Large scale domain movement in cytochrome bc1: a new device for electron transfer in proteins

Darrouzet, Élisabeth; Moser, Christopher C.; Dutton, P. Leslie; Daldal, Fevzi

doi:10.1016/s0968-0004(01)01897-7

Cited by 133 publications

(116 citation statements)

References 44 publications

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“…Apparently, even when the FeS domain moves unperturbedly (microseconds), the risk of an occurrence of the state with SQ at the Q o site and FeS away from the site does exist, as reflected by the various levels of superoxide production seen in the wild type and the c 1 knockout. 4 Indeed, the variations in the production of superoxide by cytochrome bc 1 observed by us and others could reflect variations in the distribution of all states described in Figure 4 and, thus, result from reactions involving SQ o produced in both semiforward and semireverse reactions. It is, however, worth mentioning that there is one significant difference between the states encountered by the enzyme after formation of SQ o in semiforward and semireverse reactions.…”

Section: Competition Of Short-circuits With Leaks On Oxygen During Thmentioning

confidence: 72%

Movement of the Iron−Sulfur Head Domain of Cytochrome bc₁ Transiently Opens the Catalytic Q_o Site for Reaction with Oxygen

2008

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Cytochrome bc 1 , a key enzyme of biological energy conversion, generates or uses a proton motive force through the Q cycle that operates within the two chains of cofactors that embed two catalytic quinone oxidation/reduction sites, the Q o site and the Q i site. The Q o site relies on the joint action of two cofactors, the iron-sulfur (FeS) cluster and heme b L . Side reactions of the Q cycle involve a generation of superoxide which is commonly thought to be a product of an oxidation of a highly unstable semiquinone formed in the Q o site (SQ o ), but the overall mechanism of superoxide generation remains poorly understood. Here, we use selectively modified chains of cytochrome bc 1 to clearly isolate states linked with superoxide production. We show that this reaction takes place under severely impeded electron flow that traps heme b L in the reduced state and reflects a probability with which a single electron on SQ o is capable of reducing oxygen. SQ o gains this capability only when the FeS head domain, as a part of a catalytic cycle, transiently leaves the Q o site to communicate with the outermost cofactor, cytochrome c 1 . This increases the distance between the FeS cluster and the remaining portion of the Q o site, reducing the likelihood that the FeS cluster participates in an immediate removal of SQ o . In other states, the presence of both the FeS cluster and heme b L in the Q o site increases the probability of completion of short-circuit reactions which retain single electrons within the enzyme instead of releasing them on oxygen. We propose that in this way, cytochrome bc 1 under conditions of impeded electron flow employs the leak-proof short-circuits to minimize the unwanted single-electron reduction of oxygen.In respiratory and photosynthetic systems that couple electron transfer with a transmembrane proton gradient driving ATP production (1), cytochrome bc 1 (mitochondrial complex III) uses the Q cycle (2, 3) to catalyze electron transfer between quinone and cytochrome c. During the Q cycle, a reversible oxidation of quinol in the catalytic Q o site delivers one electron into the high-potential c-chain and the other into the low-potential b-chain. This reaction which is unique in biology relies on the energetic coupling of the two reduction/oxidation reactions, one involving the FeS 1 center of the c-chain and the other heme b L of the b-chain. The electrons are then exchanged between the FeS center and heme c 1 in the c-chain and among heme b L , heme b H , and the other quinone catalytic Q i site in the b-chain (Figure 1a) (3, 4). It appears that the two chains of cytochrome bc 1 have evolved to favor those productive electron transfers over the energy-wasting short-circuits of direct exchange of electrons between the chains or the uncontrolled leaks of electrons that produce damaging superoxide (5-9). Indeed, the enzyme working unperturbedly under driving force provided by substrates, quinol and cytochrome c, does not produce superoxide at detectable levels. This, however, may cha...

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Section: Competition Of Short-circuits With Leaks On Oxygen During Thmentioning

confidence: 72%

Movement of the Iron−Sulfur Head Domain of Cytochrome bc₁ Transiently Opens the Catalytic Q_o Site for Reaction with Oxygen

2008

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“…The ubihydroquinone : cytochrome (cyt) c oxidoreductase (or cyt bc 1 ), is a multi subunit membrane integral enzyme encountered in a broad variety of prokaryotic and eukaryotic organisms (for reviews see Darrouzet et al 2001;Cramer et al 2004;Darrouzet et al 2004)). While the mitochondrial and bacterial enzymes are referred to as cyt bc 1 , the homologous enzyme in plant and algal chloroplasts and cyanobacteria is called plastohydroquinone : plastocyanin oxidoreductase or cyt b 6 f (for a review see Cramer et al 1996;Cramer et al 2004).…”

Section: Introductionmentioning

confidence: 99%

X-Ray Structure of Rhodobacter Capsulatus Cytochrome bc₁: Comparison with its Mitochondrial and Chloroplast Counterparts

Berry

Huang

Saechao

et al. 2004

Photosynthesis Research

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197

217

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“…This makes up the Q cycle and leads to pumping of protons across the membrane. Crystallographic studies by Zhang et al [28] suggest that a significant conformational change in the protein is associated with this direction of the electrons from the reduced coenzyme Q [27]. In one conformation the Fe 2 S 2 cluster is close enough to the coenzyme Q binding site to pick up an electron.…”

Section: The Coqh 2 -Cyt C Reductase Complexmentioning

confidence: 99%

“…The CoQH 2 -cyt c reductase complex, also referred to as the cytochrome bc 1 complex or complex III, is a homodimeric transmembrane protein complex that takes electrons from the reduced coenzyme Q, produced by the NADH-CoQ reductase and succinate-CoQ reductase complexes, and passes the electrons to cytochrome c, a water soluble 13 kDa electron transfer protein through the so-called Q cycle [26,27]. In doing so it pumps two protons across the membrane and releases another two from the reduced quinone The reduced coenzyme Q, CoQH 2 , is oxidised in two steps with one electron being transferred to a high potential redox chain to give the semiquinone, CoQ , which then gives up a second electron to a separate low-potential redox chain in what appears to be a concerted electron transfer, since no intermediate semiquinone can be detected.…”

Section: The Coqh 2 -Cyt C Reductase Complexmentioning

confidence: 99%

Bioenergetics and Biological Electron Transport

Bartlett

2008

Bioelectrochemistry

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Large scale domain movement in cytochrome bc1: a new device for electron transfer in proteins

Cited by 133 publications

References 44 publications

Movement of the Iron−Sulfur Head Domain of Cytochrome bc₁ Transiently Opens the Catalytic Q_o Site for Reaction with Oxygen

Movement of the Iron−Sulfur Head Domain of Cytochrome bc₁ Transiently Opens the Catalytic Q_o Site for Reaction with Oxygen

X-Ray Structure of Rhodobacter Capsulatus Cytochrome bc₁: Comparison with its Mitochondrial and Chloroplast Counterparts

Bioenergetics and Biological Electron Transport

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Large scale domain movement in cytochrome bc1: a new device for electron transfer in proteins

Cited by 133 publications

References 44 publications

Movement of the Iron−Sulfur Head Domain of Cytochrome bc1 Transiently Opens the Catalytic Qo Site for Reaction with Oxygen

Movement of the Iron−Sulfur Head Domain of Cytochrome bc1 Transiently Opens the Catalytic Qo Site for Reaction with Oxygen

X-Ray Structure of Rhodobacter Capsulatus Cytochrome bc1: Comparison with its Mitochondrial and Chloroplast Counterparts

Bioenergetics and Biological Electron Transport

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Product

Resources

About

Movement of the Iron−Sulfur Head Domain of Cytochrome bc₁ Transiently Opens the Catalytic Q_o Site for Reaction with Oxygen

Movement of the Iron−Sulfur Head Domain of Cytochrome bc₁ Transiently Opens the Catalytic Q_o Site for Reaction with Oxygen

X-Ray Structure of Rhodobacter Capsulatus Cytochrome bc₁: Comparison with its Mitochondrial and Chloroplast Counterparts