Electron transfer pathways and spin–spin interactions in Mo- and Cu-containing oxidoreductases

Coordination Chemistry Reviews - Tập 449 - Trang 214202 - 2021
Pablo J. González1, María G. Rivas1, Felix M. Ferroni1, Alberto C. Rizzi1, Carlos D. Brondino1
1Departamento de Física, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, and CONICET, S3000ZAA Santa Fe, Argentina

Tài liệu tham khảo

Berg, 2012 Waldron, 2009, Metalloproteins and metal sensing, Nature, 460, 823, 10.1038/nature08300 Davidson, 2008, Protein control of true, gated, and coupled electron transfer reactions, Acc Chem Res, 41, 730, 10.1021/ar700252c Liu, 2014, Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers, Chem Rev, 114, 4366, 10.1021/cr400479b Brondino, 2006, Structural and electron paramagnetic resonance (EPR) studies of mononuclear molybdenum enzymes from sulfate-reducing bacteria, Acc Chem Res, 39, 788, 10.1021/ar050104k Yilmazer, 2020, Structural insights into the NAD(+)-dependent formate dehydrogenase mechanism revealed from the NADH complex and the formate NAD(+) ternary complex of the Chaetomium thermophilum enzyme, J Struct Biol, 212, 10.1016/j.jsb.2020.107657 Wushur, 2015, The catalytic reaction mechanism of drosophilid alcohol dehydrogenases, Perspectives in Science, 4, 46, 10.1016/j.pisc.2014.12.008 Plapp, 2010, Conformational changes and catalysis by alcohol dehydrogenase, Arch Biochem Biophys, 493, 3, 10.1016/j.abb.2009.07.001 Marcus, 1985, Electron transfers in chemistry and biology, Biochim Biophys Acta- Reviews on, Bioenergetics, 811, 265 Hopfield, 1974, Electron transfer between biological molecules by thermally activated tunneling, Proc Natl Acad Sci USA, 71, 3640, 10.1073/pnas.71.9.3640 Moser, 2010, Guidelines for tunneling in enzymes, Biochim Biophys Acta, 1797, 1573, 10.1016/j.bbabio.2010.04.441 Page, 2003, Mechanism for electron transfer within and between proteins, Curr Opin Chem Biol, 7, 551, 10.1016/j.cbpa.2003.08.005 Hille, 2014, The mononuclear molybdenum enzymes, Chem Rev, 114, 3963, 10.1021/cr400443z Maia, 2015, Molybdenum and tungsten-dependent formate dehydrogenases, J Biol Inorg Chem, 20, 287, 10.1007/s00775-014-1218-2 Nojiri, 2017, Structure and Function of Copper Nitrite Reductase, 91 Horrell, 2017, Recent structural insights into the function of copper nitrite reductases, Metallomics, 9, 1470, 10.1039/C7MT00146K 1990 Rizzi, 2016, EPR as a Tool for Study of Isolated and Coupled Paramagnetic Centers in Coordination Compounds and Macromolecules of Biological Interest, Eur J Inorg Chem, 2016, 192, 10.1002/ejic.201501111 Formosinho, 2012 Marcus, 2006, Enzymatic catalysis and transfers in solution. I. Theory and computations, a unified view, J Chem Phys, 125, 10.1063/1.2372496 Marcus, 2006, Summarizing lecture: factors influencing enzymatic H-transfers, analysis of nuclear tunnelling isotope effects and thermodynamic versus specific effects, Philos Trans R Soc Lond B Biol Sci, 361, 1445, 10.1098/rstb.2006.1873 Darrouzet, 2001, Large scale domain movement in cytochrome bc(1): a new device for electron transfer in proteins, Trends Biochem Sci, 26, 445, 10.1016/S0968-0004(01)01897-7 Moser, 1992, Nature of biological electron transfer, Nature, 355, 796, 10.1038/355796a0 Moser, 2000, Electron transfer in natural proteins theory and design, Subcell Biochem, 35, 1, 10.1007/0-306-46828-X_1 Moser, 1995, Biological electron transfer, J Bioenerg Biomembr, 27, 263, 10.1007/BF02110096 Beratan, 1992, Electron-tunneling pathways in proteins, Science, 258, 1740, 10.1126/science.1334572 Onuchic, 1992, Pathway analysis of protein electron-transfer reactions, Annu Rev Biophys Biomol Struct, 21, 349, 10.1146/annurev.bb.21.060192.002025 Page, 1999, Natural engineering principles of electron tunnelling in biological oxidation-reduction, Nature, 402, 47, 10.1038/46972 Gray, 2003, Electron tunneling through proteins, Q Rev Biophys, 36, 341, 10.1017/S0033583503003913 Winkler, 2014, Long-range electron tunneling, J Am Chem Soc, 136, 2930, 10.1021/ja500215j Winkler, 2014, Electron flow through metalloproteins, Chem Rev, 114, 3369, 10.1021/cr4004715 Winkler, 1997, Effects of folding on metalloprotein active sites, Proc Natl Acad Sci USA, 94, 4246, 10.1073/pnas.94.9.4246 Gray, 2000, Copper coordination in blue proteins, J Biol Inorg Chem, 5, 551, 10.1007/s007750000146 Simonson, 2002, Gaussian fluctuations and linear response in an electron transfer protein, Proc Natl Acad Sci USA, 99, 6544, 10.1073/pnas.082657099 Dobbek, 1999, Crystal structure and mechanism of CO dehydrogenase, a molybdo iron-sulfur flavoprotein containing S-selanylcysteine, Proc Natl Acad Sci USA, 96, 8884, 10.1073/pnas.96.16.8884 Rothery, 2015, Shifting the metallocentric molybdoenzyme paradigm: the importance of pyranopterin coordination, J Biol Inorg Chem, 20, 349, 10.1007/s00775-014-1194-6 Rothery, 2012, Pyranopterin conformation defines the function of molybdenum and tungsten enzymes, Proc Natl Acad Sci USA, 109, 14773, 10.1073/pnas.1200671109 Gonzalez, 2013, Periplasmic nitrate reductases and formate dehydrogenases: Biological control of the chemical properties of Mo and W for fine tuning of reactivity, substrate specificity and metabolic role, Coord Chem Rev, 257, 315, 10.1016/j.ccr.2012.05.020 Ellis, 2001, Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 A and 2.03 A, Structure, 9, 125, 10.1016/S0969-2126(01)00566-4 Conrads, 2002, The active site of arsenite oxidase from Alcaligenes faecalis, J Am Chem Soc, 124, 11276, 10.1021/ja027684q Seiffert, 2007, Structure of the non-redox-active tungsten/[4Fe:4S] enzyme acetylene hydratase, Proc Natl Acad Sci USA, 104, 3073, 10.1073/pnas.0610407104 Messerschmidt, 2004, Crystal structure of pyrogallol-phloroglucinol transhydroxylase, an Mo enzyme capable of intermolecular hydroxyl transfer between phenols, Proc Natl Acad Sci USA, 101, 11571, 10.1073/pnas.0404378101 Mukund, 1991, The novel tungsten-iron-sulfur protein of the hyperthermophilic archaebacterium, Pyrococcus furiosus, is an aldehyde ferredoxin oxidoreductase, Evidence for its participation in a unique glycolytic pathway, J Biol Chem, 266, 14208 Dhawan, 2000, Spectroscopic studies of the tungsten-containing formaldehyde ferredoxin oxidoreductase from the hyperthermophilic archaeon Thermococcus litoralis, J Biol Inorg Chem, 5, 313, 10.1007/PL00010660 Mukund, 1993, Characterization of a novel tungsten-containing formaldehyde ferredoxin oxidoreductase from the hyperthermophilic archaeon, Thermococcus litoralis, A role for tungsten in peptide catabolism, J Biol Chem, 268, 13592 Roy, 1999, Purification and molecular characterization of the tungsten-containing formaldehyde ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus: the third of a putative five-member tungstoenzyme family, J Bacteriol, 181, 1171, 10.1128/JB.181.4.1171-1180.1999 Chan, 1995, Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase, Science, 267, 1463, 10.1126/science.7878465 Hu, 1999, Formaldehyde ferredoxin oxidoreductase from Pyrococcus furiosus: the 1.85 A resolution crystal structure and its mechanistic implications, J Mol Biol, 286, 899, 10.1006/jmbi.1998.2488 Mukund, 1995, Glyceraldehyde-3-phosphate ferredoxin oxidoreductase, a novel tungsten-containing enzyme with a potential glycolytic role in the hyperthermophilic archaeon Pyrococcus furiosus, J Biol Chem, 270, 8389, 10.1074/jbc.270.15.8389 Roy, 2002, Characterization of a fourth tungsten-containing enzyme from the hyperthermophilic archaeon Pyrococcus furiosus, J Bacteriol, 184, 6952, 10.1128/JB.184.24.6952-6956.2002 Bevers, 2005, WOR5, a novel tungsten-containing aldehyde oxidoreductase from Pyrococcus furiosus with a broad substrate Specificity, J Bacteriol, 187, 7056, 10.1128/JB.187.20.7056-7061.2005 White, 1989, Carboxylic acid reductase: a new tungsten enzyme catalyses the reduction of non-activated carboxylic acids to aldehydes, Eur J Biochem, 184, 89, 10.1111/j.1432-1033.1989.tb14993.x D. Rauh, A. Graentzdoerffer, K. Granderath, J.R. Andreesen, A. Pich, Tungsten-containing aldehyde oxidoreductase of Eubacterium acidaminophilum, Eur J Biochem 271 (2004) 212-219. Hensgens, 1995, Purification and characterization of a benzylviologen-linked, tungsten-containing aldehyde oxidoreductase from Desulfovibrio gigas, J Bacteriol, 177, 6195, 10.1128/jb.177.21.6195-6200.1995 Arndt, 2019, Characterization of an Aldehyde Oxidoreductase From the Mesophilic Bacterium Aromatoleum aromaticum EbN1, a Member of a New Subfamily of Tungsten-Containing Enzymes, Front Microbiol, 10, 71, 10.3389/fmicb.2019.00071 Bevers, 2009, The bioinorganic chemistry of tungsten, Coord Chem Rev, 253, 269, 10.1016/j.ccr.2008.01.017 Hagen, 2011, Cellular uptake of molybdenum and tungsten, Coord Chem Rev, 255, 1117, 10.1016/j.ccr.2011.02.009 Romo, 1995, Crystal Structure of the Xanthine Oxidase-Related Aldehyde Oxido-Reductase from D. gigas, Science, 270, 1170, 10.1126/science.270.5239.1170 Rebelo, 2001, Structure refinement of the aldehyde oxidoreductase from Desulfovibrio gigas (MOP) at 1.28 Å, J Biol Inor Chem, 6, 791, 10.1007/s007750100255 Enroth, 2000, Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion, Proc Natl Acad Sci USA, 97, 10723, 10.1073/pnas.97.20.10723 Dias, 1999, Crystal structure of the first dissimilatory nitrate reductase at 1.9 A solved by MAD methods, Structure, 7, 65, 10.1016/S0969-2126(99)80010-0 Najmudin, 2008, Periplasmic nitrate reductase revisited: a sulfur atom completes the sixth coordination of the catalytic molybdenum, J Biol Inorg Chem, 13, 737, 10.1007/s00775-008-0359-6 Coelho, 2007, Heterodimeric nitrate reductase (NapAB) from Cupriavidus necator H16: purification, crystallization and preliminary X-ray analysis, Acta Crystallogr Sect F Struct Biol Cryst Commun, 63, 516, 10.1107/S1744309107022129 Kappler, 2005, Molecular Basis of Intramolecular Electron Transfer in Sulfite-oxidizing Enzymes Is Revealed by High Resolution Structure of a Heterodimeric Complex of the Catalytic Molybdopterin Subunit and a c-Type Cytochrome Subunit, J Biol Chem, 280, 24999, 10.1074/jbc.M503237200 Emesh, 2009, Intramolecular electron transfer in sulfite-oxidizing enzymes: elucidating the role of a conserved active site arginine, Biochemistry, 48, 2156, 10.1021/bi801553q Doonan, 2006, Structure of the active site of sulfite dehydrogenase from Starkeya novella, Inorg Chem, 45, 7488, 10.1021/ic0607944 Kappler, 2006, Kinetic and structural evidence for the importance of Tyr236 for the integrity of the Mo active site in a bacterial sulfite dehydrogenase, Biochemistry, 45, 9696, 10.1021/bi060058b Chemistry, 2004 Periyasamy, 2007, The dithiolene ligand–'innocent' or 'non-innocent'? A theoretical and experimental study of some cobalt-dithiolene complexes, Faraday Discuss 135, 135, 469, 10.1039/B607144A Matz, 2010, Noninnocent dithiolene ligands: a new oxomolybdenum complex possessing a donor-acceptor dithiolene ligand, J Am Chem Soc, 132, 7830, 10.1021/ja100220x Matz, 2011, Study of molybdenum(4+) quinoxalyldithiolenes as models for the noninnocent pyranopterin in the molybdenum cofactor, Inorg Chem, 50, 9804, 10.1021/ic200783a Romao, 1997, Crystal structure and mechanism of action of the xanthine oxidase-related aldehyde oxidoreductase from Desulfovibrio gigas, Biochem Soc Trans, 25, 755, 10.1042/bst0250755 Marangon, 2013, Kinetic and structural studies of aldehyde oxidoreductase from Desulfovibrio gigas reveal a dithiolene-based chemistry for enzyme activation and inhibition by H2O2, PLoS One, 8, e83234, 10.1371/journal.pone.0083234 Nishino, 1983, Reversible interconversion between sulfo and desulfo xanthine oxidase in a system containing rhodanese, thiosulfate, and sulfhydryl reagent, Proc Natl Acad Sci USA, 80, 1826, 10.1073/pnas.80.7.1826 Santos-Silva, 2009, Kinetic, structural, and EPR studies reveal that aldehyde oxidoreductase from Desulfovibrio gigas does not need a sulfido ligand for catalysis and give evidence for a direct Mo-C interaction in a biological system, J Am Chem Soc, 131, 7990, 10.1021/ja809448r Adamson, 2015, Electrochemical evidence that pyranopterin redox chemistry controls the catalysis of YedY, a mononuclear Mo enzyme, Proc Natl Acad Sci USA, 112, 14506, 10.1073/pnas.1516869112 Rothery, 2010, Protein crystallography reveals a role for the FS0 cluster of Escherichia coli nitrate reductase A (NarGHI) in enzyme maturation, J Biol Chem, 285, 8801, 10.1074/jbc.M109.066027 Trieber, 1994, Multiple pathways of electron transfer in dimethyl sulfoxide reductase of Escherichia coli, J Biol Chem, 269, 7103, 10.1016/S0021-9258(17)37253-8 Tang, 2011, Correct assembly of iron-sulfur cluster FS0 into Escherichia coli dimethyl sulfoxide reductase (DmsABC) is a prerequisite for molybdenum cofactor insertion, J Biol Chem, 286, 15147, 10.1074/jbc.M110.213306 Tang, 2013, A variant conferring cofactor-dependent assembly of Escherichia coli dimethylsulfoxide reductase, Biochim Biophys Acta, 1827, 730, 10.1016/j.bbabio.2013.02.009 Wu, 2015, Pyranopterin Coordination Controls Molybdenum Electrochemistry in Escherichia coli Nitrate Reductase, J Biol Chem, 290, 25164, 10.1074/jbc.M115.665422 Elliott, 2004, Voltammetric studies of the catalytic mechanism of the respiratory nitrate reductase from Escherichia coli: how nitrate reduction and inhibition depend on the oxidation state of the active site, Biochemistry, 43, 799, 10.1021/bi035869j Frangioni, 2004, In Rhodobacter sphaeroides respiratory nitrate reductase, the kinetics of substrate binding favors intramolecular electron transfer, J Am Chem Soc, 126, 1328, 10.1021/ja0384072 Heffron, 2001, Determination of an optimal potential window for catalysis by E. coli dimethyl sulfoxide reductase and hypothesis on the role of Mo(V) in the reaction pathway, Biochemistry, 40, 3117, 10.1021/bi002452u George, 1985, Complexes with halide and other anions of the molybdenum centre of nitrate reductase from Escherichia coli, Biochem J, 227, 925, 10.1042/bj2270925 Marangon, 1817, Substrate-dependent modulation of the enzymatic catalytic activity: reduction of nitrate, chlorate and perchlorate by respiratory nitrate reductase from Marinobacter hydrocarbonoclasticus 617, Biochim Biophys Acta, 2012, 1072 Lowe, 1978, Magnetic coupling of the molybdenum and iron-sulphur centres in xanthine oxidase and xanthine dehydrogenases, Biochem J, 169, 471, 10.1042/bj1690471 Lowe, 1972, Spin–spin interaction between molybdenum and one of the iron–sulphur systems of xanthine oxidase and its relevance to the enzymic mechanism, Biochem J, 130, 239, 10.1042/bj1300239 Boer, 2004, X-ray Crystal Structure and EPR Spectra of “Arsenite-Inhibited” Desulfovibrio gigas Aldehyde Dehydrogenase: A Member of the Xanthine Oxidase Family, J Am Chem Soc, 126, 8614, 10.1021/ja0490222 Thapper, 2007, Correlating EPR and X-ray structural analysis of arsenite-inhibited forms of aldehyde oxidoreductase, J Biol Inorg Chem, 12, 353, 10.1007/s00775-006-0191-9 Hille, 2013, The molybdenum oxotransferases and related enzymes, Dalton Trans, 42, 3029, 10.1039/c2dt32376a Maia, 2018 Smith, 1974, The determination of structural properties of dimeric transition metal ion complexes from epr spectra, Coord Chem Rev, 13, 173, 10.1016/S0010-8545(00)80255-6 Gracia, 2020, What Are the Electrons Really Doing in Molecules? A Space-Time Picture, European, Journal of Physics Education, 11, 2020 Heisenberg, 1928, Zur Theorie des Ferromagnetismus, Zeitschrift für Physik, 49, 619, 10.1007/BF01328601 Dirac, 1958 van Vleck, 1932 Anderson, 1959, New Approach to the Theory of Superexchange Interactions, Phys Rev, 115, 2, 10.1103/PhysRev.115.2 Kahn, 1985, Dinuclear complexes with predictable magnetic properties, Angew Chem Int Ed Engl, 24, 834, 10.1002/anie.198508341 González, 2009, EPR studies of the Mo-enzyme aldehyde oxidoreductase from Desulfovibrio gigas: An application of the Bloch-Wangsness-Redfield theory to a system containing weakly-coupled paramagnetic redox centers with different relaxation rates, J Inorg Biochem, 103, 1342, 10.1016/j.jinorgbio.2009.06.006 Gómez, 2015, Isotropic Exchange Interaction between Mo and the Proximal FeS Center in the Xanthine Oxidase Family Member Aldehyde Oxidoreductase from Desulfovibrio gigas on Native and Polyalcohol Inhibited Samples: An EPR and QM/MM Study, J Biol Inorg Chem, 20, 233, 10.1007/s00775-014-1204-8 Bertrand, 1994, Biological polynuclear clusters coupled by magnetic interactions: From the point dipole approximation to a local spin model, J Am Chem Soc, 116, 3078, 10.1021/ja00086a042 Caldeira, 2000, Analysis of the electron paramagnetic resonance properties of the [2Fe-2S]1+ centers in molybdenum enzymes of the xanthine oxidase family: assignment of signals I and II, Biochemistry, 39, 2700, 10.1021/bi9921485 Hoffmann, 1994, Weak long-distance superexchange interaction and its temperature variations in copper(II) compounds studied by single crystal EPR, Appl Magn Reson, 7, 289, 10.1007/BF03162617 Neuman, 2010, Single Crystal EPR Study of the Dinuclear Cu(II) Complex [Cu(tda)(phen)]2·H2tda (tda = Thiodiacetate, phen = Phenanthroline): Influence of Weak Interdimeric Magnetic Interactions, J Phys Chem A, 114, 13069, 10.1021/jp108736p Desplanches, 2002, Exchange Coupling of Transition-Metal Ions through Hydrogen Bonding: A Theoretical Investigation, J Am Chem Soc, 124, 5197, 10.1021/ja0178160 Pérez, 2017, Exchange interaction between S = 1/2 centers bridged by multiple noncovalent interactions: Contribution of the individual chemical pathways to the magnetic coupling, Polyhedron, 123, 404, 10.1016/j.poly.2016.12.018 González, 2006, EPR and redox properties of periplasmic nitrate reductase from Desulfovibrio desulfuricans ATCC 27774, J Biol Inorg Chem, 11, 609, 10.1007/s00775-006-0110-0 Rivas, 2007, EPR characterization of the molybdenum(V) forms of formate dehydrogenase from Desulfovibrio desulfuricans ATCC 27774 upon formate reduction, J Inorg Biochem, 101, 1617, 10.1016/j.jinorgbio.2007.04.011 Correia, 2008, Biochemical and spectroscopic characterization of the membrane-bound nitrate reductase from Marinobacter hydrocarbonoclasticus 617, J Biol Inorg Chem, 13, 1321, 10.1007/s00775-008-0416-1 Brondino, 2004, Incorporation of either molybdenum or tungsten into formate dehydrogenase from Desulfovibrio alaskensis NCIMB 13491, EPR assignment of the proximal iron-sulfur cluster to the pterin cofactor in formate dehydrogenases from sulfate-reducing bacteria, J Biol Inorg Chem, 9, 145 Niks, 2016, Spectroscopic and Kinetic Properties of the Molybdenum-containing, NAD+-dependent Formate Dehydrogenase from Ralstonia eutropha, J Biol Chem, 291, 1162, 10.1074/jbc.M115.688457 Jacques, 2014, Reductive activation in periplasmic nitrate reductase involves chemical modifications of the Mo-cofactor beyond the first coordination sphere of the metal ion, Biochim Biophys Acta, 1837, 277, 10.1016/j.bbabio.2013.10.013 Rothery, 1999, Interactions between the Molybdenum Cofactor and Iron-Sulfur Clusters of Escherichia coli Dimethylsulfoxide Reductase*, J Biol Chem, 274, 13002, 10.1074/jbc.274.19.13002 Andrade, 2000, Aldehyde oxidoreductase activity in Desulfovibrio alaskensis NCIMB 13491, Eur J Biochem, 267, 2054, 10.1046/j.1432-1327.2000.01209.x Calvo, 2000, EPR Study of the Molecular and Electronic Structure of the Semiquinone Biradical QA-•QB-• in Photosynthetic Reaction Centers from Rhodobacter sphaeroides, J Am Chem Soc, 122, 7327, 10.1021/ja000399r Metz, 2009, Reductive half-reaction of aldehyde oxidoreductase toward acetaldehyde: a combined QM/MM study, J Am Chem Soc, 131, 4628, 10.1021/ja805938w Hitchman, 1970, 4 Solomon, 2006, Spectroscopic methods in bioinorganic chemistry: blue to green to red copper sites, Inorg Chem, 45, 8012, 10.1021/ic060450d Strange, 1999, Structural and kinetic evidence for an ordered mechanism of copper nitrite reductase1, J Mol Biol, 287, 1001, 10.1006/jmbi.1999.2648 Boulanger, 2000, Catalytic Roles for Two Water Bridged Residues (Asp-98 and His-255) in the Active Site of Copper-containing Nitrite Reductase, J Biol Chem, 275, 23957, 10.1074/jbc.M001859200 Cristaldi, 2018, Study of the Cys-His bridge electron transfer pathway in a copper-containing nitrite reductase by site-directed mutagenesis, spectroscopic, and computational methods, Biochim Biophys Acta Gen Subj, 1862, 752, 10.1016/j.bbagen.2017.10.011 Suzuki, 1994, Pulse Radiolysis Studies on Nitrite Reductase from Achromobacter cycloclastes IAM 1013: Evidence for Intramolecular Electron Transfer from Type 1 Cu to Type 2 Cu, J Am Chem Soc, 116, 11145, 10.1021/ja00103a035 Fukuda, 2016, Redox-coupled proton transfer mechanism in nitrite reductase revealed by femtosecond crystallography, Proc Natl Acad Sci USA, 113, 2928, 10.1073/pnas.1517770113 Cristaldi, 2020, Heterologous production and functional characterization of Bradyrhizobium japonicum copper-containing nitrite reductase and its physiological redox partner cytochrome c550, Metallomics, 12, 2084, 10.1039/d0mt00177e Ferroni, 2014, Pseudoazurin from Sinorhizobium meliloti as an electron donor to copper-containing nitrite reductase: influence of the redox partner on the reduction potentials of the enzyme copper centers, J Biol Inorg Chem, 19, 913, 10.1007/s00775-014-1124-7 Zumft, 1997, Cell biology and molecular basis of denitrification, Microbiol Mol Biol Rev, 61, 533 Berry, 2003, Probing the role of axial methionine in the blue copper center of azurin with unnatural amino acids, J Am Chem Soc, 125, 8760, 10.1021/ja029699u Suzuki, 2000, Metal coordination and mechanism of multicopper nitrite reductase, Acc Chem Res, 33, 728, 10.1021/ar9900257 Kataoka, 2000, Functional analysis of conserved aspartate and histidine residues located around the type 2 copper site of copper-containing nitrite reductase, J Biochem, 127, 345, 10.1093/oxfordjournals.jbchem.a022613 Leferink, 2011, Proton-coupled electron transfer in the catalytic cycle of Alcaligenes xylosoxidans copper-dependent nitrite reductase, Biochemistry, 50, 4121, 10.1021/bi200246f Pinho, 2004, Copper-containing nitrite reductase from Pseudomonas chlororaphis DSM50135, Eur J Biochem, 271, 2361, 10.1111/j.1432-1033.2004.04155.x Leferink, 2012, Laser-flash photolysis indicates that internal electron transfer is triggered by proton uptake by Alcaligenes xylosoxidans copper-dependent nitrite reductase, FEBS J, 279, 2174, 10.1111/j.1742-4658.2012.08601.x Leferink, 2012, Gating mechanisms for biological electron transfer: integrating structure with biophysics reveals the nature of redox control in cytochrome P450 reductase and copper-dependent nitrite reductase, FEBS Lett, 586, 578, 10.1016/j.febslet.2011.07.003 Brenner, 2009, Demonstration of proton-coupled electron transfer in the copper-containing nitrite reductases, J Biol Chem, 284, 25973, 10.1074/jbc.M109.012245 Farver, 1998, The intramolecular electron transfer between copper sites of nitrite reductase: a comparison with ascorbate oxidase, FEBS Lett, 436, 239, 10.1016/S0014-5793(98)01120-X Suzuki, 1997, Deligeer, Spectroscopic characterization and intramolecular electron transfer processes of native and type 2 Cu-depleted nitrite reductases, JBIC Journal of Biological Inorganic Chemistry, 2, 265, 10.1007/s007750050132 Hough, 2005, Samar Hasnain, High Resolution Structural Studies of Mutants Provide Insights into Catalysis and Electron Transfer Processes in Copper Nitrite Reductase, J Mol Biol, 350, 300, 10.1016/j.jmb.2005.04.006 Ellis, 2004, Observation of an Unprecedented Cu Bis-His Site: Crystal Structure of the H129V Mutant of Nitrite Reductase, Inorg Chem, 43, 7591, 10.1021/ic048966p Kukimoto, 1994, X-ray Structure and Site-Directed Mutagenesis of a Nitrite Reductase from Alcaligenes faecalis S-6: Roles of Two Copper Atoms in Nitrite Reduction, Biochemistry, 33, 5246, 10.1021/bi00183a030 Hadt, 2014, Anisotropic covalency contributions to superexchange pathways in type one copper active sites, J Am Chem Soc, 136, 15034, 10.1021/ja508361h Ferroni, 2011, Study of the interaction of the catalytic copper center with nitrite and NO, J Inorg Biochem, 114, 8 Abraham, 1997, pH-dependence for binding a single nitrite ion to each type-2 copper centre in the copper-containing nitrite reductase of Alcaligenes xylosoxidans, Biochem J, 324, 511, 10.1042/bj3240511 Kobayashi, 1999, The pH-Dependent Changes of Intramolecular Electron Transfer on Copper-Containing Nitrite Reductase1, J Biochem, 126, 408, 10.1093/oxfordjournals.jbchem.a022465 Zhao, 2002, Catalytic Function and Local Proton Structure at the Type 2 Copper of Nitrite Reductase: The Correlation of Enzymatic pH Dependence, Conserved Residues, and Proton Hyperfine Structure, Biochemistry, 41, 7464 Ghosh, 2009, Spectroscopic and computational studies of nitrite reductase: proton induced electron transfer and backbonding contributions to reactivity, J Am Chem Soc, 131, 277, 10.1021/ja806873e Jacobson, 2007, pH Dependence of Copper Geometry, Reduction Potential, and Nitrite Affinity in Nitrite Reductase*, J Biol Chem, 282, 6347, 10.1074/jbc.M605746200 Ghosh, 2009, Thermodynamic equilibrium between blue and green copper sites and the role of the protein in controlling function, Proc Natl Acad Sci USA, 106, 4969, 10.1073/pnas.0900995106 Solomon, 2011, Recent advances in understanding blue copper proteins, Coord Chem Rev, 255, 774, 10.1016/j.ccr.2010.12.008 Choi, 2012, Characterization of electron tunneling and hole hopping reactions between different forms of MauG and methylamine dehydrogenase within a natural protein complex, Biochemistry, 51, 6942, 10.1021/bi300817d Warren, 2012, Electron hopping through proteins, Coord Chem Rev, 256, 2478, 10.1016/j.ccr.2012.03.032 Gray, 2005, Long-range electron transfer, Proc Natl Acad Sci USA, 102, 3534, 10.1073/pnas.0408029102 Sasaki, 2020, Structures of substrate- and product-bound forms of a multi-domain copper nitrite reductase shed light on the role of domain tethering in protein complexes, IUCrJ, 7, 557, 10.1107/S2052252520005230 Antonyuk, 2013, Structures of protein–protein complexes involved in electron transfer, Nature, 496, 123, 10.1038/nature11996 Sasaki, 2021, Reverse protein engineering of a novel 4-domain copper nitrite reductase reveals functional regulation by protein–protein interaction, The FEBS Journal, 288, 262, 10.1111/febs.15324 A. Tsuda, R. Ishikawa, H. Koteishi, K. Tange, Y. Fukuda, K. Kobayashi, T. Inoue, M. Nojiri, Structural and mechanistic insights into the electron flow through protein for cytochrome c-tethering copper nitrite reductase, J Biochem 154 (2013) 51-60. Nojiri, 2007, Structure and function of a hexameric copper-containing nitrite reductase, Proc Natl Acad Sci USA, 104, 4315, 10.1073/pnas.0609195104 Opperman, 2019, A three-domain copper-nitrite reductase with a unique sensing loop, IUCrJ, 6, 248, 10.1107/S2052252519000241 Shaik, 2011, Exchange-enhanced reactivity in bond activation by metal-oxo enzymes and synthetic reagents, Nat Chem, 3, 19, 10.1038/nchem.943 Biz, 2020, Catalysis Meets Spintronics; Spin Potentials Associated with Open-Shell Orbital Configurations Enhance the Activity of Pt3Co Nanostructures for Oxygen Reduction: A Density Functional Theory Study, ACS Applied Nano Materials, 3, 506, 10.1021/acsanm.9b02067 Naaman, 2019, Chiral molecules and the electron spin, Nature Reviews Chemistry, 3, 250, 10.1038/s41570-019-0087-1