Electron Transfer in Bioinorganic Chemistry - Advances in Chemistry

May 5, 1997 - The unique spectral features of oxidized blue copper proteins have often been used to support the concept that the reduced geometry is ...
0 downloads 0 Views 1MB Size
19 Electron Transfer in Bioinorganic

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

Chemistry Role of Electronic Structure and the Entatic State Edward I. Solomon*, Michael D. Lowery, Jeffrey A. Guckert, and Louis B. LaCroix Department of Chemistry, Stanford University, Stanford, CA 94305

The unique spectral features of oxidized blue copper proteins have often been used to support the concept that the reduced geometry is imposed on the oxidized copper site by the protein. This has beencalledan "entatic" or "rack" state and is thought to make a significant contribu-tion to rapid electron transfer in biology. In this presentation, the unique spectral features of the oxidized d state are shown to reflect a novel ground state wavefunction that plays a key role in defining electron transfer pathways. Further, the electronic structure of the reduced d blue copper site has been determined using a combination of variable-energy photoelectron spectroscopy and electronic structure calculations. These studies determine the change in electronic structure that occurs on oxidation and allow an evaluation of whether the reduced geometry is, in fact, imposed on the oxidized site. 9

10

HENRY TAUBE'S EXTENSIVE CONTRIBUTIONS TO INORGANIC CHEMISTRY

have laid the foundations for many important areas in bioinorganic chemistry. Taube has clearly had a major impact in how we describe long-range electronic transfer in biology, which is mostly accomplished by three classes of metalloproteins: heme, iron-sulfur, and blue copper. The blue copper proteins have been generally used as the example that demonstrates the presence of an "entatic" or "rack" state in bioinorganic chemistry (1-3). In the entatic state, the protein is thought to impose an unusual geometry on a metal center that activates it for reactivity. The blue copper site that is found in proteins such as Corresponding author.

© 1997 American Chemical Society

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

317

E L E C T R O N T R A N S F E R REACTIONS

318

the plastocyanins and azurins is thought to exist in an entatic state because the oxidized site exhibits unique spectral features compared to those of normal cupric complexes [4-6). In the plastocyanin absorption spectrum, there is an extremely intense band at —600 nm ( c « 5000 M " c m ) , where normal Cu(II) complexes have weak d -> d transitions (e « 40 M cm ), and the parallel hyperfine coupling (A„) in the electron paramagnetic resonance (EPR) spectrum is reduced by more than a factor of 2 relative to that of normal Cu(II) complexes. These unique spectral features are thought to reflect the presence of an unusual geometric structure, which is imposed on the Cu(II) site by the protein (2-3). In particular, reduced copper complexes are often tetrahedrally coordinated, whereas oxidized complexes are frequently found i n tetragonal geometries due to the Jahn-Teller effect. Thus, in the entatic or rack state, the protein would oppose the Jahn-Teller distortion of the oxidized site leading to little geometric change upon oxidation and thus rapid electron transfer. As first predicted from the unique spectral features (7), the oxidized site (Figure 1A) does, i n fact, have a very different geometric structure from that of normal Cu(II) complexes (which are tetragonal) in that the blue copper site has a distorted tetrahedral geometry with two unusual ligand-metal bonds: a short thiolate S - C u bond at —2.1 Â from cysteine (Cys) and a long thioether S - C u bond at —2.8 Â from methionine (Met) (8). The remaining two ligands are fairly normal imidazole N - C u bonds to histidine (His) residues. Also, as shown in Figure I B , little change in geometric structure occurs on reduction (8, 9). The unique spectral features of the oxidized d site are now well under­ stood and reflect a novel ground-state wavefunction (5, 6, 10). Recent experi­ ments that have defined the nature of this ground state are described i n the next section. It is important to emphasize that this is the highest-energy halfoccupied redox-active orbital and thus plays a key role in the electron transfer function of this active site. We have also developed a new method of inorganic spectroscopy to probe the reduced d site, variable-energy photoelectron spectroscopy using synchrotron radiation (11). These experiments combined with self-consistent field-Xa-scattered wave ( S C F - X a - S W ) calculations define, for the first time, the electronic structure of the reduced blue copper site and determine the change in electronic (and associated geometric) struc­ ture that occurs on oxidation. These studies are presented in this chapter and are used to evaluate whether the reduced geometry is in fact imposed on the oxidized blue copper site by the protein. 1

max

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

max

-1

- 1

-1

9

1 0

Electronic Structure of the Oxidized Blue Copper Site: Contributions to Electron Transfer Pathways In earlier studies we used S C F - X a - S W calculations adjusted to the ground state g values to develop a description of the electronic structure of the oxi­ dized blue copper site in plastocyanin (5, 6). The ground state shown in Figure 2 (the contour is in the xy plane, which contains the Cu, cysteine S, and two N -

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

19.

SOLOMON ET AL.

Electron Transfer in Bioinorganic Chemistry

319

Figure 1. Plastocyanin crystallography: (A) X-ray structure of the Cu coordination environment in oxidized poplar plastocyanin (faased on datafromreference 8); (B) crystallographically determined structural changes in the bond lengths and angles between the oxidized and reduced sites in the NNS equatorial plane (lefi) and in the S(Met)CuL angles (nght) (based on datafromreferences 8 and 9). (Reproduced with permissionfromreference 11. Copyright 1995 American Chemical Society.)

atoms of histidine ligands in Figure 1) is quite unusual in that the (1^2 orbital is highly eovalent and the derealization is strongly anisotropic with the domi­ nant interaction involving the ρπ orbital of the cysteine sulfur. This description of the ground state is extremely important for defining possible electronic structure contributions to function in that this wavefunction describes the redox-active orbital that is involved in long-range rapid electron transfer. As this chapter will describe, we have now experimentally confirmed the key fea­ tures of this novel ground state electronic structure.

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

E L E C T R O N TRANSFER REACTIONS

320

42% Cu d 2. 2

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

x

y

Figure 2. Contour of plastocyanin ground-state wavefunction (HOMO). Contour lines are at ±0.64, ±0.32, ±0.16, ±0.08, ±0.04, ±0.02, and ±0.01 (electrons/ bohr ) . The outermost contour encompasses 90% of the electron density. 2

112

The highest occupied molecular orbital (HOMO) in Figure 2 would indi­ cate that the unusually small parallel hyperfine splitting (A ) exhibited in the Ε PR spectrum of the blue copper site already described is due to the high covalency. However, the small A had generally been attributed to a geometric origin where the distorted tetrahedral structure results in the C u 4p orbital mixing into the C u (^2^2 orbital (12). Approximately 12% C u 4p mixing would account for the small A observed for the blue copper site in plastocyanin. This mixing was probed experimentally through an analysis of the polarized singlecrystal X-ray absorption spectral (XAS) data taken at the C u K-edge of plasto­ cyanin (13). The absorption peak observed at —8979 eV in cupric complexes is assigned as the C u Is - » C u (^2^2 transition. In square planar CuClf", there is a small amount of intensity i n this transition due to its quadrupole moment (14). In plastocyanin the intensity increases by a factor of 2 due to 4p mixing with (^2^2, which results in the presence of electric dipole intensity for a tran­ sition from the C u Is orbital. Our earlier single-crystal E P R studies on plasto­ cyanin showed that the orbital is perpendicular to the long thioether S - C u bond present at the blue copper site and within 15° of the plane defined by the remaining three strong ligands (15). Therefore, polarized single-crystal X A S data were taken with the Ε vector of light 11 and J_ to the ζ axis (the thioether S - C u bond) (16). As can be seen from the data in Figure 3, all the 8979 eV intensity is observed with Ε _L ζ [i.e., Ε II (x,y)\ which indicates that C u 4p is mixing with the (^2^2 orbital (4p mixing would increase A„). This suggests that the origin of the small A„ is not 4p mixing but instead would reflect a highly covalent site (13). This possibility was confirmed experimen­ tally through XAS studies at the C u L-edge. N

M

z

z

M

x y

x>

z

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

19.

SOLOMON ET AL.

Electron Transfer in Bioinorganic Chemistry

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

Τ

1

321

Γ

Ell (x,y)(1s->4p )

ι

Li

L J Z

I

8960 8970 8980 8990 9000

Energy (eV)

Figure 3. Polarized single-crystal X-ray absorption spectroscopy at the Cu K-edge for poplar plastocyanin (based on data from reference 16). The C u 2p to half-occupied H O M O transition occurs at - 9 3 0 eV The C u 2p -> 3d transition ( L -edge) is electric-dipole-allowed; thus the intensity of the 930 eV transition reflects the amount of C u character in this H O M O . The L -edge of plastocyanin exhibits 60% of the intensity of the L -edge of square planar D ^ - C u C l f (Figure 4) (17). We have studied D ^ - C u C l f - in great detail and found that the ground state has 61 ± 5% C u character (18). The intensity ratio i n Figure 4 thus indicates that the blue copper site has 38% C u d 2_ 2 character. This value is i n good agreement with the results from elec­ tronic structure calculations in Figure 2(17). The fact that the delocalization dominantly involves the thiolate S was demonstrated by S K-edge XAS studies. [With Hodgson and Hedman we have been developing (13, 19-21) ligand K edge X-ray absorption spectroscopy as a new method for determining the covalency of transition metal complexes.] The S Is -> half-occupied H O M O transi­ tion occurs at —2470 eV. The S Is -> 3p transition is electric-dipole-allowed; therefore, absorption intensity at the S K-edge should reflect the amount of S 3p character mixed into the half-occupied H O M O . The K-edge of plastocyanin is a factor of 2.5 times more intense than tet b, a model complex prepared by Schugar (13) that has a fairly normal thiolate S - C u bond with —15% covalency (Figure 5). Thus the intensity ratio i n Figure 5 indicates that the blue copper ground state has —38% S character, which is also in reasonable agreement with the adjusted SCF-Χα -SW calculations (Figure 2). 23

3

3

-

c

J/

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

322

E L E C T R O N TRANSFER REACTIONS

930

935

940

Energy (eV) Figure 4. Cu L-edge XAS as a probe of ligand-metal covalency: XAS spectra for D -CuClf~ and plastocyanin (based on data from reference 17). Values listed are the amount of Cu d character in the HOMO. 4h

plastocyanin

2468

2469

2470 2471

Energy (eV) Figure 5. S K-edge XAS as a probe of ligand-metal covalency: orientation-aver­ aged XAS spectra for tet b and plastocyaninfoasedon data from reference 13). a is the amount of S ρ character in the HOMO.

2

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

19.

SOLOMON ET AL.

Electron Transfer in Bioinorganic Chemistry

323

A final key feature of the ground-state wavefunction depicted in Figure 2 was confirmed experimentally from our assignments of the unique absorption spectral features of the blue copper site (5). These assignments were made uti­ lizing low-temperature absorption, polarized single-crystal absorption, and cir­ cular (CD) and magnetic circular dichroism (MCD) data, each method having different selection rules. There are a minimum of eight bands required to simultaneouslyfitthe spectra. From the assignments indicated in the low-tem­ perature absorption spectrum in Figure 6, Cys -> C u charge transfer domi­ nates the intensity but with the lower-energy π charge-transfer transition being more intense than the higher-energy Cys (pseudo)-a charge-transfer transition. This is inverted from what is observed for a normal ligand-metal bond and requires that the d 2_ 2 orbital be rotated 45° such that its lobes are bisected by the Cys S - C u axis as in Figure 2. This rotation of the orbital occurs due to the strong π antibonding interaction with the thiolate at the short Cys S - C u bond length. We have correlated the ground-state wavefunction with the crystal struc­ ture of several blue copper proteins and obtained significant insight into its contributions to long-range electron transfer pathways. In plastocyanin, the cysteine is adjacent to a tyrosine that is at the "remote patch" on the protein (Figure 7) (22). In ascorbate oxidase (23) and nitrite reductase (24), it is flanked x

y

ι CysTC/V 4 / \

5

ν

Cys

Ο

ί,

pseudo-σ/ι

CO

^2 ω

1

1 —

-

\

\

- \ '

from MCD*"

(not to scale)

-Met π, J ι l J /'-

8 ...

a

25000

20000

15000

10000

5000

Energy (cm ) 1

Figure 6. Blue copper excited-state spectral features: low-temperature absorption spectrum of plastocyanin. The position of band 8 has been determined from nearIB MCD data. The dashed lines indicate Gaussian resolution into the component bands (5).

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

324

E L E C T R O N TRANSFER REACTIONS

Figure 7. Proposed long-range électron transfer pathway in plastocyanin (5, 6,10.) Left: polypeptide backbone for plastocyanin. The residues that form the proposed path are darkened. Side groups for the blue copper ligated residues and the adjacent tyrosine are included (8). Right: the plastocyanin wavefunction contours superimposed on the crystallographically defined site including the adjacent tyrosine residue that, along with the cysteine, form the path to the "remote" patch (22). The contour shows the substantial electron delocalizaUon onto the cysteine S ρ π orbital that activates electron transfer to the remote patch —12.5 λ from the blue copper site. This low-energy, intense Cys Sn->Cu charge transfer transition pro­ vides an effective hole superexchange mechanism for rapid long-range electron transfer.

by histidine, which is a ligand at an additional copper center. In all three pro­ teins rapid electron transfer occurs over —13 Â, to the remote patch in plasto­ cyanin and the additional copper center in ascorbate oxidase and nitrite reduc­ tase. The highly anisotropic covalency involving the thiolate activates this group for directional electron transfer, while the low-energy intense Cys π - » C u charge transfer transition (Figure 6) provides a very efficient hole superex­ change mechanism for rapid electron transfer (JO). Thus the unique spectral features of the oxidized blue copper site reflect a ground-state wavefunction that is activated for rapid electron transfer to a specific site on or in the protein.

Electronic Structure of the Reduced Blue Copper Site: Contributions to Reduction Potentials and Geometry Over recent years, we have been strongly involved in the development of vari­ able-energy photoelectron spectroscopy (PES) using synchrotron radiation as a new method of defining the bonding and its change with ionization i n inor­ ganic complexes {18, 25-28). We have now used this method combined with

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

19.

SOLOMON E T AL.

325

Electron Transfer in Bioinorganic Chemistry

S C F - X a - S W calculations to determine the electronic structure of the reduced d blue copper site and thus the change in electronic structure with oxidation (11). We have also been interested in whether the reduced geometry is, in fact, imposed by the protein on the oxidized site (i.e., the entatic or rack state). Since P E S detects valence electrons, these studies were performed on model complexes, and as we are interested in understanding unconstrained ligandmetal bonding and how it relates to the protein, the models we studied using variable-energy P E S involved the blue copper relevant imidazole, ( C H ) S , and C H S ~ ligands bound to coordinatively unsaturated Cu(I) sites on oxide and chloride single-crystal surfaces in ultra-high vacuum (11). The P E S spec­ trum of methyl thiolate on cuprous oxide is presented as an example of the data obtained (Figure 8A). The surface oxide was used to drive the deprotonation of methanethiol (which was confirmed by chemical shifts of core levels). The dashed line is the valence band spectrum of clean cuprous oxide, while the solid spectrum is that of the thiolate-bound Cu(I) site. The difference spectrum on the bottom thus gives the P E S of the valence orbitals of the thiolate involved in bonding to the Cu(I). Varying the photon energy changes the rela­ tive intensities of the peaks and allows for the specific assignments indicated in Figure 8A. There are three thiolate valence orbitals involved in bonding: π, pseudo-σ, and σ (Figure 8B). The π and pseudo-σ dominate based on crosssection effects, and these split in energy indicating that the thiolate is bound to the surface copper site with an R - S - C u angle φ < < 180°. Thus, the energy splitting and intensities of the valence orbital peaks in the difference spectrum in Figure 8A define the geometric and electronic structure of the thiolate S-Cu(I) bond. 1 0

3

2

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

3

Our approach was first to use variable-energy P E S to experimentally esti­ mate the geometric and electronic structure of each ligand-metal surface com­ plex unconstrained by the protein matrix. We then used these data to evaluate and calibrate transition-state S C F - X a - S W calculations of the surface com­ plexes. These calculations were then extended to generate an electronic struc­ ture description of the reduced blue copper site and to determine the changes in the electronic structure that occur upon oxidation. These are described in detail in reference 11. The key points of these studies are summarized as follows. (1) The bonding is dominated by ligand donor interactions with the unoc­ cupied C u 4p orbitals. Thus, even though it is a Cu(I) site there is no backbonding with the blue copper ligand set. (2) The long thioether S-Cu(I) (2.9 Â) bond is imposed on the copper site by

Thus, this a clear example of a protein-constrained entatic state. This long thioether bond reduces its donor interaction with the copper, which is compensated for by the thiolate leading to its short 2.1 Âbond. The long thioether S-Cu(I) bond also preferentially destabilizes the oxidized site and is thus a major contribution to the generally high reduction potentials of many of the blue copper proteins. the protein.

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

326

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

E L E C T R O N TRANSFER REACTIONS

I—ι 1—-I l_J 1 1 ι ι I ι ι ι ι I I I I I I I I u—i I 25 20 15 10 5 0

Ionization Energy (eV)

π

pseudo-σ

σ

Figure 8. CH S-Cu(I) bonding. (A): valence band PES of clean Cu 0(lU), Cu 0(lll) exposed to methaneihiol, and their difference spectrum with Gauss­ ian/Lorenzian resolution of the low-energy region. (B): valence orbitals of rnethanethioUtte. (Reproduced with permission from reference 11. Copyright 1995 American Chemical Society.) 3

2

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

2

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

19.

SOLOMON ET AL.

Electron Transfer in Bioinorganic Chemistry

327

(3) The major change in electronic structure that occurs on oxidation is the hole produced i n the cL^a-derived molecular orbital pictured i n Figure 2, which is strongly antibonchng with the thiolate and more weakly antibonding with the two histidine ligands. (4) Having obtained an experimentally calibrated description of the change i n electronic structure on oxidation, we could evaluate the associated change in geometric structure that would occur for a blue copper site uncon­ strained by the protein. This was accomplished by evaluating the electronnuclear linear-coupling terms of the oxidized site in the reduced geometry along all the normal modes of the blue copper structure. A nonzero slope i n Figure 9 corresponds to a distorting force along a specific normal mode. The geometric structural changes we predict on oxidation are consistent with the change i n electronic structure described already in this chapter. There is a large distorting force to contract the thiolate S - C u bond. This, however, is opposed by a large force constant associated with the short strong Cys S - C u

distortion coordinate, Q; Figure 9. Distorting forces in the blue copper site on oxidation. Configuration coordinate diagram of the linear coupling term for the distorting force along the ith normal mode of vibration, Q on the oxidized Cu(II) site relative to the reduced Cu(I) ground state (11). Γ and Γ are the ground and excited state wave func­ tions, respectively. 10,000 c m ; it would be an electron-nuclear cou­ pling term between these levels that would produce a Jahn-Teller distorting force. Thus there is litde geometric change that occurs on oxidation leading to a low Franck-Condon barrier to electron transfer (8, 30). x

y

-1

xy

Summary The unique spectral features of the oxidized blue copper site are now under­ stood. These reflect high anisotropic covalency in the ground-state wavefunc­ tion involving the thiolate that activates this residue as an efficient superexchange pathway for electron transfer. Photoelectron spectroscopy has been developed as a new spectroscopic probe of the reduced blue copper site. It has defined the change i n electron structure that occurs on oxidation, which is found to be consistent with the limited geometric change observed experimen­ tally. This limited geometric change leads to a low Franck-Condon barrier to electron transfer. Thus, the reduced geometry is not imposed by the protein on the oxidized site. The protein does impose a long thioether S - C u (i.e., weak axial) bond on the reduced site, which is compensated by the short thiolate S - C u bond. This raises the reduction potential, quenches the possible Jahn-Teller distortion of the oxidized site, and activates the thiolate electron transfer pathway.

Acknowledgments Ε. I. Solomon wishes to express sincere appreciation to all his students and collaborators who are listed as his co-authors in the Reference list, for their commitment and contribution to this science.

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

19.

SOLOMON ET AL.

Electron Transfer in Bioinorganic Chemistry

329

This work has been supported by National Science Foundation Grant CHE-9528250.

References 1. 2. 3. 4.

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27.

Lumry, R.; Eyring,H.J.Phys. Chem. 1954, 58, 110-120. Malmström,B.G.Eur. J. Biochem. 1994, 223, 711-718. Williams,R.J.Ρ.Eur. J. Biochem. 1995, 234, 363-381. Solomon, Ε. I.; Penfield, K. W.; Wilcox, D. E. Struct. Bonding (Berlin) 1983, 53, 1-57. Solomon, E. I.; Baldwin, M. J.; Lowery, M. D. Chem. Rev. 1992, 92, 521-542. Solomon, Ε. I.; Lowery, M . D. Science (Washington,D.C.)1993, 259, 15751581. Solomon, Ε. I.; Hare, J. W.; Gray, Η. B. Proc. Natl. Acad. Sci. U.S.A. 1976, 73, 1389-1392. Guss, J. M . Bartunik, H. D.; Freeman, H. C. Acta. Crystalbgr. 1992, B48, 790-811. Guss, J. M.; Freeman,H.C.J.Mol.Biol. 1986, 192, 361-381. Lowery, M . D.; Guckert, J. Α.; Gebhard, M. S.; Solomon, Ε. I. J. Am. Chem. Soc. 1993, 115, 3012-3013. Guckert, J. Α.; Lowery, M . D.; Solomon, Ε. I. J. Am. Chem. Soc. 1995, 117, 2817-2844. Bates, C. Α.; Moore, W. S.; Standley, K. J.; Stevens, K. W. H . Proc. Phys. Soc. Lon­ -don 1962, 79, 73-93. Shadle, S. E.; Penner-Hahn, J. E.; Schugar, H. J.; Hedman, B.; Hodgson, Κ. O.; Solomon, Ε. I. J. Am. Chem. Soc. 1993, 115, 767-776. Hahn, J. E.; Scott, R. Α.; Hodgson, K. O.; Doniach, S.; Desjardins, S. R.; Solomon, Ε. I. Chem. Phys. Lett. 1982, 88, 595-598. Penfield, K. W.; Gay, R. R.; Himmelwright, R. S.; Eickman, N. C.; Norris, V. Α.; Freeman, H. C.; Solomon,Ε.I.J.Am. Chem. Soc. 1981, 103, 4382-4388. Scott, R. Α.; Hahn, J. E.; Doniach, S.; Freeman, H. C.; Hodgson,K.O.J.Am. Chem. Soc. 1982, 104, 5364-5369. George, S. J.; Lowery, M. D.; Solomon, Ε. I. Cramer,S.P.J.Am. Chem. Soc. 1993, 115, 2968-2969. Didziulis, S. V.; Cohen, S. L.; Gewirth, Α. Α.; Solomon, Ε. I. J. Am. Chem. Soc. 1988, 110, 250-268. Hedman, B.; Hodgson, K. O.; Solomon, Ε. I. J. Am. Chem. Soc. 1990, 112, 1643-1645. Shadle, S. E.; Hedman, B.; Hodgson, K. O.; Solomon, Ε. I. Inorg. Chem. 1994, 33, 4235-4244. Shadle, S. E.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1995, 117, 2259-2272. Guss, J. M.; Freeman, H. C. J. Mol. Biol. 1983, 169, 521-563. Messerschmidt, Α.; Ladenstein, R.; Huber, R.; Bolognesi, M . ; Avigliano, L.; Petruzzelli, R.; Rossi, Α.; Finazzi-Agro, A. J. Mol. Biol. 1992, 224, 179-205. Godden, J. W.; Turley, S.; Teller, D. C.; Adman, Ε. T.; Liu, M . Y.; Payne, W. J.; Legall, J. Science (Washington,D.C.)1991, 253, 438-442. Didziulis,S.V.;Cohen, S. L.; Butcher, K. D.; Solomon,Ε.I.Inorg. Chem. 1988, 27, 2238-2250. Butcher, K. D.; Gebhard, M . S.; Solomon, Ε. I. Inorg. Chem. 1990, 29, 2067-2074. Butcher, K. D.; Didziulis, S. V.; Briat, B.; Solomon, Ε. I. Inorg. Chem. 1990, 29, 1626-1637. ;

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.

330

E L E C T R O N TRANSFER REACTIONS

Downloaded by IOWA STATE UNIV on September 27, 2013 | http://pubs.acs.org Publication Date: May 5, 1997 | doi: 10.1021/ba-1997-0253.ch019

28. Butcher, K. D.; Didziulis, S. V.; Briat, B.; Solomon, Ε. I. J. Am. Chem. Soc. 1990, 112, 2231-2242. 29. Murphy, L. M.; Hasnain, S. S.; Strange, R. W.; Harvey, I.; Ingledew, W. J. In X-ray Absorption Fine Structure; Hasnain, S. S., Ed.; Ellis Hardwood: Chichester, Eng­ -land,1990; p 152. 30. Sykes, A. G. Adv. Inorg. Chem. 1991, 36, 377-408.

In Electron Transfer Reactions; Isied, S.; Advances in Chemistry; American Chemical Society: Washington, DC, 1997.