Ru(II)-diimine functionalized metalloproteins: From electron transfer studies to light-driven biocatalysis

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1857, Issue 5, 2016, Pages 589-597

  Lam, Quan ^a   Kato, Mallory ^a   Cheruzel, Lionel ^a  

^a SAN JOSE STATE UNIVERSITY   (United States)

Author keywords

Electron transfer studies; Light driven biocatalysis; Ruthenium photosensitizers

Indexed keywords

ACETYLENE; CARBON MONOXIDE; CARBON MONOXIDE DEHYDROGENASE; CYTOCHROME P450 BM3; HEMOPROTEIN; HYDROGEN CYANIDE; IMINE; LACCASE; METALLOPROTEIN; NITROGENASE; OXYGEN; PHOTOSENSITIZING AGENT; PROTON; RUTHENIUM; PROTEIN BINDING;

ARTICLE; BIOCATALYSIS; BIOCATALYST; ELECTRON; ELECTRON TRANSPORT; EXCITATION; LIGHT; PHOTOCHEMISTRY; PRIORITY JOURNAL; ANIMAL; CATALYSIS; CHEMISTRY; ENERGY METABOLISM; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; OXIDATION REDUCTION REACTION; PROCEDURES; PROTEIN ENGINEERING;

ANIMALS; CATALYSIS; ELECTRON TRANSPORT; ENERGY METABOLISM; HUMANS; IMINES; METALLOPROTEINS; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN ENGINEERING; RUTHENIUM;

EID: 84964319275     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.09.004     Document Type: Article

References (91)

1. H.B. Gray Powering the planet with solar fuel Nat. Chem. 1 2009 7
2. N.S. Lewis, and D.G. Nocera Powering the planet: chemical challenges in solar energy utilization Proc. Natl Acad. Sci. 104 2007 20142-20142
3. N. Nelson, and A. Ben-Shem The complex architecture of oxygenic photosynthesis Nat. Rev. Mol. Cell Bio. 5 2004 971 982
4. C. Tommos, and G.T. Babcock Oxygen production in nature: a light-driven metalloradical enzyme process Acc. Chem. Res. 31 1998 18 25
5. S. Styring, J. Sjoholm, and F. Mamedov Two tyrosines that changed the world: interfacing the oxidizing power of photochemistry to water splitting in photosystem II BBA-Bioenerg. 1817 2012 76 87
6. R.A. Marcus, and N. Sutin Electron transfers in chemistry and biology Biochim. Biophys. Acta 811 1985 265 322
7. H.B. Gray, and J.R. Winkler Electron flow through metalloproteins BBA-Bioenerg. 1797 2010 1563 1572
8. J.R. Winkler, and H.B. Gray Electron flow through metalloproteins Chem. Rev. 114 2014 3369 3380
9. H.B. Gray, and J.R. Winkler Electron transfer in proteins Annu. Rev. Biochem. 65 1996 537 561
10. J.R. Winkler, and H.B. Gray Long-range electron tunneling J. Am. Chem. Soc. 136 2014 2930 2939
11. K. Kalyanasundaram Photophysics, photochemistry and solar-energy conversion with tris(bipyridyl)ruthenium(Ii) and its analogs Coord. Chem. Rev. 46 1982 159 244
12. I.J. Chang, H.B. Gray, and J.R. Winkler High-driving-force electron-transfer in metalloproteins - intramolecular oxidation of ferrocytochrome-C by Ru(2,2'-bpy)2(Im)(his-33)3 + J. Am. Chem. Soc. 113 1991 7056 7057
13. H. Kotani, T. Suenobu, Y.M. Lee, W. Nam, and S. Fukuzumi Photocatalytic generation of a non-heme oxoiron(IV) Complex with water as an oxygen source J. Am. Chem. Soc. 133 2011 3249 3251
14. S. Berardi, S. Drouet, L. Francas, C. Gimbert-Surinach, M. Guttentag, C. Richmond, T. Stoll, and A. Llobet Molecular artificial photosynthesis Chem. Soc. Rev. 43 2014 7501 7519
15. P.D. Frischmann, K. Mahata, and F. Wurthner Powering the future of molecular artificial photosynthesis with light-harvesting metallosupramolecular dye assemblies Chem. Soc. Rev. 42 2013 1847 1870
16. M.D. Karkas, O. Verho, E.V. Johnston, and B. Akermark Artificial photosynthesis: molecular systems for catalytic water oxidation Chem. Rev. 114 2014 11863 12001
17. S. Fukuzumi Artificial photosynthetic systems for production of hydrogen Curr. Opin. Chem. Biol. 25 2015 18 26
18. T.R. Simmons, G. Berggren, M. Bacchi, M. Fontecave, and V. Artero Mimicking hydrogenases: from biomimetics to artificial enzymes Coord. Chem. Rev. 270 2014 127 150
19. B. Durham, and F. Millett Design of photoactive ruthenium complexes to study electron transfer and proton pumping in cytochrome oxidase BBA-Bioenerg. 1817 2012 567 574
20. F. Millett, and B. Durham Design of photoactive ruthenium complexes to study interprotein electron transfer Biochemistry 41 2002 11315 11324
21. S.Y. Reece, and D.G. Nocera Proton-coupled electron transfer in biology: results from synergistic studies in natural and model systems Annu. Rev. Biochem. 78 2009 673 699
22. V. Balzani, A. Credi, and M. Venturi Photochemistry and photophysics of coordination compounds: an extended view Coord. Chem. Rev. 171 1998 3 16
23. S. Campagna, F. Puntoriero, F. Nastasi, G. Bergamini, and V. Balzani Photochemistry and photophysics of coordination compounds: ruthenium Top. Curr. Chem. 280 2007 117 214
24. J.R. Winkler, D.G. Nocera, K.M. Yocom, E. Bordignon, and H.B. Gray Electron-transfer kinetics of pentaammineruthenium(Iii)(histidine-33)-ferricytochrome-C - measurement of the rate of intramolecular electron-transfer between redox centers separated by 15-a in a protein J. Am. Chem. Soc. 104 1982 5798 5800
25. K.M. Yocom, J.B. Shelton, J.R. Shelton, W.A. Schroeder, G. Worosila, S.S. Isied, E. Bordignon, and H.B. Gray Preparation and characterization of a pentaammineruthenium(Iii) derivative of horse heart ferricytochrome-C Proc. Natl. Acad. Sci. USA 79 1982 7052 7055
26. B.R. Crane, A.J. Di Bilio, J.R. Winkler, and H.B. Gray Electron tunneling in single crystals of Pseudomonas aeruginosa azurins J. Am. Chem. Soc. 123 2001 11623 11631
27. O.A. Zadvornyy, J.E. Lucon, R. Gerlach, N.A. Zorin, T. Douglas, T.E. Elgren, and J.W. Peters Photo-induced H-2 production by [NiFe]-hydrogenase from T. roseopersicina covalently linked to a Ru(II) photosensitizer J. Inorg. Biochem. 106 2012 151 155
28. E. Terpetschnig, H. Szmacinski, H. Malak, and J.R. Lakowicz Metal-ligand complexes as a new class of long-lived fluorophores for protein hydrodynamics Biophys. J. 68 1995 342 350
29. E.M. Ryan, R. Okennedy, M.M. Feeney, J.M. Kelly, and J.G. Vos Covalent linkage of ruthenium polypyridyl compounds to poly(l-lysine), albumins, and immunoglobulin-G Bioconjug. Chem. 3 1992 285 290
30. H.J. Youn, E. Terpetschnig, H. Szmacinski, and J.R. Lakowicz Fluorescence energy-transfer immunoassay based on a long-lifetime luminescent metal-ligand complex Anal. Biochem. 232 1995 24 30
31. J.M. Chalker, G.J.L. Bernardes, Y.A. Lin, and B.G. Davis Chemical modification of proteins at cysteine: opportunities in chemistry and biology Chem. Asian J. 4 2009 630 640
32. E. Terpetschnig, J.D. Dattelbaum, H. Szmacinski, and J.R. Lakowicz Synthesis and spectral characterization of a thiol-reactive long-lifetime Ru(II) complex Anal. Biochem. 251 1997 241 245
33. J. Weh, A. Duerkop, and O.S. Wolfbeis A resonance energy transfer immunoassay based on a thiol-reactive ruthenium donor dye and a longwave-emitting acceptor Chembiochem 8 2007 122 128
34. L. Geren, B. Durham, and F. Millett Use of ruthenium photoreduction techniques to study electron transfer in cytochrome oxidase Methods Enzymol. 456 2009 507 520 456
35. F.N. Castellano, J.D. Dattelbaum, and J.R. Lakowicz Long-lifetime Ru(II) complexes as labeling reagents for sulfhydryl groups Anal. Biochem. 255 1998 165 170
36. S. Dwaraknath, N.H. Tran, T. Dao, A. Colbert, S. Mullen, A. Nguyen, A. Cortez, and L. Cheruzel A facile and versatile methodology for cysteine specific labeling of proteins with octahedral polypyridyl d(6) metal complexes J. Inorg. Biochem. 136 2014 154 160
37. I. Hamachi, S. Tsukiji, S. Shinkai, and S. Oishi Direct observation of the ferric-porphyrin cation radical as an intermediate in the phototriggered oxidation of ferric- to ferryl-heme tethered to Ru(bpy)(3) in reconstituted myoglobin J. Am. Chem. Soc. 121 1999 5500 5506
38. C.E. Immoos, A.J. Di Bilio, M.S. Cohen, W. Van der Veer, H.B. Gray, and P.J. Farmer Electron-transfer chemistry of Ru-linker-(heme)-modified myoglobin: rapid intraprotein reduction of a photogenerated porphyrin cation radical Inorg. Chem. 43 2004 3593 3596
39. E.C. Glazer, Y.H.L. Nguyen, H.B. Gray, and D.B. Goodin Probing inducible nitric oxide synthase with a pterin-ruthenium(II) sensitizer wire Angew. Chem. Int. Ed. 47 2008 898 901
40. M.E. Ener, Y.T. Lee, J.R. Winkler, H.B. Gray, and L. Cheruzel Photooxidation of cytochrome P450-BM3 Proc. Natl. Acad. Sci. USA 107 2010 18783 18786
41. N.H. Tran, D. Nguyen, S. Dwaraknath, S. Mahadevan, G. Chavez, A. Nguyen, T. Dao, S. Mullen, T.A. Nguyen, and L.E. Cheruzel An efficient light-driven P450 BM3 biocatalyst J. Am. Chem. Soc. 135 2013 14484 14487
42. H. Szmacinski, F.N. Castellano, E. Terpetschnig, J.D. Dattelbaum, J.R. Lakowicz, and G.J. Meyer Long-lifetime Ru(II) complexes for the measurement of high molecular weight protein hydrodynamics BBA-Protein Struct. Mol. 1383 1998 151 159
43. L.E. Roth, J.C. Nguyen, and F.A. Tezcan ATP- and Iron-protein-independent activation of nitrogenase catalysis by light J. Am. Chem. Soc. 132 2010 13672 13674
44. C. Shih, A.K. Museth, M. Abrahamsson, A.M. Blanco-Rodriguez, A.J. Di Bilio, J. Sudhamsu, B.R. Crane, K.L. Ronayne, M. Towrie, A. Vlcek, J.H. Richards, J.R. Winkler, and H.B. Gray Tryptophan-accelerated electron flow through proteins Science 320 2008 1760 1762
45. I.J. Chang, H.B. Gray, and M. Albin Identification of chemical modification sites on metalloproteins by capillary electrophoresis Anal. Biochem. 212 1993 24 27
46. J.R. Winkler, B.G. Malmstrom, and H.B. Gray Rapid electron injection into multisite metalloproteins - intramolecular electron-transfer in cytochrome-oxidase Biophys. Chem. 54 1995 199 209
47. F. Millett, J. Havens, S. Rajagukguk, and B. Durham Design and use of photoactive ruthenium complexes to study electron transfer within cytochrome bc(1) and from cytochrome bc(1) to cytochrome c BBA-Bioenerg. 1827 2013 1309 1319
48. S. Yoshikawa, and A. Shimada Reaction mechanism of cytochrome c oxidase Chem. Rev. 115 2015 1936 1989
49. S.Y. Reece, J.M. Hodgkiss, J. Stubbe, and D.G. Nocera Proton-coupled electron transfer: the mechanistic underpinning for radical transport and catalysis in biology Philos. Trans. Soc. B 361 2006 1351 1364
50. J.L. Dempsey, J.R. Winkler, and H.B. Gray Proton-coupled electron flow in protein redox machines Chem. Rev. 110 2010 7024 7039
51. J. Stubbe, D.G. Nocera, C.S. Yee, and M.C.Y. Chang Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer? Chem. Rev. 103 2003 2167 2201
52. J. Berglund, T. Pascher, J.R. Winkler, and H.B. Gray Photoinduced oxidation of horseradish peroxidase J. Am. Chem. Soc. 119 1997 2464 2469
53. D.W. Low, J.R. Winkler, and H.B. Gray Photoinduced oxidation of microperoxidase-8: generation of ferryl and cation-radical porphyrins J. Am. Chem. Soc. 118 1996 117 120
54. A.R. Dunn, I.J. Dmochowski, J.R. Winkler, and H.B. Gray Nanosecond photoreduction of cytochrome P450cam by channel-specific Ru-diimine electron tunneling wires J. Am. Chem. Soc. 125 2003 12450 12456
55. J.J. Wilker, I.J. Dmochowski, J.H. Dawson, J.R. Winkler, and H.B. Gray Substrates for rapid delivery of electrons and holes to buried active sites in proteins Angew. Chem. Int. Ed. 38 1999 90 92
56. D.B. Langley, D.E. Brown, L.E. Cheruzel, S.M. Contakes, A.P. Duff, K.M. Hilmer, D.M. Dooley, H.B. Gray, J.M. Guss, and H.C. Freeman Enantiomer-specific binding of ruthenium(II) molecular wires by the amine oxidase of Arthrobacter globiformis J. Am. Chem. Soc. 130 2008 8069 8078
57. M.T. Green, J.H. Dawson, and H.B. Gray Oxoiron(IV) in chloroperoxidase compound II is basic: implications for P450 chemistry Science 304 2004 1653 1656
58. R. Margalit, I. Pecht, and H.B. Gray Oxidation reduction catalytic activity of a pentaammineruthenium(Iii) derivative of sperm whale myoglobin J. Am. Chem. Soc. 105 1983 301 302
59. W. Lubitz, H. Ogata, O. Rudiger, and E. Reijerse Hydrogenases Chem. Rev. 114 2014 4081 4148
60. P.W. King Designing interfaces of hydrogenase-nanomaterial hybrids for efficient solar conversion BBA-Bioenerg. 1827 2013 949 957
61. I. Okura, and N. Kimthuan Kinetic-studies of photoinduced methyl viologen reduction with ruthenium complexes and hydrogen evolution from water by hydrogenase J. Chem. Soc. Farad. 77 1981 1411 1415
62. N. Asakura, T. Hiraishi, T. Kamachi, and I. Okura Photoinduced hydrogen evolution with cytochrome c(3)-viologen-ruthenium(II) triad complex and hydrogenase J. Mol. Catal. 172 2001 1 7
63. M. Ihara, H. Nishihara, K.S. Yoon, O. Lenz, B. Friedrich, H. Nakamoto, K. Kojima, D. Honma, T. Kamachi, and I. Okura Light-driven hydrogen production by a hybrid complex of a [NiFe]-hydrogenase and the cyanobacterial photosystem I Photochem. Photobiol. 82 2006 676 682
64. T. Noji, M. Kondo, T. Jin, T. Yazawa, H. Osuka, Y. Higuchi, M. Nango, S. Itoh, and T. Dewa Light-driven hydrogen production by hydrogenases and a ru-complex inside a nanoporous glass plate under aerobic external conditions J. Phys. Chem. Lett. 5 2014 2402 2407
65. B.L. Greene, C.A. Joseph, M.J. Maroney, and R.B. Dyer Direct evidence of active-site reduction and photodriven catalysis in sensitized hydrogenase assemblies J. Am. Chem. Soc. 134 2012 11108 11111
66. E. Reisner, J.C. Fontecilla-Camps, and F.A. Armstrong Catalytic electrochemistry of a [NiFeSe]-hydrogenase on TiO2 and demonstration of its suitability for visible-light driven H-2 production Chem. Commun. 2009 550 552
67. E. Reisner, D.J. Powell, C. Cavazza, J.C. Fontecilla-Camps, and F.A. Armstrong Visible Light-driven H-2 production by hydrogenases attached to dye-sensitized TiO2 nanoparticles J. Am. Chem. Soc. 131 2009 18457 18466
68. 2 to CO by enzyme-modified TiO2 nanoparticles using visible light J. Am. Chem. Soc. 132 2010 2132 2135
69. 2 photoreduction at enzyme-modified metal oxide nanoparticles Energy Environ. Sci. 4 2011 2393 2399
70. B.M. Hoffman, D. Lukoyanov, Z.Y. Yang, D.R. Dean, and L.C. Seefeldt Mechanism of nitrogen fixation by nitrogenase: the next stage Chem. Rev. 114 2014 4041 4062
71. F.A. Tezcan, J.T. Kaiser, D. Mustafi, M.Y. Walton, J.B. Howard, and D.C. Rees Nitrogenase complexes: multiple docking sites for a nucleotide switch protein Science 309 2005 1377 1380
72. L.E. Roth, and F.A. Tezcan ATP-uncoupled, six-electron photoreduction of hydrogen cyanide to methane by the molybdenum-iron protein J. Am. Chem. Soc. 134 2012 8416 8419
73. A. Ruggi, F.W.B. van Leeuwen, and A.H. Velders Interaction of dioxygen with the electronic excited state of Ir(III) and Ru(II) complexes: principles and biomedical applications Coord. Chem. Rev. 255 2011 2542 2554
74. S.M. Jones, and E.I. Solomon Electron transfer and reaction mechanism of laccases Cell. Mol. Life Sci. 72 2015 869 883
75. T. Kudanga, and M. Le Roes-Hill Laccase applications in biofuels production: current status and future prospects Appl. Microbiol. Biot. 98 2014 6525 6542
76. F.P. Cardoso, S.A. Neto, L.B. Crepaldi, S. Nikolaou, V.P. Barros, and A.R. De Andrade Biocathodes for enzymatic biofuel cells using laccase and different redox mediators entrapped in polypyrrole matrix J. Electrochem. Soc. 161 2014 F445 F450
77. S.C. Barton, H.H. Kim, G. Binyamin, Y.C. Zhang, and A. Heller The "wired" laccase cathode: high current density electroreduction of O-2 to water at + 0.7 V (NHE) at pH 5 J. Am. Chem. Soc. 123 2001 5802 5803
78. N. Mano, V. Soukharev, and A. Heller A laccase-wiring redox hydrogel for efficient catalysis of O-2 electroreduction J. Phys. Chem. B 110 2006 11180 11187
79. T. Lazarides, I.V. Sazanovich, A.J. Simaan, M.C. Kafentzi, M. Delor, Y. Mekmouche, B. Faure, M. Reglier, J.A. Weinstein, A.G. Coutsolelos, and T. Tron Visible light-driven O-2 reduction by a porphyrin-laccase system J. Am. Chem. Soc. 135 2013 3095 3103
80. A.J. Simaan, Y. Mekmouche, C. Herrero, P. Moreno, A. Aukauloo, J.A. Delaire, M. Reglier, and T. Tron Photoinduced multielectron transfer to a multicopper oxidase resulting in dioxygen reduction into water Chem. Eur. J. 17 2011 11743 11746
81. V.B. Urlacher, and M. Girhard Cytochrome P450 monooxygenases: an update on perspectives for synthetic application Trends Biotechnol. 30 2012 26 36
82. I.G. Denisov, T.M. Makris, S.G. Sligar, and I. Schlichting Structure and chemistry of cytochrome P450 Chem. Rev. 105 2005 2253 2277
83. C.J.C. Whitehouse, S.G. Bell, and L.L. Wong P450(BM3) (CYP102A1): connecting the dots Chem. Soc. Rev. 41 2012 1218 1260
84. N.H. Tran, N. Huynh, T. Bui, Y. Nguyen, P. Huynh, M.E. Cooper, and L.E. Cheruzel Light-initiated hydroxylation of lauric acid using hybrid P450 BM3 enzymes Chem. Commun. 47 2011 11936 11938
85. N.H. Tran, N. Huynh, G. Chavez, A. Nguyen, S. Dwaraknath, T.A. Nguyen, M. Nguyen, and L. Cheruzel A series of hybrid P450 BM3 enzymes with different catalytic activity in the light-initiated hydroxylation of lauric acid J. Inorg. Biochem. 115 2012 50 56
86. M. Kato, D. Nguyen, M. Gonzalez, A. Cortez, S.E. Mullen, and L.E. Cheruzel Regio- and stereoselective hydroxylation of 10-undecenoic acid with a light-driven P450 BM3 biocatalyst yielding a valuable synthon for natural product synthesis Bioorg. Med. Chem. 22 2014 5687 5691
87. Y. Ma, X.L. Wang, Y.S. Jia, X.B. Chen, H.X. Han, and C. Li Titanium dioxide-based nanomaterials for photocatalytic fuel generations Chem. Rev. 114 2014 9987 10043
88. M. Filice, and J.M. Palomo Cascade reactions catalyzed by bionanostructures ACS Catal. 4 2014 1588 1598
89. J.H. Kim, D.H. Nam, and C.B. Park Nanobiocatalytic assemblies for artificial photosynthesis Curr. Opin. Biotechnol. 28 2014 1 9
90. M. Mifsud, S. Gargiulo, S. Iborra, I.W.C.E. Arends, F. Hollmann, and A. Corma Photobiocatalytic chemistry of oxidoreductases using water as the electron donor Nat Commun 5 2014
91. J.H. Park, S.H. Lee, G.S. Cha, D.S. Choi, D.H. Nam, J.H. Lee, J.K. Lee, C.H. Yun, K.J. Jeong, and C.B. Park cofactor-free light-driven whole-cell cytochrome P450 catalysis Angew. Chem. Int. Ed. 54 2015 969 973