6944
J . Am. Chem. SOC.1987, 109, 6944-6947
Spectroscopy as a Tool for Studying Synthetic Oxygen Carriers Related to Biological Systems: Application to a Synthetic Single-Face Hindered Iron Porphyrin-Dioxygen Complex in Solution 170NMR
I. P. Gerothanassis*+and M. Momentem* Contribution from the Department of Chemistry, Section of Organic Chemistry and Biochemistry, University of Ioannina, 451 10 Ioannina, Greece, and Znstitut Curie, Section de Biologie. U 21 9 Inserm, Centre Universitaire, 91 405 Orsay Cedex, France. Received March 2, 1987
Abstract: The high-resolution ” 0 NMR spectrum of a single-face hindered iron porphyrin-dioxygen complex in solution is reported. T h e spectrum exhibits two well-resolved resonances of the FeO, moiety, with different line widths, in agreement with a n end-on structure proposed by Pauling for oxyhaemoglobin. Assignment of the two resonances was achieved on the basis of theoretical literature calculations. The experimental d a t a can be explained in terms of bonding models in which the electrons of the FeO, moiety a r e totally paired, without a charge transfer Fe(d5)02- superoxide configuration. An ozone-like bonding of the FeO, moiety is emphasized.
The structure of iron porphyrin-oxygen carriers, both natural and synthetic, and in particular the n a t u r e of t h e metal-oxygen bond have been debated for decades.’,* 170NMR spectroscopy can be considered as an excellent m e a n s t o derive direct information about binding, structure, and reactivity of the coordinated molecular oxygen. This spectroscopic tool, despite several inherent disadvantages, Le., low sensitivity, large line widths, and rolling base lines,3 has a t t r a c t e d considerable interest as applied t o dioxygen complexes due t o t h e availability of oxygen-17 enriched gas and the extremely large chemical shift range ( 1500 ppm) of the oxygen bonded t o transition metak3q4 However, it was only recently t h a t the first successful application of 1 7 0 NMR to a peroxo-type oxygen was reported by Postel et aL5after several unsuccessful 170NMR studies of oxyhaemoglobin6* and synthetic Vaska-type oxygen carrier^.^*'^ Postel et al.,5 however, painted a rather pessimistic picture of the future of I7O NMR spectroscopy as applied t o those 0, derivatives that bind molecular oxygen reversibly, a prognosis that has recently been ruled out by the 170 NMR observation of Vaska-type reversible complexes1’ (Lauterwein, J.; Gerothanassis I. P.; Schumacher, M., manuscript in
Chart I
N
preparation).
In the present work we report the first successful high-resolution ” 0 NMR s p e c t r u m of the FeO, linkage of a dioxygen-lmethylimidazole-iron (d6) porphyrin complex having one “handle” and two pivaloyl “pickets” as substituents ( C h a r t I). This sixcoordinated dioxygen a d d u c t h a s been shown t o b e stable and re~ersible.’~,’~ M a t e r i a l s and Methods The sample used in our study was prepared following a similar procedure to that published in ref 12. Gaseous oxygen containing 33 atom % oxygen-17 (Yeda-Stable Isotopes, Rehovot, Israel) was added in the toluene solution and the tube sealed (0,pressure - 5 atm). The N M R data were obtained with a Bruker AM-400 multinuclear spectrometer operating at 54.2 MHz for I’O. No field/frequency locking system was used. The temperature was adjusted with use of a calibrated thermoresistance introduced into the magnet by way of a cylindrical tube containing the same solvent. Chemical shifts were measured relative to 1,4-dioxane determined in separate replacement experiments. At 34 OC the chemical shift of dioxane is identical with that of H,O. Data manipulations were carried out on an Aspect-3000 computer. The following spectral parameters were used: spectral width = 100 KHz; 90’ pulse length = 30 ps; quadrature phase detection; acquisition time = 5 p s ; preacquisition delay At = 100 ps when the normal 90° pulse train sequence was used; no relaxation delay; zero-filling to 2 K before FT. In order to eliminate acoustic ringing problems several spectra at low temperatures were recorded with either the extended spin-echo pulse se‘University of Ioannina. t Centre Universitaire.
R = CO-(CH,)&O q ~ e n c e ’ ~or* ’the ~ reference-base line-substraction 90’ pulse s e q u e n ~ e l ~ * ’ ~ with practically negligible preacquisition and pulse delays. Because of the limited power of the 180° pulse over the entire spectral range, it was necessary to adjust the carrier frequency near the observed frequency. As a consequence, when the above pulse sequences were used, the 170 NMR spectrum had to be recorded in two steps.
Results and Discussion Chemical Shifts. Figure 1 shows t h e I7O NMR spectrum of the compound of C h a r t I at 34 O C . The spectrum exhibits two distinct resonances a t 1755 and 2488 ppm with an integral ratio of 1(1755)/1(2488) = 0.41 instead of t h e expected ratio (after (1) Jones, R. D.; Summerville, D. A,; Basolo, F. Chem. Rev. 1979, 79, 139-179. (2) Drago, R. S.;Corden, B. B. Acc. Chem. Res. 1980, 13, 353-360. (3) Kintzinger, J.-P. In NMR-Basic Principles and Progress; Diehl, P., Fluck, E., Kosfeld, R., Eds.; Springer: Berlin, 1981; Vol. 17, pp 1-64. (4) Klemperer, W. G. In The Multinuclear Approach to N M R Spectroscopy; Lambert, J. B., Riddell, F. G., Eds.; Reidel D.: Dordrecht, 1983; pp 245-260. (5) Postel, M.; Brevard, C.; Arzoumanian, H.; Riess, J. G. J . A m . Chem. SOC. 1983, 105, 4922-4926. (6) Maricic, S.;Leigh, J. S., Jr.; Sunko, D. E. Nature (London) 1967, 214, 462-466. (7) Pifat, G.;Maricic, S.;Petrinovic, M.; Kramer, V.;Marsel, J.; Bonhard, K. Croat. Chem. Acta 1969, 41, 195-203. (8) Irving, C. S . ; Lapidot, A. Nature (London) 1971, 230, 224. (9) Lapidot, A.; Irving, C. S. J. Chem. SOC., Dalton Tram. 1972,668-670. (IO) Lumpkin, 0.; Dixon, W. T.; Poser, J. Inorg. Chem. 1979, 18, 982-984. (11) Lee, H. H.; Oldfield, E. J . Magn. Reson. 1986, 69, 367-370. (12) Momenteau M.; Look, B.; Tetreau, C.; Lavalette, D.; Croisy, A.; Schaeffer, C.; Huel, C.; Lhoste, J.-M. J . Chem. SOC.,Perkin Trans. 2 1987, 249-257. (13) Momenteau, M. Pure Appl. Chem. 1986, 58, 1493-1502. (14) Gerothanassis, I. P.; Lauterwein, J. J . Magn. Reson. 1986.66, 32-42. (15) Gerothanassis, I. P. Progr. N M R Spectrosc. 1987, 19, 267-329. (16) Gerothanassis, I. P. Magn. Reson. Chem. 1986, 24, 428-433.
0002-7863/87/1509-6944%01.50/0 0 1987 American Chemical Society
J . Am. Chem. SOC.,Vol. 109, No. 23, 1987 6945
Study of Synthetic Oxygen Carriers
1?SO
ZSDO
lono rrn
2zsn
I7SC
ISCC
-
Figure 1. I7O N M R spectrum (54.2 MHz) of the compound of Chart I with use of the normal 90° pulse train sequence. Concentration IO-, M in toluene solution. Concentration of 1-methylimidazole -2.5 X 10-' M. T = 34 OC, number of scans -1.2 X lo6, linebroadening filtering LB = 500 Hz, total experimental time ca. 100 min. Upper trace: Simulation of the I7O resonances with a Lorentzian line shape. The symbol
t
indicates the position of the transmitter carrier frequency.
Chart 11. Pauling Model for the FeO, Moiety lo\ \
'1
according to Maricic et a1.,6 in a chemical shift A6 N 1500 ppm. For structure I, A6 E 110 ppm. Assuming an equal contribution of each hybrid structure then, A6 = 805 ppm which is in excellent agreement with the experimental value of 733 ppm. However, the chemical shifts 6, and b2 of the individual oxygens are too low compared with the experimental values. Velenic and Lynden-BellZ4suggested that the methodology employed by Maricic et aL6 is not suitable for the estimation of I7O chemical shifts. They proposed that reasonable estimates can be obtained from an extended Hiickel method.25 The dioxygen ligand was considered as an independent unit and significant electron transfer between oxygen and iron was supposed not to occur. According to these calculations both oxygen nuclei exhibit chemical shifts to high frequency at least 1000 ppm relative to H 2 0 . The nucleus of the oxygen atom 2 near the iron atom (Chart 11) was found to be more shielded than the nucleus of the terminal oxygen 1 by about 1400 to 1500 ppm. This shift, A6, between the two nuclei is remarkably constant and independent of the value of the charge q on the oxygen nucleus 2 and the splitting AE of the degenerate a orbitals of the oxygen atom on complexing. However, the magnitudes of 6,and a2 critically depend on both values q and AE. Thus for AE = 1.04 eV and q = 0.19 e, 6, = 3224 ppm and 62 = 1647 ppm; for AE = 0.20 eV and q = 0.029 e, 6, = 13 216 ppm and b2 = 11 844 ppm. The former value is in reasonable agreement with our experimental data. According to Velenic and L ~ n d e n - B e lthe l ~ ~calculated chemical 1500 ppm) of the two nuclei is likely to shift difference (A6 be correct to f 5 0 0 ppm and would probably be enhanced by electron delocalization. Although it is difficult to know how much faith to put on assignments based on theoretical calculations with such a considerable amount of uncertainty, we should emphasize that the above assignment is also supported by the oxygen chemical shifts of the ozone molecule (see discussion below). Line Widths: Nuclear Quadrupole Coupling Constants. In diamagnetic solutions the I7O nucleus ( I = 5/2; quadrupole moment Q = -0.026 X loz8mZ)relaxes predominantly by the quadrupolar mechanism. In the motional narrowing limit, uo272
