J . Am. Chem. SOC.1989, 111, 6183-6195
6183
Models for Iron-Oxo Proteins. Structures and Properties of FeIIFeIII, Zn"Fe'I*, and Fe"Ga"' Complexes with (p-Phenoxo)bis(p-carboxy1ato)dimetal Cores A. S. Borovik,+ Vasilios Papaefthymiou,l Lucille F. Taylor,$ Oren P. Anderson,*,$and Lawrence Que, Jr.*.+ Contribution from the Department of Chemistry, University of Minnesota, Minneapolis, Minnesota 55455, Department of Chemistry, Colorado State University, Fort Collins, Colorado 80523, and Gray Freshwater Biological Institute, University of Minnesota, Navarre, Minnesota 55392. Received December 12, 1988
Abstract: A series of bimetallic complexes, [M11M'"'BPMP(02CR)2]X2 where BPMP is the anion of 2,6-bis[(bis(2pyridylmethyl)amino)methyl]-4-methylphenol,has been synthesized to provide models for binuclear metal-oxo centers in proteins (1, M = M' = Fe, R = C2H5,X = BPh4; 2, M = M' = Fe, R = C6HS,X = PF6; 3, M = Fe, M' = Ga, R = C2H5, X = BPh4; 4, M = Zn, M' = Fe, R = CH,, X = BPh4; 5, M = Zn, M' = Fe, R = C2H5, X = BPh4). The complexes 1' (1.CH3COCH3. 0.5CH3CN) and 4' ( 4 C H 3 C N ) have been characterized by X-ray diffraction methods as having (r-phenoxo)bis(p carboxy1ato)dimetal cores. Both 1' and 4' crystallize in the triclinic space group PT with the following unit cell parameters: for l', a = 13.489 (9) A, b = 13.514 (6) A, c = 25.258 (15) A, (Y = 77.23 (4)O, /3 = 77.89 ( S ) O , y = 61.43 (4)O, and Z = 2; for 4', a = 12.914 (4) A, b = 14.991 (3) A, = 20.736 (6) A, (Y = 101.66 ( 2 ) O , /3 = 106.84 (2)O, y = 100.19 (2)', and Z = 2. The metal centers in the mixed valence complex 1' are ordered as indicated by the differences in the Fe-O bond lengths; these match well with Fe"'-O and Fell-0 bond lengths in complexes of established structure and valence. The metal centers in 4' exhibit differences in Fe-O and Zn-O bond lengths, but the crystallographic analysis suggests the presence of some disorder in the metal occupancies in this case. The Fe"Ee"' complexes have been characterized by electronic spectral, Mossbauer, EPR, N M R , and electrochemical methods. The assignment of these properties to the individual iron centers is facilitated by the availability of the analogous heterobimetallic complexes wherein one of the paramagnetic centers in the mixed valence complex is replaced with a diamagnetic center of corresponding charge, i t . , Zn" for Fe" or Gall' for Fe"' Thus, 1 exhibits electronic spectral features near 385, 554, and 1350 nm, assigned to Fe"-to-pyridine, phenolate-to-Fe"', and intervalence charge-transfer transitions, respectively. Its N M R spectrum exhibits sharp, isotropically shifted resonances, which number half of that expected for a valence-trapped species; this indicates that electron transfer between the metal centers is fast on the N M R time scale under ambient conditions. Its Mossbauer spectrum at temperatures below 200 K, on the other hand, shows features indicative of trapped valences. Taken together, the N M R , Mossbauer, and electronic spectral data classify 1 as a class I1 mixed valence complex in the Robin-Day scheme. In contrast, the valences appear trapped in the solid state, even at room temperature, as indicated by crystallographic and Mossbauer data. 1 exhibits reversible one-electron waves at +692 and -1 0 mV versus SCE, corresponding to the Fe"'Fe"'/Fe"Fe"' and FellFelll/FellFell couples, respectively. The high potential of the first wave, which is also observed for the corresponding Fe"Ga"'-bis(propionate) and Mn"Mn"'-bis(acetate) complexes, emphasizes the point that the BPMP/bis(carboxylate) ligand combination appears to stabilize a total metal charge of +5. Lastly, 1 exhibits a broad EPR signal centered near g = 1.6, which is not observed in either the analogous Zn"Fe"' or Fe"Ga"' complexes. This signal is similar to those observed for the mixed valence forms of binuclear iron-oxo proteins.
c
In recent years, binuclear iron-oxo centers have emerged as a common structural component in the active sites of several metalloproteins.' These centers have important functional roles in hemerythrin,2 ribonucleotide r e d ~ c t a s e ,methane ~ monoo x y g e n a ~ e and , ~ the purple acid phosphatase^.^ T h e binuclear centers in such proteins are known or are postulated to exist in either a n oxidized (Fe"'Fe"'), a reduced (Fe"Fe"), or a mixed valence (Fe"Fe"') form. T h e prototype and best characterized member of this class of proteins is hemerythrin (Hr), a respiratory protein found in some marine invertebrates. In particular, the FeII'Fe"' form has been shown by crystallographic and spectroscopic studies to have a (p-oxo)bis(pcarboxylato)diiron core.1,2,6 This structure has been reproduced in synthetic Fe"'Fe"' complexes by spontaneous self-assembly methods, thus illustrating the thermodynamic stability of this triply bridged binuclear unit.' Diiron complexes of this type have served as excellent models for the structural and spectroscopic properties of the oxidized form of binuclear iron proteins. T h e structures of the diiron centers in the reduced and mixed valence forms are less well understood. For deoxyhemerythrin (deoxyHr), a variety of physical measurements suggest that the triply bridged unit is retained, with the oxo group being protonated to give a (phydroxo)bis(pcarboxylato)diiron(II,II) ~ o r e . ' . ~I,t ~ appears that this structure may also be present in the Fe"Fe"' 'University of Minnesota, Minneapolis. *ColoradoState University. University of Minnesota, Navarre. 0002-7863/89/1511-6183$01.50/0
(semimet) forms of hemerythrin,I0 which can be generated either from the oxidation of deoxyHr or reduction of metHr,Il yet efforts (1) (a) Que, L., Jr.; Scarrow, R. C. In Metal Clusters i n Proteins; Que, L., Jr., Ed.; ACS Symposium Series 372; American Chemical Society: Washington DC, 1988; pp 159-178. (b) Lippard, S. J. Angew. Chem., Intl. Ed. Engl. 1988, 27, 344-361. (2) Wilkins, P. C.; Wilkins, R. G. Coord. Chem. Reu. 1987, 79, 195-214. (3) Reichard, P.; Ehrenberg, A. Science (Washington, D.C.) 1983, 221, 5 14-5 19. (4) (a) Woodland, M. P.; Patil, D. S.; Cammack, R.; Dalton, H. Biochim. Biophys. Acta 1986,873, 237-242. ( b )Prince, R. C.; George, G. N.; Savas, J. C.; Cramer, S. P.; Pate!, R. N. Biochim. Biophys. Acta 1988, 952, 220-229. (c) Ericson, A,; Hedman, B.; Hcdgson, K. 0.;Green, J.; Dalton, H.; Bentsen, J. G.; Beer, R. H.; Lippard, S . J. J . A m . Chem. SOC.1988, 110, 2330-2332. (d) Fox, B. G.; Surerus, K. K.; Miinck, E.; Lipscomb, J . D. J . B i d . Chem. 1988, 263, 10553-10556. (5) (a) Antanaitis, B. C.; Aisen, P. Adu. Inorg. Biochem. 1983,5, 111-136. (b) Averil!, B. A,; Davis, J. C.; Burman, S . ; Zirino, T.; Sanders-Loehr, J.; Loehr, T. M.; Sage, J. T.; Debrunner, P. G.J . Am. Chem. SOC.1987, 109, 3760-3161. (6) (a) Stenkamp, R. E.; Sieker, L. C.; Jensen, L. H. J . Am. Chem. SOC. 1984,106, 618-622. (b) Sheriff, S.;Hendrickson, W. A,; Smith, J. L. J . Mol. Biol. 1987, 197, 273-296. ( 7 ) (a) Armstrong, W. H.; Spool, A,; Papaefthymiou, G.C.; Frankel, R. B.; Lippard, S. J. J . A m . Chem. SOC.1984, 106, 3653-3667. (b) Wieghardt, K.; Pohl, K.; Gebert, W. Angew. Chem., Intl. Ed. Engl. 1983, 22, 727-728. (c) Spool, A,; Williams, I. D.; Lippard, S . J. fnorg. Chem. 1985, 24, 2156-2162. (d) Toftlund, H.; Murray, K. S.; Zwack, P. R.; Taylor, L. F.; Anderson, 0. P. J . Chem. Soc., Chem. Commun. 1986, 191-193. ( e ) Gomez-Romero, P.; Casan-Pator, N.; Ben-Hussein, A.; Jameson, G. J . Am. Chem. SOC.1988, 110, 1988-1990. (8) Zhang, K.; Stern, E. A,; Ellis, F.; Sanders-Loehr, J.; Shiemke, A. K . Biochemistry 1988, 27, 7470-1479.
0 1989 American Chemical Society
61 84 J. Am. Chem. SOC.,Vol. 1 I I , No. 16, 1989
Borovik et al.
to obtain conclusive structural results for semimethemerythrins bridged core. Preliminary accounts of these results have previously have been hampered because of their thermodynamic instability. been T h e semimethemerythrins have distinct E P R signals with g,, = Experimental Section 13,llas do corresponding forms of methane m o n o ~ x y g e n a s e ~ ~ ~ ~ All reagents and solvents were purchased from commercial sources and purple acid p h o ~ p h a t a s e .The ~ g,, value of
