Structural dynamics in an electron–transfer complex

Jeng, Mei-Fen; Englander, S. Walter; Pardue, Kelli; Rogalskyj, Jill Short; McLendon, George

doi:10.1038/nsb0494-234

Cited by 41 publications

(59 citation statements)

References 40 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The presence of multiple orientations within Cc-CcP complex previously has been suggested by several studies (9)(10)(11)(12)(13)(14)(15)17). A complex comprising an equilibrium between a well defined form and a dynamic state (Fig.…”

Section: Resultsmentioning

confidence: 83%

“…However, it has remained a matter of debate whether this structure represents the only form in solution (6)(7)(8). According to several studies, the complex is dynamic, and the crystal structure might represent only a subpopulation of protein orientations (9)(10)(11)(12)(13)(14)(15). Recent studies show that the photoinduced ET between Znsubstituted CcP and Cc, both in the crystal (8,16) and in solution (17), occurs with faster backward than forward rates, indicating that the complex is present in multiple forms, only a few of which are ET-active (17).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Solution structure and dynamics of the complex between cytochromecand cytochromecperoxidase determined by paramagnetic NMR

Volkov

Worrall

Holtzmann

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

244

361

View full text Add to dashboard Cite

The physiological complex of yeast cytochrome c peroxidase and iso-1-cytochrome c is a paradigm for biological electron transfer. Using paramagnetic NMR spectroscopy, we have determined the conformation of the protein complex in solution, which is shown to be very similar to that observed in the crystal structure [ electron transfer ͉ encounter state ͉ transient complex ͉ spin label ͉ paramagnetic relaxation enhancement T he process of protein complex formation can be described by a two-step model, in which a short-lived, dynamic encounter complex precedes a dominant, well defined state (Fig. 1). The former enables proteins to undergo reduced-dimensionality search of the optimal binding geometry, thereby accelerating molecular association as compared with 3D diffusion (1). Fast molecular association is essential for protein-protein complexes that require high turnover rates, like those involved in electron transfer (ET) in photosynthesis, respiration, and other metabolic processes (2). The physiological complex of yeast iso-1-cytochrome c (Cc) and yeast cytochrome c peroxidase (CcP) is a paradigm for the intermolecular ET (3) and is one of the few transient ET complexes for which a crystal structure has been solved (4). A recent study has confirmed that the protein-protein orientation observed in the crystal is ET-active (5). However, it has remained a matter of debate whether this structure represents the only form in solution (6-8). According to several studies, the complex is dynamic, and the crystal structure might represent only a subpopulation of protein orientations (9-15). Recent studies show that the photoinduced ET between Znsubstituted CcP and Cc, both in the crystal (8, 16) and in solution (17), occurs with faster backward than forward rates, indicating that the complex is present in multiple forms, only a few of which are .Characterization of the binding interface in the dynamic encounter state (Fig. 1B) has so far proven to be elusive. Investigation of protein complexes by using x-ray crystallography or conventional NMR spectroscopy addresses only the singleorientation species (Fig. 1C), and the only way to visualize the dynamic state is offered by theoretical modeling studies (11,18). In the recent, elegant work of Clore and coworkers (19,20), it was shown how paramagnetic relaxation can be applied to study the dynamic state of protein-DNA complexes. We report on the application of an analogous experimental approach that allows us to define both the dominant protein-protein orientation (Fig. 1C) and the conformational space sampled by the proteins in the dynamic encounter complex (Fig. 1B). Results and DiscussionSolution Structure of the Complex. The concept of the approach is that NMR resonance intensities of one of the proteins in the complex are affected by a paramagnetic spin label covalently attached to the other protein (Fig. 2). The paramagnetic effects are converted into distance restraints (21-23), which can be used to calculate protein-protein orientations within the complex (24). Five ...

show abstract

Section: Resultsmentioning

confidence: 83%

mentioning

confidence: 99%

Solution structure and dynamics of the complex between cytochromecand cytochromecperoxidase determined by paramagnetic NMR

Volkov

Worrall

Holtzmann

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

244

361

View full text Add to dashboard Cite

show abstract

“…This conclusion may hold in ViVo and suggests that electron transport in real biological systems may be faster in situations where the components of a transient complex are not connected together in a single, well defined manner. [347][348][349][350][351][352][353][354][355][356] Hildebrandt and co-workers have also emphasized the similarity between self-assembled monolayers and biological membranes. 357 In the case of bare metal electrodes, the protein-electrode interaction is not expected to mimic the physiological situation.…”

Section: Interfacial and Intermolecular Electron Transfermentioning

confidence: 99%

“…This may be reminiscent of a common situation for inter-protein electron transfer. Indeed, it is now admitted that distributions of orientations and electron transfer rates also exist in protein-protein electron transfers, as evidenced in NMR experiments, [347][348][349][350][351][352][353][354] soft-docking, 355 and molecular dynamics simulations, 356 but the heterogeneity of intermolecular ET rate constants is likely to escape detection in traditional kinetic measurements. In contrast, the distribution of interfacial ET rate constants is evident from the shape of the PFV data, and this illustrates an advantage of measuring the complete dependence of rate on driving force rather than a single value of the rate as in homogeneous kinetics.…”

Section: Interfacial and Intermolecular Electron Transfermentioning

confidence: 99%

Direct Electrochemistry of Redox Enzymes as a Tool for Mechanistic Studies

2008

View full text Add to dashboard Cite

show abstract

“…The CcP enzyme could be forming a complex [5], or it could even extract the electrons internally [31]. The studies on proton exchange rates in the interface region between CcP and cytochrome c show that the region is more accessible [32] than expected from the crystallographic structure [5], and that some structural rearrangement can occur in the complex [33]. The stable structure of the heme environment certainly renders the concept of multiple electron transfer pathways possible [10], and underlines again the distance in electron transfer as an important parameter [34].…”

Section: Resultsmentioning

confidence: 99%

The crystal structure of the iron‐free cytochrome c peroxidase and its implication for the enzymatic mechanism

Yonetani

Skoglund

1994

FEBS Letters

View full text Add to dashboard Cite

We report the refined structure of an iron-free form of cytochrome c peroxidase (CcP) at 2.3 A resolution. The backbone comparison between native CcP and iron-free CcP shows that the two structures have the same protein fold within experimental error. The only difference noted is in the heme pocket where the distance between the proximal histidine and the center of the protoporphyrin has increased. The results show that the iron-free CcP should be a good substitute for native CcP in fluorescence studies and thus also validate previous studies using iron-free CcPs as efficient fluorescent probes in electron transfer studies.

show abstract

Structural dynamics in an electron–transfer complex

Cited by 41 publications

References 40 publications

Solution structure and dynamics of the complex between cytochromecand cytochromecperoxidase determined by paramagnetic NMR

Solution structure and dynamics of the complex between cytochromecand cytochromecperoxidase determined by paramagnetic NMR

Direct Electrochemistry of Redox Enzymes as a Tool for Mechanistic Studies

The crystal structure of the iron‐free cytochrome c peroxidase and its implication for the enzymatic mechanism

Contact Info

Product

Resources

About