Electron tunneling through sensitizer wires bound to proteins

Matthew R. Hartings, Igor V. Kurnikov, Alexander R. Dunn, Jay R. Winkler, Harry B. Gray, Mark A Ratner

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

We report a quantitative theoretical analysis of long-range electron transfer through sensitizer wires bound in the active-site channel of cytochrome P450cam. Each sensitizer wire consists of a substrate group with high binding affinity for the enzyme active site connected to a ruthenium-diimine through a bridging aliphatic or aromatic chain. Experiments have revealed a dramatic dependence of electron transfer rates on the chemical composition of both the bridging group and the substrate. Using combined molecular dynamics simulations and electronic coupling calculations, we show that electron tunneling through perfluorinated aromatic bridges is promoted by enhanced superexchange coupling through virtual reduced states. In contrast, electron flow through aliphatic bridges occurs by hole-mediated superexchange. We have found that a small number of wire conformations with strong donor-acceptor couplings can account for the observed electron tunneling rates for sensitizer wires terminated with either ethylbenzene or adamantane. In these instances, the rate is dependent not only on electronic coupling of the donor and acceptor but also on the nuclear motion of the sensitizer wire, necessitating the calculation of average rates over the course of a molecular dynamics simulation. These calculations along with related recent findings have made it possible to analyze the results of many other sensitizer-wire experiments that in turn point to new directions in our attempts to observe reactive intermediates in the catalytic cycles of P450 and other heme enzymes.

Original languageEnglish
Pages (from-to)248-253
Number of pages6
JournalCoordination Chemistry Reviews
Volume254
Issue number3-4
DOIs
Publication statusPublished - Feb 2010

Fingerprint

Electron tunneling
electron tunneling
wire
Wire
proteins
Proteins
Molecular dynamics
Electrons
enzymes
electron transfer
Camphor 5-Monooxygenase
Enzymes
Adamantane
molecular dynamics
Ruthenium
Ethylbenzene
cytochromes
Computer simulation
Substrates
Cytochromes

Keywords

  • Bridge effects electron transfer
  • Conformational dynamics electron transfer
  • Cytochrome P450
  • Protein electron transfer

ASJC Scopus subject areas

  • Chemistry(all)

Cite this

Hartings, M. R., Kurnikov, I. V., Dunn, A. R., Winkler, J. R., Gray, H. B., & Ratner, M. A. (2010). Electron tunneling through sensitizer wires bound to proteins. Coordination Chemistry Reviews, 254(3-4), 248-253. https://doi.org/10.1016/j.ccr.2009.08.008

Electron tunneling through sensitizer wires bound to proteins. / Hartings, Matthew R.; Kurnikov, Igor V.; Dunn, Alexander R.; Winkler, Jay R.; Gray, Harry B.; Ratner, Mark A.

In: Coordination Chemistry Reviews, Vol. 254, No. 3-4, 02.2010, p. 248-253.

Research output: Contribution to journalArticle

Hartings, MR, Kurnikov, IV, Dunn, AR, Winkler, JR, Gray, HB & Ratner, MA 2010, 'Electron tunneling through sensitizer wires bound to proteins', Coordination Chemistry Reviews, vol. 254, no. 3-4, pp. 248-253. https://doi.org/10.1016/j.ccr.2009.08.008
Hartings, Matthew R. ; Kurnikov, Igor V. ; Dunn, Alexander R. ; Winkler, Jay R. ; Gray, Harry B. ; Ratner, Mark A. / Electron tunneling through sensitizer wires bound to proteins. In: Coordination Chemistry Reviews. 2010 ; Vol. 254, No. 3-4. pp. 248-253.
@article{4db18a4b9ebb4c5f85bc4f5b93368a25,
title = "Electron tunneling through sensitizer wires bound to proteins",
abstract = "We report a quantitative theoretical analysis of long-range electron transfer through sensitizer wires bound in the active-site channel of cytochrome P450cam. Each sensitizer wire consists of a substrate group with high binding affinity for the enzyme active site connected to a ruthenium-diimine through a bridging aliphatic or aromatic chain. Experiments have revealed a dramatic dependence of electron transfer rates on the chemical composition of both the bridging group and the substrate. Using combined molecular dynamics simulations and electronic coupling calculations, we show that electron tunneling through perfluorinated aromatic bridges is promoted by enhanced superexchange coupling through virtual reduced states. In contrast, electron flow through aliphatic bridges occurs by hole-mediated superexchange. We have found that a small number of wire conformations with strong donor-acceptor couplings can account for the observed electron tunneling rates for sensitizer wires terminated with either ethylbenzene or adamantane. In these instances, the rate is dependent not only on electronic coupling of the donor and acceptor but also on the nuclear motion of the sensitizer wire, necessitating the calculation of average rates over the course of a molecular dynamics simulation. These calculations along with related recent findings have made it possible to analyze the results of many other sensitizer-wire experiments that in turn point to new directions in our attempts to observe reactive intermediates in the catalytic cycles of P450 and other heme enzymes.",
keywords = "Bridge effects electron transfer, Conformational dynamics electron transfer, Cytochrome P450, Protein electron transfer",
author = "Hartings, {Matthew R.} and Kurnikov, {Igor V.} and Dunn, {Alexander R.} and Winkler, {Jay R.} and Gray, {Harry B.} and Ratner, {Mark A}",
year = "2010",
month = "2",
doi = "10.1016/j.ccr.2009.08.008",
language = "English",
volume = "254",
pages = "248--253",
journal = "Coordination Chemistry Reviews",
issn = "0010-8545",
publisher = "Elsevier",
number = "3-4",

}

TY - JOUR

T1 - Electron tunneling through sensitizer wires bound to proteins

AU - Hartings, Matthew R.

AU - Kurnikov, Igor V.

AU - Dunn, Alexander R.

AU - Winkler, Jay R.

AU - Gray, Harry B.

AU - Ratner, Mark A

PY - 2010/2

Y1 - 2010/2

N2 - We report a quantitative theoretical analysis of long-range electron transfer through sensitizer wires bound in the active-site channel of cytochrome P450cam. Each sensitizer wire consists of a substrate group with high binding affinity for the enzyme active site connected to a ruthenium-diimine through a bridging aliphatic or aromatic chain. Experiments have revealed a dramatic dependence of electron transfer rates on the chemical composition of both the bridging group and the substrate. Using combined molecular dynamics simulations and electronic coupling calculations, we show that electron tunneling through perfluorinated aromatic bridges is promoted by enhanced superexchange coupling through virtual reduced states. In contrast, electron flow through aliphatic bridges occurs by hole-mediated superexchange. We have found that a small number of wire conformations with strong donor-acceptor couplings can account for the observed electron tunneling rates for sensitizer wires terminated with either ethylbenzene or adamantane. In these instances, the rate is dependent not only on electronic coupling of the donor and acceptor but also on the nuclear motion of the sensitizer wire, necessitating the calculation of average rates over the course of a molecular dynamics simulation. These calculations along with related recent findings have made it possible to analyze the results of many other sensitizer-wire experiments that in turn point to new directions in our attempts to observe reactive intermediates in the catalytic cycles of P450 and other heme enzymes.

AB - We report a quantitative theoretical analysis of long-range electron transfer through sensitizer wires bound in the active-site channel of cytochrome P450cam. Each sensitizer wire consists of a substrate group with high binding affinity for the enzyme active site connected to a ruthenium-diimine through a bridging aliphatic or aromatic chain. Experiments have revealed a dramatic dependence of electron transfer rates on the chemical composition of both the bridging group and the substrate. Using combined molecular dynamics simulations and electronic coupling calculations, we show that electron tunneling through perfluorinated aromatic bridges is promoted by enhanced superexchange coupling through virtual reduced states. In contrast, electron flow through aliphatic bridges occurs by hole-mediated superexchange. We have found that a small number of wire conformations with strong donor-acceptor couplings can account for the observed electron tunneling rates for sensitizer wires terminated with either ethylbenzene or adamantane. In these instances, the rate is dependent not only on electronic coupling of the donor and acceptor but also on the nuclear motion of the sensitizer wire, necessitating the calculation of average rates over the course of a molecular dynamics simulation. These calculations along with related recent findings have made it possible to analyze the results of many other sensitizer-wire experiments that in turn point to new directions in our attempts to observe reactive intermediates in the catalytic cycles of P450 and other heme enzymes.

KW - Bridge effects electron transfer

KW - Conformational dynamics electron transfer

KW - Cytochrome P450

KW - Protein electron transfer

UR - http://www.scopus.com/inward/record.url?scp=71649086737&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=71649086737&partnerID=8YFLogxK

U2 - 10.1016/j.ccr.2009.08.008

DO - 10.1016/j.ccr.2009.08.008

M3 - Article

VL - 254

SP - 248

EP - 253

JO - Coordination Chemistry Reviews

JF - Coordination Chemistry Reviews

SN - 0010-8545

IS - 3-4

ER -