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)
Please use this url to cite or link to this publication:
https://lup.lub.lu.se/record/139692
- author
- Jensen, Kasper
LU
and Ryde, Ulf
LU
- organization
- publishing date
- 2004
- type
- Contribution to journal
- publication status
- published
- subject
- in
- Journal of Biological Chemistry
- volume
- 279
- issue
- 15
- pages
- 14561 - 14569
- publisher
- American Society for Biochemistry and Molecular Biology
- external identifiers
-
- wos:000220594700013
- scopus:2442616950
- ISSN
- 1083-351X
- DOI
- 10.1074/jbc.M314007200
- language
- English
- LU publication?
- yes
- additional info
- The information about affiliations in this record was updated in December 2015. The record was previously connected to the following departments: Theoretical Chemistry (S) (011001039)
- id
- 06123783-8870-448e-bb59-f9f3638132ce (old id 139692)
- date added to LUP
- 2016-04-01 11:40:32
- date last changed
- 2023-01-10 08:57:37
@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 < 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.}},
author = {{Jensen, Kasper and Ryde, Ulf}},
issn = {{1083-351X}},
language = {{eng}},
number = {{15}},
pages = {{14561--14569}},
publisher = {{American Society for Biochemistry and Molecular Biology}},
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}},
doi = {{10.1074/jbc.M314007200}},
volume = {{279}},
year = {{2004}},
}