Ruffling in a Series of Nickel(II) meso-Tetrasubstituted Porphyrins as a Model for the Conserved Ruffling of the Heme of Cytochromes c

Metalloporphyrins undergo remarkable nonplanar distortions of the macrocycle that perturb the chemical and photochemical properties of these important protein cofactors. Further, the tertiary structure of the surrounding protein can manipulate these distortions as a means of regulating biological function. For cytochromes c, for example, an energetically unfavorable, conserved nonplanar distortion of the heme exists and likely plays a role in its electrontransfer function. The heme distortion is primarily of the ruffling (ruf) type (corresponding to the lowest frequency B_1u-symmetry normal mode) in which the pyrroles are twisted about the metal–N_pyrrole bond. This B_1u-symmetry nonplanar distortion is commonly observed in metalloporphyrin crystal structures, as are the saddling (sad) B_2u-symmetry distortion, waving (wav) E_g-symmetry distortions, and doming (dom) A_2u-symmetry distortion. Each of these nonplanar distortions is expected to result in unique alterations of the chemical and physical properties of the nominally planar porphyrin macrocycle. Symmetrical porphyrin substitution with tetrahedrally bonded atoms at the four meso bridging carbons generally results in the B_1u ruffling distortion; therefore, we investigated a series of meso-tetrasubstituted porphyrins for which the substituents vary in size (methyl, ethyl, propyl, pentyl, isopropyl, cyclopropyl derivative 11a, cyclohexyl, apopinenyl (10), tert-butyl, adamantyl), increasing the steric crowding at the periphery. Molecular mechanics calculations show increasing degree of ruffling (C_αNNC_α angle for opposite pyrroles varies from 0 to 57°) for this series of porphyrins, generally agreeing with the X-ray structures that are available. In addition, the frequencies of the structure-sensitive Raman lines decrease nonlinearly with increasing ruffling angle. The localization of the B_1u nonplanar distortion in only the C_α-C_m bond torsion (not the case for the B_2u sad distortion) suggests a means by which the B_1u distortion might be distinguished from other types of nonplanar distortion by using resonance Raman spectroscopy. Also, the size of the red shifts in the π → π* absorption bands depends on C_α–C_m torsion angle in a nonlinear fashion and the shift is accurately predicted by INDO/s molecular orbital calculations when the nonplanar structures obtained from molecular mechanics are used.