reijerse, E., Lubitz, W., Happe, T., Artero, V., and Fontecave, M. (2013) Biomimetic assembly and activation of [FeFe]-hydrogenases Nature 499, 66-69