Online citations, reference lists, and bibliographies.
Please confirm you are human
(Sign Up for free to never see this)
← Back to Search

Physical Contact Between Cytochrome C1 And Cytochrome C Increases The Driving Force For Electron Transfer.

Gonzalo Pérez-Mejías, José Luis Olloqui-Sariego, Alejandra Guerra-Castellano, A. Díaz-Quintana, J. J. Calvente, R. Andreu, Miguel Á De la Rosa, I. Díaz-Moreno
Published 2020 · Chemistry, Medicine

Save to my Library
Download PDF
Analyze on Scholarcy
Share
In oxidative phosphorylation, the transfer of electrons from reduced cofactors to molecular oxygen via the electron transport chain (ETC) sustains the electrochemical transmembrane potential needed for ATP synthesis. A key component of the ETC is complex III (CIII, cytochrome bc1), which transfers electrons from reduced ubiquinone to soluble cytochrome c (Cc) coupled to proton translocation into the mitochondrial intermembrane space. One electron from every two donated by hydroquinone at site P is transferred to Cc via the Rieske-cytochrome c1 (Cc1) pathway. According to recent structural analyses of CIII and its transitory complex with Cc, the interaction between the Rieske subunit and Cc1 switches intermittently during CIII activity. However, the electrochemical properties of Cc1 and their function as a wire between Rieske and Cc are rather unexplored. Here, temperature variable cyclic voltammetry provides novel data on the thermodynamics and kinetics of interfacial electron transfer of immobilized Cc1. Findings reveal that Cc1 displays two channels for electron exchange, with a remarkably fast heterogeneous electron transfer rate. Furthermore, the electrochemical properties are strongly modulated by the binding mode of the protein. Additionally, we show that electron transfer from Cc1 to Cc is thermodynamically favored in the immobilized Cc1-Cc complex. Nuclear Magnetic Resonance, HADDOCK, and Surface Plasmon Resonance experiments provide further structural and functional data of the Cc1-Cc complex. Our data supports the Rieske-Cc1-Cc pathway acting as a unilateral switch thyristor in which redox potential modulation through protein-protein contacts are complemented with the relay-like Rieske behavior.
This paper references
10.1021/acs.chemrev.7b00257
Multifunctional Cytochrome c: Learning New Tricks from an Old Dog.
Damián Alvarez-Paggi (2017)
10.1016/j.biocel.2020.105704
Cytochrome c phosphorylation: Control of mitochondrial electron transport chain flux and apoptosis.
Hasini A Kalpage (2020)
10.1002/ANIE.200502386
High-pressure probing of a changeover in the charge-transfer mechanism for intact cytochrome c at gold/self-assembled monolayer junctions.
D. Khoshtariya (2005)
10.1016/j.cellsig.2012.01.008
Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling.
P. D. Ray (2012)
10.1016/S0005-2728(02)00360-2
Spectroscopic and oxidation-reduction properties of Rhodobacter capsulatus cytochrome c1 and its M183K and M183H variants.
J. Li (2002)
10.1016/s0021-9258(19)69355-5
Electrostatic interaction of cytochrome c with cytochrome c1 and cytochrome oxidase.
H. Smith (1981)
10.1016/j.bbabio.2016.01.011
Structural and functional characterization of phosphomimetic mutants of cytochrome c at threonine 28 and serine 47.
Alejandra Guerra-Castellano (2016)
10.1016/0022-2836(91)90027-4
Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors.
S. Hubbard (1991)
10.1016/0005-2795(75)90006-9
A trypsin-resistant heme peptide from cardiac cytochrome c1.
L. Yu (1975)
10.1016/0014-5793(80)80835-0
Mapping of the interaction domain for purified cytochrome c 1 on cytochrome c
B. Koenig (1980)
10.1016/s0021-9258(18)98678-3
Preparation and characterization of the water-soluble heme-binding domain of cytochrome c1 from the Rhodobacter sphaeroides bc1 complex.
K. Konishi (1991)
10.1073/PNAS.97.9.4567
Uncovering the [2Fe2S] domain movement in cytochrome bc1 and its implications for energy conversion.
E. Darrouzet (2000)
10.1021/BI061345I
Resilience of Rhodobacter sphaeroides cytochrome bc1 to heme c1 ligation changes.
H. Zhang (2006)
10.1074/jbc.M710126200
Structure of Complex III with Bound Cytochrome c in Reduced State and Definition of a Minimal Core Interface for Electron Transfer*
Sozanne R. Solmaz (2008)
10.1038/33612
Electron transfer by domain movement in cytochrome bc1
Z. Zhang (1998)
10.1021/JZ200734A
The Reorganization Energy in Cytochrome c is Controlled by the Accessibility of the Heme to the Solvent
C. A. Bortolotti (2011)
10.1159/000366402
CYC1 Silencing Sensitizes Osteosarcoma Cells to TRAIL-Induced Apoptosis
G. Li (2014)
10.1016/j.cell.2017.07.050
Architecture of Human Mitochondrial Respiratory Megacomplex I2III2IV2
Runyu Guo (2017)
10.1074/JBC.M412422200
NMR Analysis of the Transient Complex between Membrane Photosystem I and Soluble Cytochrome c6*
I. Díaz-Moreno (2005)
10.1021/BI00355A035
Control of the redox potential of cytochrome c and microscopic dielectric effects in proteins.
A. Churg (1986)
10.1007/s007750100208
Crystal structure of low-potential cytochrome c549 from Synechocystis sp. PCC 6803 at 1.21 Å resolution
C. Frazão (2001)
10.1016/j.ajhg.2013.06.015
Mutations in CYC1, encoding cytochrome c1 subunit of respiratory chain complex III, cause insulin-responsive hyperglycemia.
P. Gaignard (2013)
10.1016/J.ELECTACTA.2015.07.065
Thermodynamics and kinetics of reduction and species conversion at a hydrophobic surface for mitochondrial cytochromes c and their cardiolipin adducts
A. Ranieri (2015)
10.1073/pnas.052704699
Crystal structure of the yeast cytochrome bc1 complex with its bound substrate cytochrome c
C. Lange (2002)
10.1021/bi800932c
Probing the Paracoccus denitrificans cytochrome c(1)-cytochrome c(552) interaction by mutagenesis and fast kinetics.
Julia Janzon (2008)
10.1016/j.bbabio.2011.04.005
Conformationally linked interaction in the cytochrome bc(1) complex between inhibitors of the Q(o) site and the Rieske iron-sulfur protein.
E. Berry (2011)
10.1038/cddis.2014.280
A common signalosome for programmed cell death in humans and plants
J. Martínez-Fábregas (2014)
10.1110/ps.041150205
The orientations of cytochrome c in the highly dynamic complex with cytochrome b5 visualized by NMR and docking using HADDOCK
A. N. Volkov (2005)
10.1002/chem.200802450
Multiple mechanisms for electron transfer at metal/self-assembled monolayer/room-temperature ionic liquid junctions: dynamical arrest versus frictional control and non-adiabaticity.
D. Khoshtariya (2009)
10.1038/nature12985
Mitochondrial form and function
J. Friedman (2014)
10.1016/S0968-0004(01)01897-7
Large scale domain movement in cytochrome bc(1): a new device for electron transfer in proteins.
E. Darrouzet (2001)
10.1021/jz500150y
Temperature-Driven Changeover in the Electron-Transfer Mechanism of a Thermophilic Plastocyanin.
José Luis Olloqui-Sariego (2014)
10.1021/jp202656w
Electrochemistry of cytochrome c1, cytochrome c552, and CuA from the respiratory chain of Thermus thermophilus immobilized on gold nanoparticles.
T. Meyer (2011)
10.1016/j.cell.2016.11.012
Structure of Mammalian Respiratory Supercomplex I1III2IV1
M. Wu (2016)
10.1021/jp302301m
Perturbation of the redox site structure of cytochrome c variants upon tyrosine nitration.
H. K. Ly (2012)
10.1074/jbc.M803236200
The Mechanism of Mitochondrial Superoxide Production by the Cytochrome bc1 Complex*
S. Dröse (2008)
10.1073/pnas.1108320108
NMR basis for interprotein electron transfer gating between cytochrome c and cytochrome c oxidase
K. Sakamoto (2011)
10.1006/BBRC.1998.9549
Overproduction of theBradyrhizobium japonicum c-Type Cytochrome Subunits of thecbb3Oxidase inEscherichia coli
E. Arslan (1998)
10.1074/jbc.M413298200
Structure of the Complex between Plastocyanin and Cytochrome f from the Cyanobacterium Nostoc sp. PCC 7119 as Determined by Paramagnetic NMR
I. Díaz-Moreno (2005)
Preparation and properties of cardiac cytochrome c 1 .
C. Yu (1972)
10.1074/JBC.274.19.13292
Site-directed mutagenesis of cytochrome c6 from Synechocystis sp. PCC 6803. The heme protein possesses a negatively charged area that may be isofunctional with the acidic patch of plastocyanin.
B. De la Cerda (1999)
10.1021/ja3030356
The reversible opening of water channels in cytochrome c modulates the heme iron reduction potential.
C. A. Bortolotti (2012)
10.1016/0014-5793(92)81200-6
A laser flash absorption spectroscopy study of Anabaena sp. PCC 7119 flavodoxin photoreduction by photosystem I particles from spinach
M. Medina (1992)
10.1002/1439-7633(20020603)3:6<526::AID-CBIC526>3.0.CO;2-N
The Ternary Complex of Cytochrome f and Cytochrome c: Identification of a Second Binding Site and Competition for Plastocyanin Binding
P. Crowley (2002)
10.1039/c9cc05611d
Electron bifurcation: progress and grand challenges.
J. Yuly (2019)
10.1016/S0010-8545(00)00292-7
Redox reactions of heme-containing metalloproteins: dynamic effects of self-assembled monolayers on thermodynamics and kinetics of cytochrome c electron-transfer reactions
M. Fedurco (2000)
10.1016/j.febslet.2005.04.031
An NMR‐based docking model for the physiological transient complex between cytochrome f and cytochrome c 6
I. Díaz-Moreno (2005)
10.1016/j.bbabio.2008.01.003
Electron transfer kinetics between soluble modules of Paracoccus denitrificans cytochrome c1 and its physiological redox partners.
Julia Janzon (2008)
10.1073/pnas.1618008114
Structural basis of mitochondrial dysfunction in response to cytochrome c phosphorylation at tyrosine 48
Blas Moreno-Beltrán (2017)
10.1016/j.molcel.2016.01.028
The Mitochondrial Basis of Aging.
N. Sun (2016)
10.1016/j.tcb.2020.01.006
Mitochondrial Functions in Infection and Immunity
Varnesh Tiku (2020)
10.1006/JMRE.2000.2206
Extending the excitation sculpting concept for selective excitation.
C. Roumestand (2000)
10.1016/j.bbabio.2009.12.004
Redox potential of the Rieske iron-sulfur protein quantum-chemical and electrostatic study.
A. M. Kuznetsov (2010)
10.1002/1099-0682(200112)2001:12<2989::AID-EJIC2989>3.0.CO;2-E
Medium and Temperature Effects on the Redox Chemistry of Cytochrome c
G. Battistuzzi (2001)
10.1016/j.bbrc.2015.12.079
Investigation of the redox-dependent modulation of structure and dynamics in human cytochrome c.
Mizue Imai (2016)
10.1016/0022-0728(88)80308-5
Unusual quasi-reversibility (UQR) or apparent non-kinetic hysteresis in cyclic voltammetry: An elaboration upon the implications of N-shaped free energy relationships as explanation
S. Feldberg (1988)
10.1016/S0162-0134(97)00100-1
The Soret circular dichroism spectrum as a probe for the heme Fe(III)-Met(80) axial bond in horse cytochrome c.
R. Santucci (1997)
10.1021/BI990211K
Substitution of the sixth axial ligand of Rhodobacter capsulatus cytochrome c1 heme yields novel cytochrome c1 variants with unusual properties.
E. Darrouzet (1999)
10.1016/j.bpj.2010.08.042
The binding interface of cytochrome c and cytochrome c₁ in the bc₁ complex: rationalizing the role of key residues.
O. Kokhan (2010)
10.1002/ANIE.200290021
Electron-transfer dynamics of cytochrome C: a change in the reaction mechanism with distance.
J. Wei (2002)
10.1021/JP013841G
Spectroscopic Characterization of Nonnative Conformational States of Cytochrome c
S. Oellerich (2002)
10.1021/bi1007673
DsrJ, an essential part of the DsrMKJOP transmembrane complex in the purple sulfur bacterium Allochromatium vinosum, is an unusual triheme cytochrome c.
F. Grein (2010)
10.1021/JP9052659
A Unified Model for the Electrochemical Rate Constant That Incorporates Solvent Dynamics
Ambuj Mishra (2009)
10.1073/pnas.1806833115
Oxidative stress is tightly regulated by cytochrome c phosphorylation and respirasome factors in mitochondria
Alejandra Guerra-Castellano (2018)
10.1093/bioinformatics/btu830
NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy
Woonghee Lee (2015)
10.1006/ABBI.1995.1202
Purification and physicochemical properties of the low-potential cytochrome C549 from the cyanobacterium Synechocystis sp. PCC 6803.
J. A. Navarro (1995)
10.1074/jbc.M802174200
Demonstration of Short-lived Complexes of Cytochrome c with Cytochrome bc1 by EPR Spectroscopy
M. Sarewicz (2008)
10.7554/eLife.21290
Functional asymmetry and electron flow in the bovine respirasome
J. S. Sousa (2016)
10.1074/mcp.M113.034322
Structural and Functional Analysis of Novel Human Cytochrome c Targets in Apoptosis*
Jonathan Martínez-Fábregas (2014)
10.1021/acs.jpcb.9b04816
eMap: A Web Application for Identifying and Visualizing Electron or Hole Hopping Pathways in Proteins.
Ruslan N Tazhigulov (2019)
10.1016/s0021-9258(18)31553-9
Ubiquinol-cytochrome c oxidoreductase of higher plants. Isolation and characterization of the bc1 complex from potato tuber mitochondria.
E. Berry (1991)
10.1042/BST0360981
A structural analysis of the transient interaction between the cytochrome bc1 complex and its substrate cytochrome c.
Ajeeta Nyola (2008)
10.1021/BI027213G
Design of a ruthenium-labeled cytochrome c derivative to study electron transfer with the cytochrome bc1 complex.
G. Engstrom (2003)
10.1021/JA026939X
HADDOCK: a protein-protein docking approach based on biochemical or biophysical information.
C. Dominguez (2003)
10.1016/j.jmb.2015.09.014
The HADDOCK2.2 Web Server: User-Friendly Integrative Modeling of Biomolecular Complexes.
G. V. van Zundert (2016)
10.3390/biology8020048
Mitochondrial Dysfunction in Aging and Diseases of Aging
R. Haas (2019)
10.1006/BBRC.1997.7953
Cloning and correct expression in Escherichia coli of the petE and petJ genes respectively encoding plastocyanin and cytochrome c6 from the cyanobacterium Anabaena sp. PCC 7119.
F. P. Molina-Heredia (1998)
10.1016/j.bbabio.2012.12.002
Superoxide generation by complex III: from mechanistic rationales to functional consequences.
Lea Bleier (2013)
10.1242/jcs.099234
Mitochondria and cell signalling
S. Tait (2012)
10.1073/PNAS.76.1.155
Definition of cytochrome c binding domains by chemical modification: kinetics of reaction with beef mitochondrial reductase and functional organization of the respiratory chain.
S. Speck (1979)
10.1111/J.1432-1033.1981.TB05319.X
Membrane-bound and water-soluble cytochrome c1 from Neurospora mitochondria.
Y. Li (1981)
10.1016/j.bbabio.2014.03.009
The dynamic complex of cytochrome c6 and cytochrome f studied with paramagnetic NMR spectroscopy.
I. Díaz-Moreno (2014)
10.1016/j.febslet.2015.01.004
Respiratory complexes III and IV can each bind two molecules of cytochrome c at low ionic strength
Blas Moreno-Beltrán (2015)
10.1126/SCIENCE.281.5373.64
Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex.
S. Iwata (1998)
10.1016/j.bbabio.2012.11.008
Structural analysis of cytochrome bc1 complexes: implications to the mechanism of function.
D. Xia (2013)
10.1016/j.bbabio.2018.04.010
Functional flexibility of electron flow between quinol oxidation Qo site of cytochrome bc1 and cytochrome c revealed by combinatory effects of mutations in cytochrome b, iron-sulfur protein and cytochrome c1.
A. Borek (2018)
10.1021/cr400479b
Metalloproteins Containing Cytochrome, Iron–Sulfur, or Copper Redox Centers
J. Liu (2014)
10.1016/j.bbabio.2014.07.017
Cytochrome c1 exhibits two binding sites for cytochrome c in plants.
Blas Moreno-Beltrán (2014)
10.1038/nature19774
The architecture of respiratory supercomplexes
J. A. Letts (2016)
10.1021/AC980557L
Fast-scan cyclic voltammetry of protein films on pyrolytic graphite edge electrodes: characteristics of electron exchange.
J. Hirst (1998)
10.1073/pnas.0601149103
Surface-modulated motion switch: Capture and release of iron–sulfur protein in the cytochrome bc1 complex
L. Esser (2006)
10.1016/j.bbabio.2011.09.012
Nitration of tyrosines 46 and 48 induces the specific degradation of cytochrome c upon change of the heme iron state to high-spin.
I. Díaz-Moreno (2011)
Comparison of the binding sites on cytochrome c for cytochrome c oxidase, cytochrome bc1, and cytochrome c1. Differential acetylation of lysyl residues in free and complexed cytochrome c.
R. Rieder (1980)
10.1016/S0005-2728(02)00249-9
Electron transfer between yeast cytochrome bc(1) complex and cytochrome c: a structural analysis.
C. Hunte (2002)
10.1021/BI0350957
Reduction potentials of Rieske clusters: importance of the coupling between oxidation state and histidine protonation state.
Y. Zu (2003)
10.1006/ABBI.1995.1390
Site-specific mutagenesis demonstrates that the structural requirements for efficient electron transfer in Anabaena ferredoxin and flavodoxin are highly dependent on the reaction partner: kinetic studies with photosystem I, ferredoxin:NADP+ reductase, and cytochrome c.
J. A. Navarro (1995)
10.1021/BI0025823
Interaction of yeast iso-1-cytochrome c with cytochrome c peroxidase investigated by [15N, 1H] heteronuclear NMR spectroscopy.
J. Worrall (2001)
10.1021/acs.biochem.5b01385
Alternative Conformations of Cytochrome c: Structure, Function, and Detection.
Luciana Hannibal (2016)
10.1021/BI00463A004
Large-scale purification and characterization of a highly active four-subunit cytochrome bc1 complex from Rhodobacter sphaeroides.
K. Andrews (1990)
10.1021/JA034719T
Charge-transfer mechanism for cytochrome c adsorbed on nanometer thick films. Distinguishing frictional control from conformational gating.
D. Khoshtariya (2003)
10.1002/jcc.20084
UCSF Chimera—A visualization system for exploratory research and analysis
E. F. Pettersen (2004)
10.1016/j.ajhg.2008.03.020
Mitochondrial complex III deficiency associated with a homozygous mutation in UQCRQ.
O. Barel (2008)
10.1021/BI00162A027
Mutagenesis of methionine-183 drastically affects the physicochemical properties of cytochrome c1 of the bc1 complex of Rhodobacter capsulatus.
K. A. Gray (1992)
10.1021/JE00015A050
Density and Viscosity of Concentrated Aqueous Solutions of Polyethylene Glycol
P. González-Tello (1994)
10.1111/febs.12207
Communication between L–galactono–1,4–lactone dehydrogenase and cytochrome c
M. Hervás (2013)
10.1152/physrev.00006.2014
Electronic connection between the quinone and cytochrome C redox pools and its role in regulation of mitochondrial electron transport and redox signaling.
M. Sarewicz (2015)
10.1021/BI801329S
Effect of nitration on the physicochemical and kinetic features of wild-type and monotyrosine mutants of human respiratory cytochrome c.
Vicente Rodríguez-Roldán (2008)
10.1021/BI047855Z
Different modes of interaction in cyanobacterial complexes of plastocyanin and cytochrome f.
I. Díaz-Moreno (2005)
10.1021/acs.biochem.5b00922
Active Site Structure and Peroxidase Activity of Oxidatively Modified Cytochrome c Species in Complexes with Cardiolipin.
D. Capdevila (2015)
10.1016/j.bioelechem.2009.06.003
Electrostatic strain and concerted motions in the transient complex between plastocyanin and cytochrome f from the cyanobacterium Phormidium laminosum.
I. Díaz-Moreno (2009)
10.1016/j.jhep.2016.04.017
Severe respiratory complex III defect prevents liver adaptation to prolonged fasting.
Laura S. Kremer (2016)
10.1016/S0003-9861(03)00166-8
Aging defect at the QO site of complex III augments oxyradical production in rat heart interfibrillar mitochondria.
S. Moghaddas (2003)
10.1021/JP0620670
On the electron transfer mechanism between cytochrome C and metal electrodes. Evidence for dynamic control at short distances.
Hongjun Yue (2006)
10.1021/BI973146S
Interactions between the cytochrome b, cytochrome c1, and Fe-S protein subunits at the ubihydroquinone oxidation site of the bc1 complex of Rhodobacter capsulatus.
A. S. Saribas (1998)
10.1016/J.ELECOM.2011.10.021
A bis-histidine-ligated unfolded cytochrome c immobilized on anionic SAM shows pseudo-peroxidase activity
A. Ranieri (2012)
10.1016/J.BBRC.2003.10.182
Stability and apoptotic activity of recombinant human cytochrome c.
A. Olteanu (2003)
10.1002/humu.22257
Mitochondrial Complex III Deficiency Caused by a Homozygous UQCRC2 Mutation Presenting with Neonatal‐Onset Recurrent Metabolic Decompensation
N. Miyake (2013)
10.1002/humu.22441
A Homozygous Mutation in LYRM7/MZM1L Associated with Early Onset Encephalopathy, Lactic Acidosis, and Severe Reduction of Mitochondrial Complex III Activity
F. Invernizzi (2013)
10.1016/J.BBABIO.2005.03.009
Ubiquinol oxidation in the cytochrome bc1 complex: reaction mechanism and prevention of short-circuiting.
A. Mulkidjanian (2005)
10.1016/j.bbabio.2013.04.006
Unanswered questions about the structure of cytochrome bc1 complexes.
E. Berry (2013)



This paper is referenced by
Semantic Scholar Logo Some data provided by SemanticScholar