Metalloprotein Association, Self-Association, and Dynamics Governed by Hydrophobic Interactions:  Simultaneous Occurrence of Gated and True Electron-Transfer Reactions between Cytochrome f and Cytochrome c6 from Chlamydomonas reinhardtii

Grove, Tijana Ž.; Kostić, Nenad M.

doi:10.1021/ja036009t

Cited by 18 publications

(15 citation statements)

References 98 publications

(286 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This prediction has been verified for a variety of redox proteins immobilized on different types of SAM-coated electrodes, including Cu A centers, azurin, iso-cytochrome c and cytochromes c, c 6 , and b 562 , among others. [21][22][23][24][25][26] The average tunneling decay parameter b obtained for the different proteins is about 1.1 per methylene group of the thiols.…”

Section: Introductionmentioning

confidence: 72%

Thermal Fluctuations Determine the Electron‐Transfer Rates of Cytochrome c in Electrostatic and Covalent Complexes

Martí

Martín

et al. 2010

ChemPhysChem

View full text Add to dashboard Cite

The heterogeneous electron-transfer (ET) reaction of cytochrome c (Cyt-c) electrostatically or covalently immobilized on electrodes coated with self-assembled monolayers (SAMs) of omega-functionalized alkanethiols is analyzed by surface-enhanced resonance Raman (SERR) spectroscopy and molecular dynamics (MD) simulations. Electrostatically bound Cyt-c on pure carboxyl-terminated and mixed carboxyl/hydroxyl-terminated SAMs reveals the same distance dependence of the rate constants, that is, electron tunneling at long distances and a regime controlled by the protein orientational distribution and dynamics that leads to a nearly distance-independent rate constant at short distances. Qualitatively, the same behavior is found for covalently bound Cyt-c, although the apparent ET rates in the plateau region are lower since protein mobility is restricted due to formation of amide bonds between the protein and the SAM. The experimental findings are consistent with the results of MD simulations indicating that thermal fluctuations of the protein and interfacial solvent molecules can effectively modulate the electron tunneling probability.

show abstract

Section: Introductionmentioning

confidence: 72%

Thermal Fluctuations Determine the Electron‐Transfer Rates of Cytochrome c in Electrostatic and Covalent Complexes

Martí

Martín

et al. 2010

ChemPhysChem

View full text Add to dashboard Cite

show abstract

“…First, we study the coupling of dynamic processes to interprotein ET through the use of high-viscosity cryosolvent solutions. This approach has long been used, through such studies as our own work with mixed-metal Hb hybrids (40) (45), which presented the first comparisons of the viscosity dependence of k f and k b , numerous studies of the photosynthetic reaction center reacting with Cc (46), and a recent study of a tethered ET pair (47).…”

Section: Discussionmentioning

confidence: 99%

“…This article presents exploratory efforts that are being extended, and the ideas presented here could well provide the impetus to rethink earlier viscosity studies (18,40,(43)(44)(45)(46)(47). More broadly, consecutive ET reactions can be considered as prototypes for multistage enzyme-catalyzed chemical reaction, and studying the effects of dynamics and binding energetics on the rich behavior of these ET reactions can further the understanding of the redox processes in these complex biological systems.…”

Section: Discussionmentioning

confidence: 99%

Differential influence of dynamic processes on forward and reverse electron transfer across a protein-protein interface

Hoffman

Celis²,

Cull³

et al. 2005

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

View full text Add to dashboard Cite

We propose that the forward and reverse halves of a flash-induced protein-protein electron transfer (ET) photocycle should exhibit differential responses to dynamic interconversion of configurations when the most stable configuration is not the most reactive, because the reactants exist in different initial configurations: the flash-photoinitiated forward ET process begins with the protein partners in an equilibrium ensemble of configurations, many of which have little or no reactivity, whereas the reactant of the thermal back ET (the charge-separated intermediate) is formed in a nonequilibrium, ''activated'' protein configuration. We report evidence for this proposal in measurements on (i) mixed-metal hemoglobin hybrids, (ii) the complex between cytochrome c peroxidase and cytochrome c, and (iii and iv) the complexes of myoglobin and isolated hemoglobin ␣-chains with cytochrome b 5. For all three systems, forward and reverse ET does respond differently to modulation of dynamic processes; further, the response to changes in viscosity is different for each system. cytochrome c ͉ dynamics ͉ hemoglobin ͉ myoglobin ͉ cytochrome c peroxidase T he long-range transfer of a single electron from donor to acceptor in a condensed phase is a fascinating and widely studied process (1, 2). Much of this work seeks to understand the electron transfer (ET) process itself. However, when the ET event involves a dynamic protein-protein interface, the observed kinetics frequently are controlled not by the ET process itself, but by the dynamics of recognition and binding and͞or conversion within an ensemble of bound configurations (3, 4).Studies of interprotein ET (3, 5-10) began with the implicit assumption of a protein-protein binding-energy landscape with a single reactive complex (Fig. 1A Left), implying a direct correlation between binding and reactivity. When the landscape for complex formation has several discrete minima ( Fig. 1 A Center) the reactive conformation may differ from the most stable one, in which case the observed ET kinetics are controlled by the rates and͞or energetics of conformational conversion within a complex (11-13). Recent studies of ET between myoglobin (Mb) and cytochrome b 5 (Fe 3ϩ b 5 ), which bind to each other by weak electrostatic interactions, disclosed a new dynamic docking paradigm in protein-protein reaction dynamics: the landscape involves numerous configurations of similar affinity, only a subset of which is active in ET (Fig. 1 A Right) (4, 14).A majority of these studies have used a photocycle in which laser-flash excitation of the metallo-porphyrin in a metalsubstituted (M ϭ Zn or Mg) hemoprotein to its triplet excited state ( 3 D) triggers ET from the triplet to the metal center of an acceptor protein (A) across a protein-protein interface, with rate constant, k f , Eq. 1:[1]The acceptor metal center of A typically is a ferri-heme center, Given the exponentially steep fall-off in the matrix element for ET between the two redox centers (19,20), there will be only a subset of conformation...

show abstract

“…Reaction rates depend on factors that control both electron tunneling and conformational dynamics coupled to protein association processes (1)(2)(3). As such, interprotein ET is sensitive to structure and dynamics at the interface (1,(4)(5)(6)(7)(8)(9)(10)(11). Residue substitution (achieved either by use of protein homologs, site-directed mutants, or computations) has been a popular and powerful approach for probing how interface composition influences interprotein ET (7,(10)(11)(12)(13)(14).…”

mentioning

confidence: 99%

Effects of interface mutations on association modes and electron-transfer rates between proteins

Kang

Crane

2005

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

109

View full text Add to dashboard Cite

Although bonding networks determine electron-transfer (ET) rates within proteins, the mechanism by which structure and dynamics influence ET across protein interfaces is not well understood. Measurements of photochemically induced ET and subsequent charge recombination between Zn-porphyrin-substituted cytochrome c peroxidase and cytochrome c in single crystals correlate reactivity with defined structures for different association modes of the redox partners. Structures and ET rates in crystals are consistent with tryptophan oxidation mediating charge recombination reactions. Conservative mutations at the interface can drastically affect how the proteins orient and dispose redox centers. Whereas some configurations are ET inactive, the wild-type complex exhibits the fastest recombination rate. Other association modes generate ET rates that do not correlate with predictions based on cofactor separations or simple bonding pathways. Inhibition of photoinduced ET at <273 K indicates gating by smallamplitude dynamics, even within the crystal. Thus, different associations achieve states of similar reactivity, and within those states conformational fluctuations enable interprotein ET.cytochrome ͉ protein dynamics ͉ protein-protein interaction ͉ electron tunneling M any long-range electron-transfer (ET) reactions in biology occur across transient protein-protein interfaces. Reaction rates depend on factors that control both electron tunneling and conformational dynamics coupled to protein association processes (1-3). As such, interprotein ET is sensitive to structure and dynamics at the interface (1, 4-11). Residue substitution (achieved either by use of protein homologs, site-directed mutants, or computations) has been a popular and powerful approach for probing how interface composition influences interprotein ET (7,(10)(11)(12)(13)(14). Nevertheless, effects of residue variation on interface structure are not often known.The natural redox partners yeast cytochrome c peroxidase (CcP) and yeast cytochrome c (yCc), whose structure as a complex was first determined in 1992 (15) and later as a covalent complex (16), have served as a paradigm for studying interprotein ET reactions (8,17). Hoffman and colleagues (8) have exploited ZnCcP substitution to photoactivate ET reactions and examine the effects of many structural and chemical perturbations on interprotein ET. In this system, the ZnCcP triplet state ( 3 ZnCcP) reduces Fe(III)Cc, and then back ET recombines the charge separation (Fig. 1). Recently, it has been demonstrated that a Trp-191 3 Phe CcP variant has much slower ET back-rates (k eb ) than wild-type (WT) CcP in the 1:1 complex with yCc (18). Thus, electron hopping through Trp-191 may accelerate the recombination reaction (Fig. 1), in analogy to the natural reaction between CcP compound I and Fe(II)Cc (19). Nevertheless, much slower ET back-rates in the complex between CcP and hCc compared with yCc, both in solution (20) and in crystals (21), indicate that ET across the protein-protein interface limits the overa...

show abstract

Metalloprotein Association, Self-Association, and Dynamics Governed by Hydrophobic Interactions: Simultaneous Occurrence of Gated and True Electron-Transfer Reactions between Cytochrome f and Cytochrome c₆ from Chlamydomonas reinhardtii

Cited by 18 publications

References 98 publications

Thermal Fluctuations Determine the Electron‐Transfer Rates of Cytochrome c in Electrostatic and Covalent Complexes

Thermal Fluctuations Determine the Electron‐Transfer Rates of Cytochrome c in Electrostatic and Covalent Complexes

Differential influence of dynamic processes on forward and reverse electron transfer across a protein-protein interface

Effects of interface mutations on association modes and electron-transfer rates between proteins

Contact Info

Product

Resources

About