Redox proteins in supercomplexes and signalosomes

362 Pages·2016·19.505 MB·English

by  Díaz-Moreno, Irene, Louro, Ricardo O

REDOX PROTEINS
IN
SUPERCOMPLEXES
SIGNALOSOMES
AND

Series in Biophysics
series editor: Georg Pabst
REDOX PROTEINS
IN
SUPERCOMPLEXES
SIGNALOSOMES
AND

edited by
Ricardo O. Louro
Instituto de Tecnologia Química e Biológica António Xavier,
Universidade Nova de Lisboa, Portugal
Irene Díaz-Moreno
Instituto de Bioquímica Vegetal y Fotosíntesis, cicCartuja,
Universidad de Sevilla - CSIC
Boca Raton London New York
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Contents
Preface, vii
Editors, xi
Contributors, xiii
Chapter 1 ◾ M ulti-Electron Transfer in Biological Systems 1
Catarina M. paquete, Bruno M. FonseCa and riCardo o. Louro
Chapter 2 ◾ D iversity of Interactions in Redox Systems: From
Short- to Long-Lived Complexes 35
antonio díaz-quintana, isaBeL Cruz-GaLLardo, MiGueL a. de La rosa
and irene díaz-Moreno
Chapter 3 ◾ A TPases and Mitochondrial Supercomplexes 61
sara CoGLiati, reBeCa aCín-pérez and José a. enriquez
Chapter 4 ◾ roLe oF CardioLipin in MitoChondriaL superCoMpLex asseMBLy 81
euGenia MiLeykovskaya and WiLLiaM doWhan
Chapter 5 ◾ M itochondrial Supercomplexes and ROS Regulation:
Implications for Ageing 107
Maria L. Genova and GiorGio Lenaz

Chapter 6 ◾ M itochondrial Respiratory Supercomplexes in
Physiology and Diseases 149
anna M. GheLLi, vaLentina C. tropeano and MiCheLa ruGoLo
Chapter 7 ◾ R egulation of Photosynthetic Electron Transport via
Supercomplex Formation in the Thylakoid Membrane 167
kentaro iFuku and toshiharu shikanai
v
vi ◾ Contents
Chapter 8 ◾ M icrobial Redox Proteins and Protein Complexes
for Extracellular Respiration 187
LianG shi, MinG tien, JaMes k. FredriCkson, John M. zaChara and kevin M. rosso
Chapter 9 ◾ U nravelling New Metabolic Pathways: Supramolecular
Organisation of Aerobic Bacteria Respiratory Chains 217
ana M.p. MeLo, eMMa B. Gutiérrez-CirLos and MiGueL teixeira
Chapter 10 ◾ M embrane Organisation and Electron Transport Switches
in Cyanobacteria 239
Conrad W. MuLLineaux and tChern Lenn
Chapter 11 ◾ R egulation of Cellular Signalling by Thioredoxin 255
toshiya MaChida, hidenori iChiJo and isao naGuro
Chapter 12 ◾ C ytochrome c–Based Signalosome 275
katiuska GonzáLez-arzoLa, BLas Moreno-BeLtrán, Jonathan Martínez-FáBreGas,
MiGueL a. de La rosa and irene díaz-Moreno
Chapter 13 ◾ C ell Membrane Raft Redox Signalosomes: Platform
Responding to Danger Signals 299
pin-Lan Li, Justine M. aBais, Jun-xianG Bao and yanG zhanG
Chapter 14 ◾ C onclusions 321
irene díaz-Moreno and riCardo o. Louro
INDEX, 325
Preface
This book comes as a product of its time, a time when scientific paradigms about
biology are changing as a consequence of evolving methodologies and understanding
of the ensuing experimental results. Over the past 10 years, the structural and functional
organization of the inner mitochondrial membrane and oxidative phosphorylation have
been the focus of intense debate. Within this domain, it is becoming widely accepted that
respiratory complexes can be rearranged/reorganized into supercomplexes in response
to different stimuli, carbon sources or stress conditions, and serve as a crucial adaptive
mechanism regulated by mitochondria. Nowadays, the organization and dynamics of the
mitochondrial electron transport chain is the subject of passionate discussion, for which
two different models are being considered: the fluid model—also known as the random
collision model—proposes independent diffusional motions for all membrane proteins and
redox components; the solid model suggests specific interactions between individual respi-
ratory components to form stable assemblies. Thus, the fluid model states that each respira-
tory complex would act as an individual entity, whereas the solid model strongly supports
the oligomerization in supercomplexes upon the discovery of detergent-based strategies for
their isolation and solubilisation.
However, neither model accounts for all the experimental evidence, since the super-
complex assembly is inherently plastic and it evolves during cell lifespan and strongly var-
ies from cell to cell. The apparently opposed models—solid versus fluid—are reconciled
in the plasticity model, which assumes that the supercomplex organization is not fixed
but in equilibrium with randomly dispersed respiratory complexes in living cells under
physiological conditions. Indeed, the ensemble of supercomplexes tightly depends on the
changes of phospholipid composition of the membrane due to genetic or dietary reasons,
the mitochondrial membrane potential, the so-called supercomplex assembly factors, and
the phosphorylation state of the protein subunits of the complexes.
Evidence of respiratory supercomplexes in all life domains has been published in the
past 10 years, demonstrating that the supramolecular organization of respiratory chains
is an ancient metabolic strategy widespread in nature. Indeed, respiratory supercomplexes
have been described in different eukaryotic organisms, such as algae, fungi, plants, and
mammals, and also in bacteria, possibly to overcome the poor compartmentalization of
bacterial enzymes. In plants and green algae, there is also evidence of scaffolds between the
photosystems and the light-harvesting complexes to form photosynthetic supercomplexes
inside chloroplasts. Moreover, the photosystem I and the cytochrome b f are associated in
6
vii
viii ◾ Preface
a supercomplex that is functional in cyclic electron transport. To date, however, we are not
aware of electron transport supercomplexes in cyanobacteria, despite the proximity of the
photosynthetic apparatus and the respiratory chain inside the thylakoid membrane.
Altogether, these findings suggest that the organization in supramolecular assemblies
provides functional advantages in the context of the mitochondrial respiratory function
and oxidative phosphorylation. Then, CoQ and cytochrome c channelling promotes direct
transfer of electrons between two adjacent enzymes—from complex I to complex III and
from complex III to complex IV, respectively—by successive reduction and re-oxidation
of the intermediate—CoQ or cytochrome c—without its diffusion in the bulk medium.
Evidence for possible channelling comes from the mitochondrial respirasome IIII IV, the
1 2 1
largest supercomplex, which represents the minimal unit able to perform complete aero-
bic respiration from NADH to oxygen. It is also worth mentioning that the respirasome
assembly preserves the structural integrity and activity of complex I, when bound to com-
plex III. In addition, the supramolecular structure of mitochondrial respiratory complexes
act as a factor limiting reactive oxygen species (ROS) generation, mainly by complexes I
and III in the mitochondria, especially during ageing-dependent decay of mitochondrial
function. Therefore, the plastic and dynamic nature of supercomplexes lies at the basis of a
control mechanism of the ROS concentration in the cell. Under physiological conditions,
ROS are messengers acting through redox modifications in signalling proteins. Under
homeostasis, ROS levels are controlled by not only supercomplexes but also detoxifying cel-
lular signalosomes existing inside the mitochondria, such as thiorredoxin and cytochrome
c-signalling networks. In contrast, when mitochondria are malfunctioning, ROS levels are
increased, causing pathological effects such as lipid peroxidation, leading to membrane
raft formation, protein oxidation including cytochrome c, mitochondrial DNA damage,
and supercomplex dismantling. Thus, modulation of respiratory supercomplexes arises as
a new approach to regulate disease progression.
Yet, controversially, a number of recent studies report that mitochondrial respirasomes
may not be the preferential functional forms of the mitochondrial respiratory chain, since
the lack of respirasomes in some organisms does not lead to evident pathological pheno-
types. Although much remains to be discovered about the function of supercomplexes in
biological systems, it is clear, nonetheless, that the countless and ever-growing advances in
the field have helped the scientific community overcome the scepticism about the reality
of biological supercomplexes. In other words, respirasomes (supercomplexes) exist because
they respire (function).
Nevertheless, we consider that this novel and widely accepted scheme of the mitochon-
drial respiratory chain, dynamically organised in supercomplexes even under physiologi-
cal conditions, deserves to be discussed in a book, so as to explain the state of the art to
readers and stimulate the debate. The other aim is one of shedding light on the impact of
supercomplex assembly on mitochondrial morphology and its physiology and biogenesis
in an effort to understand the molecular mechanisms of pathological situations, including
ageing. Without any hint of doubt, answers to these and other questions will certainly
come by in the forthcoming years.
Preface ◾ ix
Keeping this in mind, this book aims to bring together the most exciting research from
leading practitioners in the field. It is impossible to cover all aspects of supercomplexes
and signalosomes into a single volume, but we sincerely hope that the selection of themes
herein presented will help the readers grasp the state of the art in this multidisciplinary
field and understand the exciting development and quick progress of current research in
biosciences. To further this aim, several of the figures appearing in black and white in the
printed book were collected in the CRC Press website for this book (http://www.crcpress.
com/product/isbn/9781482251104), from where they are freely downloadable.
We are most grateful not only to all authors who have generously accepted the invitation
to contribute to this book with their interesting and cutting-edge chapters, but also to the
editorial office of CRC Press for their excellent technical assistance and support.
Ricardo O. Louro
Universidade Nova de Lisboa
Irene Díaz-Moreno
Universidad de Sevilla