Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase

Izumi Ishigami; Ariel Lewis-Ballester; Austin Echelmeier; Gerrit Brehm; Nadia A. Zatsepin; Thomas D. Grant; Jesse D. Coe; Stella Lisova; Garrett Nelson; Shangji Zhang; Zachary F. Dobson; Sébastien Boutet; Raymond G. Sierra; Alexander Batyuk; Petra Fromme; Raimund Fromme; John C.H. Spence; Alexandra Ros; Syun Ru Yeh; Denis L. Rousseau

doi:10.1073/pnas.1814526116

Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase

Izumi Ishigami, Ariel Lewis-Ballester, Austin Echelmeier, Gerrit Brehm, Nadia A. Zatsepin, Thomas D. Grant, Jesse D. Coe, Stella Lisova, Garrett Nelson, Shangji Zhang, Zachary F. Dobson, Sébastien Boutet, Raymond G. Sierra, Alexander Batyuk, Petra Fromme, Raimund Fromme, John C.H. Spence, Alexandra Ros, Syun Ru Yeh, Denis L. Rousseau

Research output: Contribution to journal › Article › peer-review

71 Scopus citations

Abstract

Cytochrome c oxidase (CcO) reduces dioxygen to water and harnesses the chemical energy to drive proton translocation across the inner mitochondrial membrane by an unresolved mechanism. By using time-resolved serial femtosecond crystallography, we identified a key oxygen intermediate of bovine CcO. It is assigned to the P _R -intermediate, which is characterized by specific redox states of the metal centers and a distinct protein conformation. The heme a ₃ iron atom is in a ferryl (Fe ⁴⁺ = O ²⁻ ) configuration, and heme a and Cu _B are oxidized while Cu _A is reduced. A Helix-X segment is poised in an open conformational state; the heme a farnesyl sidechain is H-bonded to S382, and loop-I-II adopts a distinct structure. These data offer insights into the mechanism by which the oxygen chemistry is coupled to unidirectional proton translocation.

Original language	English (US)
Pages (from-to)	3572-3577
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	9
DOIs	https://doi.org/10.1073/pnas.1814526116
State	Published - Feb 26 2019

Keywords

Bioenergetics
Catalytic intermediates
Complex IV
Crystallography
X-ray free electron laser

ASJC Scopus subject areas

General

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10.1073/pnas.1814526116

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Ishigami, I., Lewis-Ballester, A., Echelmeier, A., Brehm, G., Zatsepin, N. A., Grant, T. D., Coe, J. D., Lisova, S., Nelson, G., Zhang, S., Dobson, Z. F., Boutet, S., Sierra, R. G., Batyuk, A., Fromme, P., Fromme, R., Spence, J. C. H., Ros, A., Yeh, S. R., & Rousseau, D. L. (2019). Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase. Proceedings of the National Academy of Sciences of the United States of America, 116(9), 3572-3577. https://doi.org/10.1073/pnas.1814526116

Ishigami, I, Lewis-Ballester, A, Echelmeier, A, Brehm, G, Zatsepin, NA, Grant, TD, Coe, JD, Lisova, S, Nelson, G, Zhang, S, Dobson, ZF, Boutet, S, Sierra, RG, Batyuk, A, Fromme, P, Fromme, R, Spence, JCH, Ros, A, Yeh, SR & Rousseau, DL 2019, 'Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 9, pp. 3572-3577. https://doi.org/10.1073/pnas.1814526116

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abstract = " Cytochrome c oxidase (CcO) reduces dioxygen to water and harnesses the chemical energy to drive proton translocation across the inner mitochondrial membrane by an unresolved mechanism. By using time-resolved serial femtosecond crystallography, we identified a key oxygen intermediate of bovine CcO. It is assigned to the P R -intermediate, which is characterized by specific redox states of the metal centers and a distinct protein conformation. The heme a 3 iron atom is in a ferryl (Fe 4+ = O 2− ) configuration, and heme a and Cu B are oxidized while Cu A is reduced. A Helix-X segment is poised in an open conformational state; the heme a farnesyl sidechain is H-bonded to S382, and loop-I-II adopts a distinct structure. These data offer insights into the mechanism by which the oxygen chemistry is coupled to unidirectional proton translocation.",

keywords = "Bioenergetics, Catalytic intermediates, Complex IV, Crystallography, X-ray free electron laser",

author = "Izumi Ishigami and Ariel Lewis-Ballester and Austin Echelmeier and Gerrit Brehm and Zatsepin, {Nadia A.} and Grant, {Thomas D.} and Coe, {Jesse D.} and Stella Lisova and Garrett Nelson and Shangji Zhang and Dobson, {Zachary F.} and S{\'e}bastien Boutet and Sierra, {Raymond G.} and Alexander Batyuk and Petra Fromme and Raimund Fromme and Spence, {John C.H.} and Alexandra Ros and Yeh, {Syun Ru} and Rousseau, {Denis L.}",

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AU - Brehm, Gerrit

AU - Zatsepin, Nadia A.

AU - Grant, Thomas D.

AU - Coe, Jesse D.

AU - Lisova, Stella

AU - Nelson, Garrett

AU - Zhang, Shangji

AU - Dobson, Zachary F.

AU - Boutet, Sébastien

AU - Sierra, Raymond G.

AU - Batyuk, Alexander

AU - Fromme, Petra

AU - Fromme, Raimund

AU - Spence, John C.H.

AU - Ros, Alexandra

AU - Yeh, Syun Ru

AU - Rousseau, Denis L.

PY - 2019/2/26

Y1 - 2019/2/26

N2 - Cytochrome c oxidase (CcO) reduces dioxygen to water and harnesses the chemical energy to drive proton translocation across the inner mitochondrial membrane by an unresolved mechanism. By using time-resolved serial femtosecond crystallography, we identified a key oxygen intermediate of bovine CcO. It is assigned to the P R -intermediate, which is characterized by specific redox states of the metal centers and a distinct protein conformation. The heme a 3 iron atom is in a ferryl (Fe 4+ = O 2− ) configuration, and heme a and Cu B are oxidized while Cu A is reduced. A Helix-X segment is poised in an open conformational state; the heme a farnesyl sidechain is H-bonded to S382, and loop-I-II adopts a distinct structure. These data offer insights into the mechanism by which the oxygen chemistry is coupled to unidirectional proton translocation.

AB - Cytochrome c oxidase (CcO) reduces dioxygen to water and harnesses the chemical energy to drive proton translocation across the inner mitochondrial membrane by an unresolved mechanism. By using time-resolved serial femtosecond crystallography, we identified a key oxygen intermediate of bovine CcO. It is assigned to the P R -intermediate, which is characterized by specific redox states of the metal centers and a distinct protein conformation. The heme a 3 iron atom is in a ferryl (Fe 4+ = O 2− ) configuration, and heme a and Cu B are oxidized while Cu A is reduced. A Helix-X segment is poised in an open conformational state; the heme a farnesyl sidechain is H-bonded to S382, and loop-I-II adopts a distinct structure. These data offer insights into the mechanism by which the oxygen chemistry is coupled to unidirectional proton translocation.

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KW - Catalytic intermediates

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KW - Crystallography

KW - X-ray free electron laser

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Snapshot of an oxygen intermediate in the catalytic reaction of cytochrome c oxidase

Abstract

Keywords

ASJC Scopus subject areas

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