Spin-dependent mechanism for diatomic ligand binding to heme

The nature of diatomic ligand recombination in heme proteins is elucidated by using a Landau–Zener model for the electronic coupling in the recombination rate constant. The model is developed by means of explicit potential energy surfaces calculated by using density functional theory (DFT). The interaction of all possible spin states of the three common diatomic ligands, CO, NO, and O2, and high-spin heme iron is compared. The electronic coupling, rebinding barrier, and Landau–Zener force terms can be obtained and used to demonstrate significant differences among the ligands. In particular the intermediate spin states of NO (S = 3/2) and O2 (S = 1) are shown to be bound states. Rapid recombination occurs from these bound states in agreement with experimental data. The slower phases of O2 recombination can be explained by the presence of two higher spin states, S = 2 and S = 3, which have a small and relatively large barrier to ligand recombination, respectively. By contrast, the intermediate spin state for CO is not a bound state, and the only recombination pathway for CO involves direct recombination from the S = 2 state. This process is significantly slower according to the Landau–Zener model. Quantitative estimates of the parameters used in the rate constants provide a complete description that explains rebinding rates that range from femtoseconds to milliseconds at ambient temperature.

[1]  J. Hofrichter,et al.  Protein reaction kinetics in a room-temperature glass , 1995, Science.

[2]  I. Schlichting,et al.  Crystal structure of photolysed carbonmonoxy-myoglobin , 1994, Nature.

[3]  M. Lim,et al.  Nonexponential protein relaxation: dynamics of conformational change in myoglobin. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Brunori,et al.  Enzyme Proteins. (Book Reviews: Hemoglobin and Myoglobin in Their Reactions with Ligands) , 1971 .

[5]  J. B. Johnson,et al.  Ligand binding to heme proteins: connection between dynamics and function. , 1991, Biochemistry.

[6]  C. M. Jones,et al.  The role of solvent viscosity in the dynamics of protein conformational changes. , 1992, Science.

[7]  S. Boxer,et al.  Ligand and proton exchange dynamics in recombinant human myoglobin mutants. , 1989, Journal of molecular biology.

[8]  D. Devault,et al.  Quantum mechanical tunnelling in biological systems. , 1980, Quarterly reviews of biophysics.

[9]  J. B. Johnson,et al.  Rebinding and relaxation in the myoglobin pocket. , 1987, Biophysical chemistry.

[10]  Y. Lecarpentier,et al.  Femtosecond photolysis of CO-ligated protoheme and hemoproteins: appearance of deoxy species with a 350-fsec time constant. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[11]  S. Boxer,et al.  Ultrafast measurements of geminate recombination of NO with site-specific mutants of human myoglobin. , 1994, Journal of molecular biology.

[12]  Richard L. Martin,et al.  Microscopic model of carbon monoxide binding to myoglobin , 2000 .

[13]  B. Delley.  From molecules to solids with the DMol3 approach , 2000 .

[14]  K. Moffat,et al.  Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K , 1994, Nature Structural Biology.

[15]  Xiaoyuan Li,et al.  Iron motion in a five-coordinated heme model , 1992 .

[16]  N. Yu,et al.  Resonance Raman investigation of nitric oxide bonding in nitrosylhemoglobin A and -myoglobin: detection of bound N-O stretching and Fe-NO stretching vibrations from the hexacoordinated NO-heme complex. , 1982, Biochemistry.

[17]  Y. Shiro,et al.  Effect of NaCl addition on nanosecond O2 escaping reaction of myoglobin: evidences for the transition of myoglobin dynamic structure at 20 degrees C. , 1992, Biochimica et biophysica acta.

[18]  D Bourgeois,et al.  Photolysis of the Carbon Monoxide Complex of Myoglobin: Nanosecond Time-Resolved Crystallography , 1996, Science.

[19]  R. Marcus.  Superexchange versus an intermediate BChl− mechanism in reaction centers of photosynthetic bacteria , 1987 .

[20]  D. Magde,et al.  Geminate recombination of diatomic ligands CO, O2, and NO with myoglobin. , 1994, Biochemistry.

[21]  U. Liebl,et al.  Ultrafast ligand rebinding in the heme domain of the oxygen sensors FixL and Dos: General regulatory implications for heme-based sensors , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  L. Kiger,et al.  Heme photolysis occurs by ultrafast excited state metal-to-ring charge transfer. , 2001, Biophysical journal.

[23]  J Berendzen,et al.  Crystal structures of myoglobin-ligand complexes at near-atomic resolution. , 1999, Biophysical journal.

[24]  J. Petrich,et al.  Photophysics and reactivity of heme proteins: a femtosecond absorption study of hemoglobin, myoglobin, and protoheme. , 1988, Biochemistry.

[25]  B. Delley.  An all‐electron numerical method for solving the local density functional for polyatomic molecules , 1990 .

[26]  C. M. Jones,et al.  Conformational relaxation and ligand binding in myoglobin. , 1994, Biochemistry.

[27]  S. Franzen,et al.  Direct evidence for the role of haem doming as the primary event in the cooperative transition of haemoglobin , 1994, Nature Structural Biology.

[28]  J. Friedman,et al.  Structure, dynamics, and reactivity in hemoglobin. , 1985, Science.

[29]  Stefan Franzen.  Carbonmonoxy Rebinding Kinetics in H93G Myoglobin: Separation of Proximal and Distal Side Effects , 2002 .

[30]  K. Mikkelsen,et al.  Direct and superexchange electron tunneling at the adjacent and remote sites of higher plant plastocyanins , 1990 .

[31]  R. Hochstrasser,et al.  Energy dissipation and relaxation processes in deoxy myoglobin after photoexcitation in the Soret region , 2000 .

[32]  A. Becke.  Density-functional thermochemistry. V. Systematic optimization of exchange-correlation functionals , 1997 .

[33]  S. Boxer,et al.  Dynamics of protein relaxation in site-specific mutants of human myoglobin. , 1993, Biochemistry.

[34]  S. Boxer,et al.  CO recombination to human myoglobin mutants in glycerol-water solutions. , 1993, Biochemistry.

[35]  M. Michel-beyerle,et al.  A kinetic analysis of the primary charge separation in bacterial photosynthesis. Energy gaps and static heterogeneity , 1995 .

[36]  R. Hochstrasser,et al.  Spectroscopic studies of oxy- and carbonmonoxyhemoglobin after pulsed optical excitation. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

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

[38]  S. Boxer,et al.  On the Origin of Heme Absorption Band Shifts and Associated Protein Structural Relaxation in Myoglobin following Flash Photolysis* , 1997, The Journal of Biological Chemistry.

[39]  Krzysztof Kuczera,et al.  Ligand binding and protein relaxation in heme proteins: a room temperature analysis of nitric oxide geminate recombination , 1991 .

[40]  E. Henry,et al.  Geminate recombination of carbon monoxide to myoglobin. , 1983, Journal of molecular biology.

[41]  S. Boxer,et al.  Protein relaxation dynamics in human myoglobin , 1991 .

[42]  Walter Kohn,et al.  Quantum Density Oscillations in an Inhomogeneous Electron Gas , 1965 .

[43]  T. Spiro,et al.  Probing protein structure and dynamics with resonance Raman spectroscopy: cytochrome c peroxidase and hemoglobin. , 1990, Biochemistry.

[44]  G. Kachalova,et al.  A steric mechanism for inhibition of CO binding to heme proteins. , 1999, Science.

[45]  M. Karplus,et al.  Nonexponential relaxation after ligand dissociation from myoglobin: a molecular dynamics simulation. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. Mukamel,et al.  SUPEREXCHANGE VERSUS SEQUENTIAL LONG RANGE ELECTRON TRANSFER ; DENSITY MATRIX PATHWAYS IN LIOUVILLE SPACE , 1995 .

[47]  S. Franzen,et al.  Evidence for sub-picosecond heme doming in hemoglobin and myoglobin: a time-resolved resonance Raman comparison of carbonmonoxy and deoxy species. , 1995, Biochemistry.

[48]  E. Chien,et al.  Probing heme protein conformational equilibration rates with kinetic selection. , 1996, Biochemistry.

[49]  M. Lim,et al.  Mid-infrared vibrational spectrum of CO after photodissociation from heme: Evidence for a ligand docking site in the heme pocket of hemoglobin and myoglobin , 1995 .

[50]  S. Boxer,et al.  Distance Dependence of Electron-Transfer Reactions in Organized Systems: The Role of Superexchange and Non-Condon Effects in Photosynthetic Reaction Centers , 1993 .

[51]  E. Henry,et al.  Simulation of the kinetics of ligand binding to a protein by molecular dynamics: geminate rebinding of nitric oxide to myoglobin. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[52]  H Frauenfelder,et al.  Dynamics of ligand binding to myoglobin. , 1975, Biochemistry.