Self-assembled complexes of oligopeptides and metalloporphyrins

Measurements of the reorganization and electronic interaction energies for photoinduced electron-transfer reactions

Mohamed Aoudia, Anton B. Guliaev, Neocles B. Leontis, Michael A J Rodgers

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Cationic porphyrins form ground state electrostatically associated complexes with anionic oligo-electrolytes such as those formed by a series of glutamic acid (E) residues. Temperature dependencies were measured of the rate constants for intra-complex electron transfer to the triplet state of Pd(II)TMPyP4+ from a tyrosine (tyr, Y) or tryptophan (trp, W) moiety connected to a glutamic acid tetramer. In complexes such as YE4, E2YE2, YE4G10E (G, glycine), and WE4 these data were used to estimate the reorganization energy (λ) and electronic interaction energy (H(DA)) relevant to the process. For all tyr-peptide complexes, λ values were found to be large (λ~1.60±0.06 eV), reflecting a relatively high medium polarity in the vicinity of tyr residues. It further indicates that the tyr residues in all oligo-peptides are exposed to the aqueous medium in a similar way irrespective of the position of the aromatic moiety in the peptide chain. A significantly lower λ value (λ=1.08 eV) was derived for the tryptophan-containing peptide complex, indicating a relatively higher hydrophobic character of trp compared to tyr. The electronic coupling matrix elements (H(DA)) derived for tyr-peptide complexes (5.1 meV for YE4, 5.4 meV for YE4G10E and 7.5 meV for E2YE2) were larger than that found for WE4 (1.1 meV). Molecular dynamics calculations were employed to obtain structural features of the porphyrin-peptide complexes. These showed average distances between the center of mass (COM) of the porphyrin ring and the center of mass of the amino acid aromatic ring of 816±140 pm (YE4), 800±80 pm (E2YE2), 900±130 pm (YE4G10E) and 970±160 pm (WE4). The molecular dynamics calculations were shown to be in good agreement with the experimentally determined electronic interaction energies, strongly suggesting that H(DA) is primarily responsible for the dependence of the electron-transfer rate constant (k(ET)) on the donor-acceptor separation distance and relative orientation. The higher H(DA) (7.55 meV) derived for tyr incorporated into the middle of the peptide backbone (E2YE2) was presumed to be associated with a higher degree of orbital overlap due to a more favorable ring-ring orientation. Overlap parameters (β derived for all peptide-porphyrin complexes were similar (~0.95±0.06 A-1), being in good agreement with most literature values for similar systems. Finally, the intra-complex electron-transfer ratio (k(trp)/k(tyr)) derived from flash photolysis experiments and the corresponding ratio derived from Marcus' theory combined with experimental data from the temperature-dependence investigations and electrochemical measurements were found to be in excellent agreement. This same consistency was found for the couple E4Y and E2YE2. The empirical expression (Moser and Dutton) governing the intraprotein electron-transfer rate constant in native systems combined with our experimental data (k(ET), λ, ΔG0) yielded tunneling pathway distances in excellent agreement with those arising from the molecular modeling studies. The exception was for the long peptide YE4G10E, for which the Quenched Molecular Dynamic (QMD) sampling technique was complicated and is probably inadequate. Copyright (C) 2000 Elsevier Science B.V.

Original languageEnglish
Pages (from-to)121-140
Number of pages20
JournalBiophysical Chemistry
Volume83
Issue number2
DOIs
Publication statusPublished - Jan 17 2000

Fingerprint

Metalloporphyrins
Oligopeptides
peptides
electron transfer
Electrons
Peptides
Porphyrins
electronics
porphyrins
interactions
Molecular Dynamics Simulation
Molecular dynamics
energy
Rate constants
glutamic acid
rings
tryptophan
molecular dynamics
Tryptophan
center of mass

Keywords

  • Electronic coupling
  • Metalloporphyrin
  • Oligopeptide
  • Photoinduced electron transfer
  • Reorganization energy

ASJC Scopus subject areas

  • Biochemistry
  • Physical and Theoretical Chemistry
  • Biophysics

Cite this

Self-assembled complexes of oligopeptides and metalloporphyrins : Measurements of the reorganization and electronic interaction energies for photoinduced electron-transfer reactions. / Aoudia, Mohamed; Guliaev, Anton B.; Leontis, Neocles B.; Rodgers, Michael A J.

In: Biophysical Chemistry, Vol. 83, No. 2, 17.01.2000, p. 121-140.

Research output: Contribution to journalArticle

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T1 - Self-assembled complexes of oligopeptides and metalloporphyrins

T2 - Measurements of the reorganization and electronic interaction energies for photoinduced electron-transfer reactions

AU - Aoudia, Mohamed

AU - Guliaev, Anton B.

AU - Leontis, Neocles B.

AU - Rodgers, Michael A J

PY - 2000/1/17

Y1 - 2000/1/17

N2 - Cationic porphyrins form ground state electrostatically associated complexes with anionic oligo-electrolytes such as those formed by a series of glutamic acid (E) residues. Temperature dependencies were measured of the rate constants for intra-complex electron transfer to the triplet state of Pd(II)TMPyP4+ from a tyrosine (tyr, Y) or tryptophan (trp, W) moiety connected to a glutamic acid tetramer. In complexes such as YE4, E2YE2, YE4G10E (G, glycine), and WE4 these data were used to estimate the reorganization energy (λ) and electronic interaction energy (H(DA)) relevant to the process. For all tyr-peptide complexes, λ values were found to be large (λ~1.60±0.06 eV), reflecting a relatively high medium polarity in the vicinity of tyr residues. It further indicates that the tyr residues in all oligo-peptides are exposed to the aqueous medium in a similar way irrespective of the position of the aromatic moiety in the peptide chain. A significantly lower λ value (λ=1.08 eV) was derived for the tryptophan-containing peptide complex, indicating a relatively higher hydrophobic character of trp compared to tyr. The electronic coupling matrix elements (H(DA)) derived for tyr-peptide complexes (5.1 meV for YE4, 5.4 meV for YE4G10E and 7.5 meV for E2YE2) were larger than that found for WE4 (1.1 meV). Molecular dynamics calculations were employed to obtain structural features of the porphyrin-peptide complexes. These showed average distances between the center of mass (COM) of the porphyrin ring and the center of mass of the amino acid aromatic ring of 816±140 pm (YE4), 800±80 pm (E2YE2), 900±130 pm (YE4G10E) and 970±160 pm (WE4). The molecular dynamics calculations were shown to be in good agreement with the experimentally determined electronic interaction energies, strongly suggesting that H(DA) is primarily responsible for the dependence of the electron-transfer rate constant (k(ET)) on the donor-acceptor separation distance and relative orientation. The higher H(DA) (7.55 meV) derived for tyr incorporated into the middle of the peptide backbone (E2YE2) was presumed to be associated with a higher degree of orbital overlap due to a more favorable ring-ring orientation. Overlap parameters (β derived for all peptide-porphyrin complexes were similar (~0.95±0.06 A-1), being in good agreement with most literature values for similar systems. Finally, the intra-complex electron-transfer ratio (k(trp)/k(tyr)) derived from flash photolysis experiments and the corresponding ratio derived from Marcus' theory combined with experimental data from the temperature-dependence investigations and electrochemical measurements were found to be in excellent agreement. This same consistency was found for the couple E4Y and E2YE2. The empirical expression (Moser and Dutton) governing the intraprotein electron-transfer rate constant in native systems combined with our experimental data (k(ET), λ, ΔG0) yielded tunneling pathway distances in excellent agreement with those arising from the molecular modeling studies. The exception was for the long peptide YE4G10E, for which the Quenched Molecular Dynamic (QMD) sampling technique was complicated and is probably inadequate. Copyright (C) 2000 Elsevier Science B.V.

AB - Cationic porphyrins form ground state electrostatically associated complexes with anionic oligo-electrolytes such as those formed by a series of glutamic acid (E) residues. Temperature dependencies were measured of the rate constants for intra-complex electron transfer to the triplet state of Pd(II)TMPyP4+ from a tyrosine (tyr, Y) or tryptophan (trp, W) moiety connected to a glutamic acid tetramer. In complexes such as YE4, E2YE2, YE4G10E (G, glycine), and WE4 these data were used to estimate the reorganization energy (λ) and electronic interaction energy (H(DA)) relevant to the process. For all tyr-peptide complexes, λ values were found to be large (λ~1.60±0.06 eV), reflecting a relatively high medium polarity in the vicinity of tyr residues. It further indicates that the tyr residues in all oligo-peptides are exposed to the aqueous medium in a similar way irrespective of the position of the aromatic moiety in the peptide chain. A significantly lower λ value (λ=1.08 eV) was derived for the tryptophan-containing peptide complex, indicating a relatively higher hydrophobic character of trp compared to tyr. The electronic coupling matrix elements (H(DA)) derived for tyr-peptide complexes (5.1 meV for YE4, 5.4 meV for YE4G10E and 7.5 meV for E2YE2) were larger than that found for WE4 (1.1 meV). Molecular dynamics calculations were employed to obtain structural features of the porphyrin-peptide complexes. These showed average distances between the center of mass (COM) of the porphyrin ring and the center of mass of the amino acid aromatic ring of 816±140 pm (YE4), 800±80 pm (E2YE2), 900±130 pm (YE4G10E) and 970±160 pm (WE4). The molecular dynamics calculations were shown to be in good agreement with the experimentally determined electronic interaction energies, strongly suggesting that H(DA) is primarily responsible for the dependence of the electron-transfer rate constant (k(ET)) on the donor-acceptor separation distance and relative orientation. The higher H(DA) (7.55 meV) derived for tyr incorporated into the middle of the peptide backbone (E2YE2) was presumed to be associated with a higher degree of orbital overlap due to a more favorable ring-ring orientation. Overlap parameters (β derived for all peptide-porphyrin complexes were similar (~0.95±0.06 A-1), being in good agreement with most literature values for similar systems. Finally, the intra-complex electron-transfer ratio (k(trp)/k(tyr)) derived from flash photolysis experiments and the corresponding ratio derived from Marcus' theory combined with experimental data from the temperature-dependence investigations and electrochemical measurements were found to be in excellent agreement. This same consistency was found for the couple E4Y and E2YE2. The empirical expression (Moser and Dutton) governing the intraprotein electron-transfer rate constant in native systems combined with our experimental data (k(ET), λ, ΔG0) yielded tunneling pathway distances in excellent agreement with those arising from the molecular modeling studies. The exception was for the long peptide YE4G10E, for which the Quenched Molecular Dynamic (QMD) sampling technique was complicated and is probably inadequate. Copyright (C) 2000 Elsevier Science B.V.

KW - Electronic coupling

KW - Metalloporphyrin

KW - Oligopeptide

KW - Photoinduced electron transfer

KW - Reorganization energy

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