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How O-2 binds to heme - Reasons for rapid binding and spin inversion

Jensen, Kasper LU and Ryde, Ulf LU (2004) In Journal of Biological Chemistry 279(15). p.14561-14569
Abstract
We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O-2 to a realistic model of ferrous deoxyheme. Beyond a Fe-O distance of similar to 2.5 Angstrom, we find a broad crossing region with five electronic states within 15 kJ/mol. The almost parallel surfaces strongly facilitate spin inversion, which is necessary in the reaction of O-2 with heme ( deoxyheme is a quintet and O-2 a triplet, whereas oxyheme is a singlet). Thus, despite a small spin-orbit coupling in heme, the transition probability approaches unity. Using reasonable parameters, we estimate a transition probability of 0.06-1, which is at least 15 times larger than for the... (More)
We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O-2 to a realistic model of ferrous deoxyheme. Beyond a Fe-O distance of similar to 2.5 Angstrom, we find a broad crossing region with five electronic states within 15 kJ/mol. The almost parallel surfaces strongly facilitate spin inversion, which is necessary in the reaction of O-2 with heme ( deoxyheme is a quintet and O-2 a triplet, whereas oxyheme is a singlet). Thus, despite a small spin-orbit coupling in heme, the transition probability approaches unity. Using reasonable parameters, we estimate a transition probability of 0.06-1, which is at least 15 times larger than for the nonbiological Fe-O+ system. Spin crossing is anticipated between the singlet ground state of bound oxyheme, the triplet and septet dissociation states, and a quintet intermediate state. The fact that the quintet state is close in energy to the dissociation couple is of biological importance, because it explains how both spin states of O-2 may bind to heme, thereby increasing the overall efficiency of oxygen binding. The activation barrier is estimated to be < 15 kJ/mol based on our results and Mossbauer experiments. Our results indicate that both the activation energy and the spin-transition probability are tuned by the porphyrin as well as by the choice of the proximal heme ligand, which is a histidine in the globins. Together, they may accelerate O-2 binding to iron by &SIM;10(11) compared with the Fe-O+ system. A similar near degeneracy between spin states is observed in a ferric deoxyheme model with the histidine ligand hydrogen bonded to a carboxylate group, i.e. a model of heme peroxidases, which bind H2O2 in this oxidation state. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Journal of Biological Chemistry
volume
279
issue
15
pages
14561 - 14569
publisher
ASBMB
external identifiers
  • wos:000220594700013
  • scopus:2442616950
ISSN
1083-351X
DOI
10.1074/jbc.M314007200
language
English
LU publication?
yes
id
06123783-8870-448e-bb59-f9f3638132ce (old id 139692)
date added to LUP
2007-07-17 11:03:00
date last changed
2017-11-26 03:15:37
@article{06123783-8870-448e-bb59-f9f3638132ce,
  abstract     = {We have used density functional methods to calculate fully relaxed potential energy curves of the seven lowest electronic states during the binding of O-2 to a realistic model of ferrous deoxyheme. Beyond a Fe-O distance of similar to 2.5 Angstrom, we find a broad crossing region with five electronic states within 15 kJ/mol. The almost parallel surfaces strongly facilitate spin inversion, which is necessary in the reaction of O-2 with heme ( deoxyheme is a quintet and O-2 a triplet, whereas oxyheme is a singlet). Thus, despite a small spin-orbit coupling in heme, the transition probability approaches unity. Using reasonable parameters, we estimate a transition probability of 0.06-1, which is at least 15 times larger than for the nonbiological Fe-O+ system. Spin crossing is anticipated between the singlet ground state of bound oxyheme, the triplet and septet dissociation states, and a quintet intermediate state. The fact that the quintet state is close in energy to the dissociation couple is of biological importance, because it explains how both spin states of O-2 may bind to heme, thereby increasing the overall efficiency of oxygen binding. The activation barrier is estimated to be &lt; 15 kJ/mol based on our results and Mossbauer experiments. Our results indicate that both the activation energy and the spin-transition probability are tuned by the porphyrin as well as by the choice of the proximal heme ligand, which is a histidine in the globins. Together, they may accelerate O-2 binding to iron by &amp;SIM;10(11) compared with the Fe-O+ system. A similar near degeneracy between spin states is observed in a ferric deoxyheme model with the histidine ligand hydrogen bonded to a carboxylate group, i.e. a model of heme peroxidases, which bind H2O2 in this oxidation state.},
  author       = {Jensen, Kasper and Ryde, Ulf},
  issn         = {1083-351X},
  language     = {eng},
  number       = {15},
  pages        = {14561--14569},
  publisher    = {ASBMB},
  series       = {Journal of Biological Chemistry},
  title        = {How O-2 binds to heme - Reasons for rapid binding and spin inversion},
  url          = {http://dx.doi.org/10.1074/jbc.M314007200},
  volume       = {279},
  year         = {2004},
}