Ruffling in a series of nickel(II) mesco-tetrasubstituted porphyrins as a model for the conserved ruffling of the heme of cytochromes c

W. Jentzen, M. C. Simpson, J. D. Hobbs, X. Song, T. Ema, Tadashi Ema, C. J. Medforth, K. M. Smith, M. Veyrat, M. Mazzanti, R. Ramasseul, J. C. Marchon, T. Takeuchi, W. A. Goddard, J. A. Shelnutt

Research output: Contribution to journalArticle

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Abstract

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 electron-transfer function. The heme distortion is primarily of the ruffling (ruf) type (corresponding to the lowest frequency B1U-symmetry normal mode) in which the pyrroles are twisted about the metal-Npyrrole bond. This B1u-symmetry nonplanar distortion is commonly observed in metalloporphyrin crystal structures, as are the saddling (sad) B2u-symmetry distortion, waving (wav) Eg-syrnmetry distortions, and doming (dom) A2U-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 B1U 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 Ha, cyclohexyl, apopinenyl (10), fert-butyl, adamantyl), increasing the steric crowding at the periphery. Molecular mechanics calculations show increasing degree of ruffling (CaNNCα 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 B1U nonplanar distortion in only the CΝ-Cm bond torsion (not the case for the B2U sad distortion) suggests a means by which the B1U 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 Cα-Cm 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.

Original languageEnglish
Pages (from-to)11085-11097
Number of pages13
JournalJournal of the American Chemical Society
Volume117
Issue number45
Publication statusPublished - Nov 15 1995
Externally publishedYes

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Porphyrins
Cytochromes c
Nickel
Heme
Metalloporphyrins
Proteins
Pyrroles
Mechanics
Raman Spectrum Analysis
Molecular Structure
Tertiary Protein Structure
Carbon
Metals
X-Rays
Electrons
Molecular mechanics
Torsional stress
Orbital calculations
Crystal symmetry
Molecular orbitals

ASJC Scopus subject areas

  • Chemistry(all)

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Ruffling in a series of nickel(II) mesco-tetrasubstituted porphyrins as a model for the conserved ruffling of the heme of cytochromes c. / Jentzen, W.; Simpson, M. C.; Hobbs, J. D.; Song, X.; Ema, T.; Ema, Tadashi; Medforth, C. J.; Smith, K. M.; Veyrat, M.; Mazzanti, M.; Ramasseul, R.; Marchon, J. C.; Takeuchi, T.; Goddard, W. A.; Shelnutt, J. A.

In: Journal of the American Chemical Society, Vol. 117, No. 45, 15.11.1995, p. 11085-11097.

Research output: Contribution to journalArticle

Jentzen, W, Simpson, MC, Hobbs, JD, Song, X, Ema, T, Ema, T, Medforth, CJ, Smith, KM, Veyrat, M, Mazzanti, M, Ramasseul, R, Marchon, JC, Takeuchi, T, Goddard, WA & Shelnutt, JA 1995, 'Ruffling in a series of nickel(II) mesco-tetrasubstituted porphyrins as a model for the conserved ruffling of the heme of cytochromes c', Journal of the American Chemical Society, vol. 117, no. 45, pp. 11085-11097.
Jentzen, W. ; Simpson, M. C. ; Hobbs, J. D. ; Song, X. ; Ema, T. ; Ema, Tadashi ; Medforth, C. J. ; Smith, K. M. ; Veyrat, M. ; Mazzanti, M. ; Ramasseul, R. ; Marchon, J. C. ; Takeuchi, T. ; Goddard, W. A. ; Shelnutt, J. A. / Ruffling in a series of nickel(II) mesco-tetrasubstituted porphyrins as a model for the conserved ruffling of the heme of cytochromes c. In: Journal of the American Chemical Society. 1995 ; Vol. 117, No. 45. pp. 11085-11097.
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abstract = "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 electron-transfer function. The heme distortion is primarily of the ruffling (ruf) type (corresponding to the lowest frequency B1U-symmetry normal mode) in which the pyrroles are twisted about the metal-Npyrrole bond. This B1u-symmetry nonplanar distortion is commonly observed in metalloporphyrin crystal structures, as are the saddling (sad) B2u-symmetry distortion, waving (wav) Eg-syrnmetry distortions, and doming (dom) A2U-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 B1U 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 Ha, cyclohexyl, apopinenyl (10), fert-butyl, adamantyl), increasing the steric crowding at the periphery. Molecular mechanics calculations show increasing degree of ruffling (CaNNCα 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 B1U nonplanar distortion in only the CΝ-Cm bond torsion (not the case for the B2U sad distortion) suggests a means by which the B1U 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 Cα-Cm 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.",
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T1 - Ruffling in a series of nickel(II) mesco-tetrasubstituted porphyrins as a model for the conserved ruffling of the heme of cytochromes c

AU - Jentzen, W.

AU - Simpson, M. C.

AU - Hobbs, J. D.

AU - Song, X.

AU - Ema, T.

AU - Ema, Tadashi

AU - Medforth, C. J.

AU - Smith, K. M.

AU - Veyrat, M.

AU - Mazzanti, M.

AU - Ramasseul, R.

AU - Marchon, J. C.

AU - Takeuchi, T.

AU - Goddard, W. A.

AU - Shelnutt, J. A.

PY - 1995/11/15

Y1 - 1995/11/15

N2 - 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 electron-transfer function. The heme distortion is primarily of the ruffling (ruf) type (corresponding to the lowest frequency B1U-symmetry normal mode) in which the pyrroles are twisted about the metal-Npyrrole bond. This B1u-symmetry nonplanar distortion is commonly observed in metalloporphyrin crystal structures, as are the saddling (sad) B2u-symmetry distortion, waving (wav) Eg-syrnmetry distortions, and doming (dom) A2U-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 B1U 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 Ha, cyclohexyl, apopinenyl (10), fert-butyl, adamantyl), increasing the steric crowding at the periphery. Molecular mechanics calculations show increasing degree of ruffling (CaNNCα 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 B1U nonplanar distortion in only the CΝ-Cm bond torsion (not the case for the B2U sad distortion) suggests a means by which the B1U 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 Cα-Cm 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.

AB - 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 electron-transfer function. The heme distortion is primarily of the ruffling (ruf) type (corresponding to the lowest frequency B1U-symmetry normal mode) in which the pyrroles are twisted about the metal-Npyrrole bond. This B1u-symmetry nonplanar distortion is commonly observed in metalloporphyrin crystal structures, as are the saddling (sad) B2u-symmetry distortion, waving (wav) Eg-syrnmetry distortions, and doming (dom) A2U-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 B1U 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 Ha, cyclohexyl, apopinenyl (10), fert-butyl, adamantyl), increasing the steric crowding at the periphery. Molecular mechanics calculations show increasing degree of ruffling (CaNNCα 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 B1U nonplanar distortion in only the CΝ-Cm bond torsion (not the case for the B2U sad distortion) suggests a means by which the B1U 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 Cα-Cm 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.

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