Theoretical modeling of the heme group with a hybrid QM/MM method

The quality of the results obtained in calculations with the hybrid QM/MM method IMOMM on systems where the heme group is partitioned in QM and MM regions is evaluated through the performance of calculations on the 4‐coordinate [Fe(P)] (P = porphyrin), the 5‐coordinate [Fe(P)(1−(Me)Im)] (Im = imidazole) and the 6‐coordinate [Fe(P)(1−(Me)Im)(O2)] systems. The results are compared with those obtained from much more expensive pure quantum mechanics calculations on model systems. Three different properties are analyzed—namely, the optimized geometries, the binding energies of the axial ligands to the heme group, and the energy cost of the biochemically relevant out‐of‐plane displacement of the iron atom. Agreement is especially good in the case of optimized geometries and energy cost of out‐of‐plane displacements, with larger discrepancies in the case of binding energies. © 2000 John Wiley & Sons, Inc. J Comput Chem 21: 282–294, 2000

[1]  T. Vangberg,et al.  Direct Porphyrin−Aryl Orbital Overlaps in Some meso-Tetraarylporphyrins , 1998 .

[2]  David F. Bocian,et al.  Carbonyl Tilting and Bending Potential Energy Surface of Carbon Monoxyhemes , 1996 .

[3]  Gilda H. Loew,et al.  Structure and Spectra of Ferrous Dioxygen and Reduced Ferrous Dioxygen Model Cytochrome P450 , 1998 .

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

[5]  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..

[6]  A. Lledós,et al.  Theoretical Study on the Origin of Enantioselectivity in the Bis(dihydroquinidine)-3,6-pyridazine·Osmium Tetroxide-Catalyzed Dihydroxylation of Styrene , 1999 .

[7]  Robert J. Deeth Saddle Distortions of Ferryl-Porphyrin Models for Peroxidase Compound I: A Density Functional Study , 1999 .

[8]  A. Cooper,et al.  Computational and Experimental Test of Steric Influence on Agostic Interactions: A Homologous Series for Ir(III) , 1999 .

[9]  R. Sheldon Metalloporphyrins in catalytic oxidations , 1994 .

[10]  T. Cundari Computational Organometallic Chemistry , 2001 .

[11]  R. Matthews,et al.  How a protein binds B12: A 3.0 A X-ray structure of B12-binding domains of methionine synthase. , 1994, Science.

[12]  Emma Sigfridsson,et al.  On the significance of hydrogen bonds for the discrimination between CO and O2 by myoglobin , 1999, JBIC Journal of Biological Inorganic Chemistry.

[13]  J. Dawson,et al.  Heme-Containing Oxygenases. , 1996, Chemical reviews.

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

[15]  David S. Latchman,et al.  Biochemistry (4th edn) , 1995 .

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

[17]  K. E. Everse,et al.  Peroxidases in chemistry and biology , 1990 .

[18]  E. Oldfield,et al.  Solid-State NMR, Crystallographic and Density Functional Theory Investigation of Fe−CO and Fe−CO Analogue Metalloporphyrins and Metalloproteins† , 1999 .

[19]  Michael T. Green ROLE OF THE AXIAL LIGAND IN DETERMINING THE SPIN STATE OF RESTING CYTOCHROME P450 , 1998 .

[20]  A. Veillard,et al.  Structure and properties of a model of deoxyheme, an ab initio SCF calculation , 1983 .

[21]  P. C. Hariharan,et al.  The influence of polarization functions on molecular orbital hydrogenation energies , 1973 .

[22]  J. Landrum,et al.  X-ray diffraction study of the electronic ground state of (meso-tetraphenylporphinato)iron(II) , 1990 .

[23]  M. Parrinello,et al.  Factors Influencing Ligand-Binding Properties of Heme Models: A First Principles Study of Picket-Fence and Protoheme Complexes , 1999 .

[24]  Michele Parrinello,et al.  The Iron−Sulfur Bond in Cytochrome c , 1999 .

[25]  M. Dupuis,et al.  Structure of a Model Transient Peroxide Intermediate of Peroxidases by ab Initio Methods , 1996 .

[26]  Teizo Kitagawa,et al.  THE PROXIMAL RESIDUE LARGELY DETERMINES THE CO DISTORTION IN CARBONMONOXY GLOBIN PROTEINS. AN AB INITIO STUDY OF A HEME PROSTHETIC UNIT , 1994 .

[27]  Y. Jean,et al.  Theoretical Evaluation of Steric Effects in [ReH(5)(PR(3))(2)(SiR(3))(2)] Complexes with the IMOMM Method. , 1996, Inorganic chemistry.

[28]  Michele Parrinello,et al.  A comparative study of O2, CO, and NO binding to iron–porphyrin , 1998 .

[29]  K. Suslick,et al.  Models for the Active Site of Oxygen-Binding Hemoproteins. Dioxygen Binding Properties and the Structures of (2-Methylimidazole)-meso-tetra(α,α,α,α-o-Pivalamidophenyl)porphyrinatoiron(II)-Ethanol and Its Dioxygen Adduct , 1980 .

[30]  M. Halcrow,et al.  Biomimetic Chemistry of Nickel , 1994 .

[31]  R. Parr Density-functional theory of atoms and molecules , 1989 .

[32]  Michele Parrinello,et al.  Equilibrium Geometries and Electronic Structure of Iron−Porphyrin Complexes: A Density Functional Study , 1997 .

[33]  Norman L. Allinger,et al.  Molecular mechanics. The MM3 force field for hydrocarbons. 3. The van der Waals' potentials and crystal data for aliphatic and aromatic hydrocarbons , 1989 .

[34]  Michael B. Hall,et al.  Theoretical Calculations of Metal-Dioxygen Complexes , 1994 .

[35]  Norman L. Allinger,et al.  Molecular mechanics. The MM3 force field for hydrocarbons. 2. Vibrational frequencies and thermodynamics , 1989 .

[36]  J. Pople,et al.  Self‐Consistent Molecular‐Orbital Methods. I. Use of Gaussian Expansions of Slater‐Type Atomic Orbitals , 1969 .

[37]  A. Varvoglis Hypervalent iodine in organic synthesis , 1996 .

[38]  Robert H. Crabtree,et al.  The organometallic chemistry of the transition metals , 1992 .

[39]  Myung-Hwan Whangbo,et al.  Orbital Interactions in Chemistry , 1985 .

[40]  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 .

[41]  James P. Collman,et al.  Structure of a dioxygen adduct of (1-methylimidazole)-meso-tetrakis(.alpha.,.alpha.,.alpha.,.alpha.,-o-pivalamidophenyl)porphinatoiron(II). An iron dioxygen model for the heme component of oxymyoglobin , 1978 .

[42]  A. Rappé,et al.  Molecular Mechanics Across Chemistry , 1997 .

[43]  Keiji Morokuma,et al.  Application of the New “Integrated MO + MM” (IMOMM) Method to the Organometallic Reaction Pt(PR3)2 + H2 (R = H, Me, t-Bu, and Ph) , 1996 .

[44]  Christopher A. Reed,et al.  Synthetic Heme Dioxygen Complexes , 1994 .

[45]  H. Fujii,et al.  Change in Electron Configuration of Ferric Ion in Bis(cyanide)(meso-tetraalkylporphyrinatoiron(III)), [Fe(TRP)(CN)2]-, Caused by the Nonplanarity of the Porphyrin Ring , 1997 .

[46]  Ben F. Luisi,et al.  Stereochemistry of cooperative mechanisms in hemoglobin , 1987 .

[47]  G. Loew,et al.  Identification of putative peroxide intermediates of peroxidases by electronic structure and spectra calculations , 1996 .

[48]  I. Ojima,et al.  Catalytic Asymmetric Synthesis , 1993 .

[49]  P. Kollman,et al.  Encyclopedia of computational chemistry , 1998 .

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

[51]  M. Perutz,et al.  Review Lecture - Stereochemical mechanism of oxygen transport by haemoglobin , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[52]  T. Spiro,et al.  Discordant Results on FeCO Deformability in Heme Proteins Reconciled by Density Functional Theory , 1998 .

[53]  Norman L. Allinger,et al.  Molecular mechanics. The MM3 force field for hydrocarbons. 1 , 1989 .

[54]  J. Barber,et al.  Revealing the blueprint of photosynthesis , 1994, Nature.

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

[56]  K. Welinder Superfamily of plant, fungal and bacterial peroxidases , 1992 .

[57]  Gregori Ujaque,et al.  Computational Evidence of the Importance of Substituent Bulk on Agostic Interactions in Ir(H)2(PtBu2Ph)2 , 1998 .

[58]  Thomas G. Spiro,et al.  Low-Lying Spin States of Iron(II) Porphine , 1998 .

[59]  A. Veillard,et al.  Ab Initio Calculations of Metalloporphyrins , 1982 .

[60]  Feliu Maseras,et al.  Binding of dioxygen in a picket-fence porphyrin complex of iron. A theoretical QM/MM study , 1998 .

[61]  H. Schaefer Methods of Electronic Structure Theory , 1977 .

[62]  Christopher A. Reed,et al.  A deoxymyoglobin model with a sterically unhindered axial imidazole , 1988 .

[63]  B. Malmström,et al.  Cytochrome oxidase as a redox-linked proton pump. , 1990, Acta physiologica Scandinavica. Supplementum.

[64]  F. Maseras,et al.  Opposing steric and electronic contributions in OsCl2H2(PPr3i)2. A theoretical study of an unusual structure , 1998 .

[65]  Teizo Kitagawa,et al.  The Proximal Residue Largely Determines the CO Distortion in Carbon Monoxy Globin Proteins. An ab Initio Study of a Heme Prosthetic Unit , 1995 .

[66]  T. Vangberg,et al.  Deformability of Fe(II)CO and Fe(III)CN groups in heme protein models: nonlocal density functional theory calculations , 1997, JBIC Journal of Biological Inorganic Chemistry.

[67]  G. Loew,et al.  An ab Initio Model System Investigation of the Proposed Mechanism for Activation of Peroxidases: Cooperative Catalytic Contributions from the Ion and Microsolvent Water , 1998 .

[68]  A. Lledós,et al.  Basis set influence on the ab initio description of the dihydrogen complex [Os(PH3)2Cl(CO)H(H2)]1 , 1996 .

[69]  M. Newman,et al.  Steric Effects In Organic Chemistry , 1956 .

[70]  Kevin M. Smith,et al.  Conformational Flexibility in Dodecasubstituted Porphyrins , 1996 .

[71]  M. Rohmer Electronic ground state of iron(II)porphyrin. Ab initio SCF and CI calculations and computed electron deformation densities , 1985 .

[72]  Michele Parrinello,et al.  A density functional study of iron-porphyrin complexes , 1997 .

[73]  T. Spiro,et al.  Will the real FeCO please stand up? , 1997, JBIC Journal of Biological Inorganic Chemistry.