Rational tuning of the thiolate donor in model complexes of superoxide reductase: direct evidence for a trans influence in Fe(III)-OOR complexes.
Iron peroxide species have been identified as important intermediates in a number of nonheme iron as well as heme-containing enzymes, yet there are only a few examples of such species either synthetic or biological that have been well characterized. We describe the synthesis and structural characterization of a new series of five-coordinate (N4S(thiolate))Fe(II) complexes that react with tert-butyl hydroperoxide ((t)BuOOH) or cumenyl hydroperoxide (CmOOH) to give metastable alkylperoxo-iron(III) species (N4S(thiolate)Fe(III)-OOR) at low temperature. These complexes were designed specifically to mimic the nonheme iron active site of superoxide reductase, which contains a five-coordinate iron(II) center bound by one Cys and four His residues in the active form of the protein. The structures of the Fe(II) complexes are analyzed by X-ray crystallography, and their electrochemical properties are assessed by cyclic voltammetry. For the Fe(III)-OOR species, low-temperature UV-vis spectra reveal intense peaks between 500-550 nm that are typical of peroxide to iron(III) ligand-to-metal charge-transfer (LMCT) transitions, and EPR spectroscopy shows that these alkylperoxo species are all low-spin iron(III) complexes. Identification of the vibrational modes of the Fe(III)-OOR unit comes from resonance Raman (RR) spectroscopy, which shows nu(Fe-O) modes between 600-635 cm(-1) and nu(O-O) bands near 800 cm(-1). These Fe-O stretching frequencies are significantly lower than those found in other low-spin Fe(III)-OOR complexes. Trends in the data conclusively show that this weakening of the Fe-O bond arises from a trans influence of the thiolate donor, and density functional theory (DFT) calculations support these findings. These results suggest a role for the cysteine ligand in SOR, and are discussed in light of the recent assessments of the function of the cysteine ligand in this enzyme.
Namuswe
Frances
F
Department of Chemistry, Johns Hopkins University, Baltimore, Maryland 21218, USA.
Kasper
Gary D
GD
Sarjeant
Amy A Narducci
AA
Hayashi
Takahiro
T
Krest
Courtney M
CM
Green
Michael T
MT
Moënne-Loccoz
Pierre
P
Goldberg
David P
DP
D001555:Benzene Derivatives / Q000737:chemistry*; D003198:Computer Simulation; D018360:Crystallography, X-Ray; D004563:Electrochemistry; D004566:Electrodes; D005290:Ferric Compounds / Q000138:chemical synthesis* / Q000737:chemistry; D005296:Ferrous Compounds / Q000737:chemistry*; D008024:Ligands; D008956:Models, Chemical; D008958:Models, Molecular; D015394:Molecular Structure; D010088:Oxidoreductases / Q000737:chemistry*; D013056:Spectrophotometry, Ultraviolet / Q000379:methods; D013059:Spectrum Analysis, Raman / Q000379:methods; D013438:Sulfhydryl Compounds / Q000737:chemistry*; D020122:tert-Butylhydroperoxide / Q000737:chemistry*
D001555:Benzene Derivatives; D005290:Ferric Compounds; D005296:Ferrous Compounds; D008024:Ligands; D013438:Sulfhydryl Compounds; D020122:tert-Butylhydroperoxide; D010088:Oxidoreductases; C121849:superoxide reductase