Galactose Oxidase Models: Creation and Modification of Proton Transfer Coupled to Copper(II) Coordination Processes in Pro-Phenoxyl Ligands

Two tripodal ligands containing two pyridyl and one 4-(benzimidazol-2-yl)-2-tert-butylphenol (HL H ) and one 2-tertbutyl-4-(N-methylbenzimidazol-2-yl)phenol (HL Me ) unit have been synthesized. They possess a N 3 O donor set that is known to stabilize phenoxyl radicals more efficiently than the corresponding N 2 O 2 donor unit. Reaction of one molar equiv. of Cu(ClO 4 ) 2 ·6H 2 O with·HL H or HL Me affords the zwitterionic benzimidazolium phenolate complexes [Cu II (HL H )] 2+ and [Cu II (HL Me )] 2+ via a proton transfer reaction coupled to copper(II) coordination. Addition of HClO 4 to [Cu II (HL H )] 2+ and [Cu II (HL Me )] 2+ results in the formation of the benzimidazolium phenol complexes [Cu II (H 2 L H )] 3+ and [Cu II (H 2 L Me )] 2+ , while addition of NEt 3 affords the benzimidazol-phenolate complexes [Cu II (L H )] 2+ and [Cu II (L Me )] 2+ , respectively. The phenol's pK a is remarkably low due to the strong withdrawing effect of the benzimidazolium substituent. X-ray crystallographic analysis of the copper(II) complexes shows that deprotonation of the axial phenol forces the metal to move out of the square plane towards the oxygen atom, and one (or two) Cu-N pyridine equatorial bond length increases. The copper(II) phenoxyl species [Cu II (HL H )] 3+ and [Cu II (HL Me )] 3+ were prepared electrochemically, or by addition of two molar equiv. of copper(II) to HL H or HL Me . Under these conditions, radical formation has never been observed for tripodal ligands containing two pyridyl and one 2,4-di-tert-butylphenol group. This difference is explained in terms of the proton transfer mechanism and redox potentials.

[1]  P. Walton,et al.  Catalytic alcohol oxidation by an unsymmetrical 5-coordinate copper complex: electronic structure and mechanism. , 2006, Dalton transactions.

[2]  A. J. Blake,et al.  Phenoxyl radicals: H-bonded and coordinated to Cu(II) and Zn(II). , 2006, Dalton transactions.

[3]  S. Teat,et al.  (N-Benzyl-bis-N',N''-salicylidene)-cis-1,3,5-triaminocyclohexane copper(II): a novel catalyst for the aerobic oxidation of benzyl alcohol. , 2006, Dalton transactions.

[4]  K. Wieghardt,et al.  Biomimetic metal-radical reactivity: aerial oxidation of alcohols, amines, aminophenols and catechols catalyzed by transition metal complexes , 2005, Biological chemistry.

[5]  Hitoshi Yamamoto,et al.  Contribution of the intramolecular hydrogen bond to the shift of the pKa value and the oxidation potential of phenols and phenolate anions. , 2005, Organic & biomolecular chemistry.

[6]  R. Peralta,et al.  New mononuclear CuII and ZnII complexes capable of stabilizing phenoxyl radicals as models for the active form of galactose oxidase , 2005 .

[7]  T. D. Stack,et al.  Snapshots of a metamorphosing Cu(II) ground state in a galactose oxidase-inspired complex. , 2004, Inorganic chemistry.

[8]  Ian J. Rhile,et al.  One-electron oxidation of a hydrogen-bonded phenol occurs by concerted proton-coupled electron transfer. , 2004, Journal of the American Chemical Society.

[9]  F. Michel,et al.  Galactose oxidase models: solution chemistry, and phenoxyl radical generation mediated by the copper status. , 2004, Chemistry.

[10]  C. Philouze,et al.  Intramolecularly hydrogen-bonded versus copper(II) coordinated mono- and bis-phenoxyl radicals. , 2004, Dalton transactions.

[11]  M. Shiro,et al.  Model complexes of the active site of galactose oxidase. Effects of the metal ion binding sites , 2004 .

[12]  K. Wieghardt,et al.  Aerial oxidation of primary alcohols and amines catalyzed by Cu(II) complexes of 2,2'-selenobis(4,6-di-tert-butylphenol) providing [O,Se,O]-donor atoms. , 2004, Dalton transactions.

[13]  A. Mangrich,et al.  Copper(II) complexes with {N,N′,N,N′-bis[(2-hydroxybenzyl) (2-pyridylmethyl)]-1,3-propanediamine}—H2bbppn: their suitability as models for the inactive form of galactose oxidase , 2003 .

[14]  O. Reinaud,et al.  Supramolecular control of an organic radical coupled to a metal ion embedded at the entrance of a hydrophobic cavity , 2003 .

[15]  C. Philouze,et al.  Galactose oxidase models: tuning the properties of CuII-phenoxyl radicals. , 2003, Chemistry.

[16]  A. Rutherford,et al.  Resolving intermediates in biological proton-coupled electron transfer: A tyrosyl radical prior to proton movement , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. D. Stack,et al.  Intramolecular charge transfer and biomimetic reaction kinetics in galactose oxidase model complexes. , 2003, Journal of the American Chemical Society.

[18]  J. W. Whittaker,et al.  Cu(I)-dependent Biogenesis of the Galactose Oxidase Redox Cofactor* , 2003, Journal of Biological Chemistry.

[19]  A. J. Blake,et al.  A phenol–imidazole pro-ligand that can exist as a phenoxyl radical, alone and when complexed to copper(II) and zinc(II) , 2003 .

[20]  J. W. Whittaker,et al.  Free radical catalysis by galactose oxidase. , 2003, Chemical reviews.

[21]  D. Dooley,et al.  Copper-tyrosyl radical enzymes. , 2003, Current opinion in chemical biology.

[22]  T. D. Stack,et al.  Oxidatively robust monophenolate-copper(II) complexes as potential models of galactose oxidase. , 2003, Chemical communications.

[23]  F. Thomas,et al.  A structural and functional model of galactose oxidase: control of the one-electron oxidized active form through two differentiated phenolic arms in a tripodal ligand. , 2002, Angewandte Chemie.

[24]  Gil,et al.  Electronic states of the phenoxyl radical , 2001 .

[25]  R. Gopalan,et al.  Copper(II) complexes of sterically hindered phenolate ligands as structural models for the active site in galactose oxidase and glyoxal oxidase: X-ray crystal structure and spectral and redox properties , 2001 .

[26]  M. McPherson,et al.  Crystal structure of the precursor of galactose oxidase: An unusual self-processing enzyme , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Fröhlich,et al.  Coordination Chemistry of Unsymmetrical Tripodal Ligands with an NNO2 Donor Set , 2001 .

[28]  A. Sykes,et al.  Interconversion of Cu(I) and Cu(II) forms of galactose oxidase: comparison of reduction potentials. , 2001, Journal of inorganic biochemistry.

[29]  Y. Matsumura,et al.  Construction of persistent phenoxyl radical with intramolecular hydrogen bonding. , 2001, Journal of the American Chemical Society.

[30]  A. Rutherford,et al.  Orientation of the tyrosyl D, pheophytin anion, and semiquinone Q(A)(*)(-) radicals in photosystem II determined by high-field electron paramagnetic resonance. , 2000, Biochemistry.

[31]  O. Yamauchi,et al.  A Structural Model for the Galactose Oxidase Active Site which Shows Counteranion‐Dependent Phenoxyl Radical Formation by Disproportionation , 2000 .

[32]  W. Tolman,et al.  Understanding the copper–phenoxyl radical array in galactose oxidase: contributions from synthetic modeling studies , 2000 .

[33]  S. Fukuzumi,et al.  Active site models for galactose oxidase containing two different phenol groups , 2000 .

[34]  S. Fukuzumi,et al.  Active Site Models for Galactose Oxidase and Related Enzymes , 2000 .

[35]  M. McPherson,et al.  Galactose Oxidase Pro-Sequence Cleavage and Cofactor Assembly Are Self-Processing Reactions , 2000 .

[36]  K. Wieghardt,et al.  Intramolecular Spin Interactions in Bis(phenoxyl)metal Complexes of Zinc(II) and Copper(II) , 1999 .

[37]  Eckhard Bill,et al.  Aerobic Oxidation of Primary Alcohols (Including Methanol) by Copper(II)− and Zinc(II)−Phenoxyl Radical Catalysts , 1999 .

[38]  Taki,et al.  Oxidation of Benzyl Alcohol with Cu(II) and Zn(II) Complexes of the Phenoxyl Radical as a Model of the Reaction of Galactose Oxidase. , 1999, Angewandte Chemie.

[39]  Chunping Xie,et al.  Highly stabilized phenoxyl radicals with hydrogen-bonding capability , 1999 .

[40]  H. Sigel,et al.  Acid-Base and Metal-Ion-Coordinating Properties of Benzimidazole and Derivatives (= 1, 3-Dideazapurines) in Aqueous Solution : Interrelation between Complex Stability and Ligand Basicity , 1999 .

[41]  K. Wieghardt,et al.  Aerobic Oxidation of Primary Alcohols by a New Mononuclear Cu(II) -Radical Catalyst. , 1999, Angewandte Chemie.

[42]  B. Diner,et al.  Hydrogen bonding, solvent exchange, and coupled proton and electron transfer in the oxidation and reduction of redox-active tyrosine Y(Z) in Mn-depleted core complexes of photosystem II. , 1998, Biochemistry.

[43]  M. Palaniandavar,et al.  Copper(II) Complexes with Unusual Axial Phenolate Coordination as Structural Models for the Active Site in Galactose Oxidase: X-ray Crystal Structures and Spectral and Redox Properties of [Cu(bpnp)X] Complexes. , 1998, Inorganic chemistry.

[44]  K. Wieghardt,et al.  From Structural Models of Galactose Oxidase to Homogeneous Catalysis: Efficient Aerobic Oxidation of Alcohols. , 1998, Angewandte Chemie.

[45]  W. Hagen,et al.  High-Frequency EPR and Pulsed Q-Band ENDOR Studies on the Origin of the Hydrogen Bond in Tyrosyl Radicals of Ribonucleotide Reductase R2 Proteins from Mouse and Herpes Simplex Virus Type 1 , 1998 .

[46]  J. Stubbe,et al.  Protein Radicals in Enzyme Catalysis. , 1998, Chemical reviews.

[47]  K. Hodgson,et al.  Catalytic galactose oxidase models: biomimetic Cu(II)-phenoxyl-radical reactivity. , 1998, Science.

[48]  M. McPherson,et al.  Properties of the Trp290His variant of Fusarium NRRL 2903 galactose oxidase: interactions of the GOasesemi state with different buffers, its redox activity and ability to bind azide , 1997, JBIC Journal of Biological Inorganic Chemistry.

[49]  E. C. Wilkinson,et al.  Synthetic models of the inactive Copper(II)-tyrosinate and active Copper(II)-tyrosyl radical forms of galactose and glyoxal oxidases , 1997 .

[50]  K. Wieghardt,et al.  Phenoxyl-copper(II) complexes: models for the active site of galactose oxidase , 1997, JBIC Journal of Biological Inorganic Chemistry.

[51]  I. Gautier-Luneau,et al.  A first model for the oxidized active form of the active site in galactose oxidase: a free-radical copper complex , 1997, JBIC Journal of Biological Inorganic Chemistry.

[52]  T. D. Stack,et al.  Galactose Oxidase Model Complexes: Catalytic Reactivities , 1996 .

[53]  A. Barra,et al.  High Field EPR Studies of Mouse Ribonucleotide Reductase Indicate Hydrogen Bonding of the Tyrosyl Radical* , 1996, The Journal of Biological Chemistry.

[54]  K. Morokuma,et al.  Ab Initio Study of the Mechanism for the Thermal Decomposition of the Phenoxy Radical , 1996 .

[55]  A. Rutherford,et al.  g-Values as a Probe of the Local Protein Environment: High-Field EPR of Tyrosyl Radicals in Ribonucleotide Reductase and Photosystem II , 1995 .

[56]  R A Sayle,et al.  RASMOL: biomolecular graphics for all. , 1995, Trends in biochemical sciences.

[57]  T. Shida,et al.  Vibronic Analysis of the ca. 400 nm Band of the Phenoxy Radical within the Approximation of the Weak Coupling Limit , 1994 .

[58]  S. Phillips,et al.  Crystal structure of a free radical enzyme, galactose oxidase. , 1994, Journal of molecular biology.

[59]  T. Momose,et al.  A Theoretical Study on the Electronic and Vibrational Structure of the Phenoxyl Radical , 1994 .

[60]  M. McPherson,et al.  Novel thioether bond revealed by a 1.7 Å crystal structure of galactose oxidase , 1994, Nature.

[61]  L. Johnston,et al.  Assignment and vibrational analysis of the 600 nm absorption band in the phenoxyl radical and some of its derivatives , 1993 .

[62]  J. W. Whittaker,et al.  Electron Paramagnetic Resonance and Electron Nuclear Double Resonance Spectroscopies of the Radical Site in Galactose Oxidase and of Thioether-Substituted Phenol Model Compounds , 1992 .

[63]  J. W. Whittaker,et al.  A tyrosine-derived free radical in apogalactose oxidase. , 1990, The Journal of biological chemistry.

[64]  Hans Eklund,et al.  Three-dimensional structure of the free radical protein of ribonucleotide reductase , 1990, Nature.

[65]  J. W. Whittaker,et al.  The active site of galactose oxidase. , 1988, The Journal of biological chemistry.

[66]  H. Jaffe,et al.  Use of the CNDO method in spectroscopy. XIV. Electronic spectra of free radicals and free radical ions , 1975 .

[67]  D. Kosman,et al.  The molecular properties of the copper enzyme galactose oxidase. , 1974, Archives of biochemistry and biophysics.

[68]  H. Jaffe,et al.  Uses of the CNDO method in spectroscopy. Doublet states , 1973 .

[69]  M. A. Ali,et al.  Calculations on the electronic spectra of anilino, phenoxyl and benzyl radicals , 1966 .

[70]  L. Eriksson,et al.  B3LYP studies of the formation of neutral tyrosyl radical Yz⋅ and regeneration of neutral tyrosine Yz in PSII , 2001 .

[71]  A. J. Blake,et al.  A phenoxyl radical complex of copper(II). , 2001, Chemical communications.

[72]  E. Defrancq,et al.  A functional model of galactose oxidase: catalytic oxidation of primary alcohols with a one-electron oxidized copper(II) complex , 1998 .

[73]  Y. Moro-oka,et al.  Oxidations of primary alcohols with a copper(II) complex as a possible galactose oxidase model , 1986 .