Hybrid quantum mechanics/molecular mechanics studies of the active site of the blue copper proteins amicyanin and rusticyanin

Abstract The structures of the oxidized form of the two blue copper proteins amicyanin and rusticyanin, two cupredoxines with strikingly different properties, were analyzed with quantum mechanics/molecular mechanics (QM/MM). The minimum model for the QM part was evaluated with pure DFT calculations, and the strain imposed by the protein backbones on this structure is in the expected range, i.e., 74 kJ mol −1 for amicyanin and 82 kJ mol −1 for rusticyanin. The optimized structures are similar to the published X-ray crystal structures but the error on the experimental data is of the same order of magnitude as the variation between the two experimental structures and similar to the difference between the computed and experimental data.

[1]  Parr,et al.  Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. , 1988, Physical review. B, Condensed matter.

[2]  S. S. Isied.  Electron transfer reactions : inorganic, organometallic, and biological applications , 1997 .

[3]  F. Cordes,et al.  Accuracy and precision in protein crystal structure analysis: two independent refinements of the structure of poplar plastocyanin at 173 K. , 1994, Acta crystallographica. Section D, Biological crystallography.

[4]  B. Malmström.  Rack-induced bonding in blue-copper proteins. , 1994, European journal of biochemistry.

[5]  U. Ryde,et al.  Quantum chemical calculations of the reorganization energy of blue‐copper proteins , 1998, Protein science : a publication of the Protein Society.

[6]  F. Allen,et al.  Implications of molecular and materials structure for new technologies , 1999 .

[7]  P. Beroza,et al.  NMR solution structure of Cu(I) rusticyanin from Thiobacillus ferrooxidans: structural basis for the extreme acid stability and redox potential. , 1996, Journal of molecular biology.

[8]  K. Hodgson,et al.  Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding and implications for the entatic/rack state. , 1996 .

[9]  Jean-Didier Maréchal,et al.  Theoretical modeling of the heme group with a hybrid QM/MM method , 2000 .

[10]  C. Buning,et al.  Loop-Directed Mutagenesis of the Blue Copper Protein Amicyanin from Paracoccus versutus and Its Effect on the Structure and the Activity of the Type-1 Copper Site , 2000 .

[11]  S. Vries,et al.  The methylamine dehydrogenase electron transfer chain , 1998 .

[12]  X. You,et al.  Steric effects, solvent effects, and turnover in hydrolytic cleavage of peptides promoted by palladium(II) aqua complexes , 1998, JBIC Journal of Biological Inorganic Chemistry.

[13]  W. R. Wadt,et al.  Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals , 1985 .

[14]  Harry B. Gray,et al.  Copper coordination in blue proteins , 2000, JBIC Journal of Biological Inorganic Chemistry.

[15]  Feliu Maseras,et al.  The IMOMM method opens the way for the accurate calculation of “real” transition metal complexes , 2000 .

[16]  Thomas M. Loehr,et al.  Resonance Raman excitation profiles indicate multiple Cys → Cu charge transfer transitions in type 1 copper proteins , 1993 .

[17]  Björn O. Roos,et al.  On the role of strain in blue copper proteins , 2000, JBIC Journal of Biological Inorganic Chemistry.

[18]  B. Roos,et al.  The cupric geometry of blue copper proteins is not strained. , 1996, Journal of molecular biology.

[19]  A. Becke.  Density-functional thermochemistry. III. The role of exact exchange , 1993 .

[20]  M. Frisch,et al.  Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields , 1994 .

[21]  Henry Eyring,et al.  Conformation Changes of Proteins , 1954 .

[22]  P. Comba,et al.  An amicyanin C-terminal loop mutant where the active-site histidine donor cannot be protonated , 2000, JBIC Journal of Biological Inorganic Chemistry.

[23]  D. Boxer,et al.  The purification and some properties of rusticyanin, a blue copper protein involved in iron(II) oxidation from Thiobacillus ferro-oxidans. , 1978, The Biochemical journal.

[24]  F. Himo,et al.  Catalytic Mechanism of Galactose Oxidase: A Theoretical Study , 2000 .

[25]  Peter Comba,et al.  Coordination compounds in the entatic state , 2000 .

[26]  A. Tsugita,et al.  Isolation and characterization of a blue copper protein from Thiobacillus versutus. , 1985, European journal of biochemistry.

[27]  Feliu Maseras,et al.  IMOMM: A new integrated ab initio + molecular mechanics geometry optimization scheme of equilibrium structures and transition states , 1995, J. Comput. Chem..

[28]  C. Dennison,et al.  Determination of the Self-Exchange Rate Constant for Rusticyanin from Thiobacillus ferrooxidans and a Comparison with Values for Other Type 1 Blue Copper Proteins , 1995 .

[29]  Structure and function of copper-containing proteins , 1991 .

[30]  W. R. Wadt,et al.  Ab initio effective core potentials for molecular calculations. Potentials for main group elements Na to Bi , 1985 .

[31]  Edward I. Solomon,et al.  Structural and Functional Aspects of Metal Sites in Biology. , 1996, Chemical reviews.

[32]  Björn O. Roos,et al.  Relation between the Structure and Spectroscopic Properties of Blue Copper Proteins , 1998 .

[33]  W. R. Wadt,et al.  Ab initio effective core potentials for molecular calculations , 1984 .

[34]  E. Solomon,et al.  ELECTRONIC STRUCTURE OF THE REDUCED BLUE COPPER ACTIVE SITE : CONTRIBUTIONS TO REDUCTION POTENTIALS AND GEOMETRY , 1995 .

[35]  W. Goddard,et al.  UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations , 1992 .

[36]  Mark S. Gordon,et al.  Self‐consistent molecular orbital methods. XXIII. A polarization‐type basis set for second‐row elements , 1982 .

[37]  W. D. Mcelroy,et al.  A Symposium on the Mechanism of Enzyme Action , 1954 .

[38]  J. Pople,et al.  Self—Consistent Molecular Orbital Methods. XII. Further Extensions of Gaussian—Type Basis Sets for Use in Molecular Orbital Studies of Organic Molecules , 1972 .

[39]  C. Dennison,et al.  LOOP-DIRECTED MUTAGENESIS CONVERTS AMICYANIN FROM THIOBACILLUS VERSUTUS INTO A NOVEL BLUE COPPER PROTEIN , 1996 .

[40]  A. Sykes.  Active-site properties of the blue copper proteins , 1991 .

[41]  U. Ryde,et al.  The influence of axial ligands on the reduction potential of blue copper proteins , 1999, JBIC Journal of Biological Inorganic Chemistry.