Membrane Hydration The Role of Water in the Structure and

Function of Biological Membranes

Visit the link below to download the full version of this book:

https://medipdf.com/product/membrane-hydration-the-role-of-water-in-the-structur
e-and-function-of-biological-membranes/

Click Download Now

Water, water, everywhere,
And all the boards did shrink;
Water, water, everywhere,
Nor any drop to drink.
The Rime of the Ancient Mariner
Samuel Taylor Coleridge (1797)
Preface

Biological membranes are unique material in terms of surface and mechanical

properties due to its contact with water, and nowadays important attempts to mimic
their properties in the search of biotechnological inputs in human health, food
industry, crop, and energy have been developed. Thus, hydration in membranes gets
new insights from the prospect of nanosystems.
Hydration is an emerging subject in the field of material sciences. In particular,
in biological systems water is organized in proteins and membranes. In this last
case, the amount of water average is no more than 20–25 molecules per lipid. If
it is considered that it may be distributed in discrete sites of different chemical
features, water environments are restricted to less than ten water molecules. With
this criterion, studies of water in biological systems in general, and in membranes
in particular, are within the scope of nanosciences.
This book is an effort to enlighten the importance of this subject in relation to
biology and biophysics. This project has been possible due to the enthusiasm of all
the authors of the chapters to which I want to particularly thank for their work.
I also like to recognize those who for different reasons could not contribute to
this edition and hope that they may enrich future ones.
Among the authors I am particularly grateful to Zoran Arsov, Stephanie Tristram-
Nagle, Helge Pfeiffer, and Gustavo Appignanessi for their help, advice, and
comments along the preparation of the manuscripts.
The ideas about membranes and water have been built along years, and therefore,
it is the product of what I have been able to collect from excellent teachers,
colleagues, and friends.
For this reason I want to specially express my gratitude and recognition to Dr.
Jorge Arvia and Dr. Hector Videla from INIFTA (Universidad Nacional de La
Plata) with whom I began my feeling for research in biophysical chemistry and
bioelectrochemistry during my PhD thesis, to Prof Raul Grigera who showed me
the importance of water, and to Prof Hans de Gier from Utrecht University who
introduced me in the world of lipids as a postdoc.

ix
x Preface

Also, I learned thermodynamics with Ernesto Timmermann and lipid monolayers

with Bruno Maggio. With all of them I had exciting and vigorous discussions.
A special place is reserved for Sid Simon and Tom McIntosh with whom I spend
my sabbatical enjoying science, tennis, and drinks.
Finally I want also to thank all the students who went through my laboratory in
the Universidad Nacional de La Plata, University of Buenos Aires, University of
Tucuman, and, in these last years, the University of Santiago del Estero, because
along their works, their doubts, their achievements, their challenges, and their
irreverences I, found new routes to pursue in this research.
I hope that this book will encourage them and the next ones in the fascinating
field of biophysics of biological membranes.

Santiago del Estero, Argentina E. Anibal Disalvo

Acknowledgments

The editor is grateful to

Prof. Gerardo Fidelio (Universidad Nacional de Cordoba),
Prof Laura Bakas (Universidad Nacional de La Plata),
Dr. Maria de los Angeles Frías (CITSE, Universidad Nacional de Santiago del
Estero-CONICET (RA)), and
Prof. Daniel Rodrigues (Universidad Nacional del Litoral)
for their contributions in the revision of the chapters.

E. Anibal Disalvo
(Editor)

xi
Contents

1 Membrane Hydration: A Hint to a New Model for Biomembranes . . 1

E. Anibal Disalvo
2 Use of X-Ray and Neutron Scattering Methods
with Volume Measurements to Determine Lipid Bilayer
Structure and Number of Water Molecules/Lipid . .. . . . . . . . . . . . . . . . . . . . 17
Stephanie Tristram-Nagle
3 Water and Lipid Bilayers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 45
Jonathan D. Nickels and John Katsaras
4 Hydration Forces Between Lipid Bilayers: A Theoretical
Overview and a Look on Methods Exploring Dehydration .. . . . . . . . . . . 69
Helge Pfeiffer
5 Monitoring Membrane Hydration
with 2-(Dimethylamino)-6-Acylnaphtalenes Fluorescent Probes.. . . . . 105
Luis A. Bagatolli
6 Long-Range Lipid-Water Interaction as Observed
by ATR-FTIR Spectroscopy .. . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 127
Zoran Arsov
7 Hydration and Nanoconfined Water: Insights
from Computer Simulations . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 161
Laureano M. Alarcón, J.A. Rodríguez Fris,
Marcela A. Morini, M. Belén Sierra, S.A. Accordino,
J.M. Montes de Oca, Viviana I. Pedroni,
and Gustavo A. Appignanesi
8 Aquaphotomics: Near Infrared Spectroscopy and Water
States in Biological Systems . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 189
Roumiana Tsenkova, Zoltan Kovacs, and Yosuke Kubota

xiii
xiv Contents

9 Hydration in Lipid Monolayers: Correlation of Water

Activity and Surface Pressure .. . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 213
E. Anibal Disalvo, Axel Hollmann, and M. Florencia Martini
10 Water at Biological Phase Boundaries: Its Role
in Interfacial Activation of Enzymes and Metabolic Pathways.. . . . . . . 233
Srinivasan Damodaran
11 Anhydrobiosis: An Unsolved Problem with Applications
in Human Welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 263
John H. Crowe

Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 281

Index . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . 283
Contributors

S.A. Accordino Departamento de Química and INQUISUR-UNS-CONICET, Uni-

versidad Nacional del Sur, Bahía Blanca, Argentina
Laureano M. Alarcón Departamento de Química and INQUISUR-UNS-
CONICET, Universidad Nacional del Sur, Bahía Blanca, Argentina
Gustavo A. Appignanesi Departamento de Química and INQUISUR-UNS-
CONICET, Universidad Nacional del Sur, Bahía Blanca, Argentina
Zoran Arsov Laboratory of Biophysics, Department of Solid State Physics,“Jozef
Stefan” Institute, Ljubljana, Slovenia
Luis A. Bagatolli Membrane Biophysics and Biophotonics Group/MEMPHYS-
Center for Biomembrane Physics, Department of Biochemistry and Molecular
Biology, University of Southern Denmark, Odense M, Denmark
John H. Crowe Department of Molecular and Cellular Biology, University of
California, Davis, CA, USA
Srinivasan Damodaran Department of Food Science, University of Wisconsin-
Madison, Madison, WI, USA
E. Anibal Disalvo Laboratorio de Biointerfases y Sistemas Biomimeticos, Centro
de Investigacion y Transferencia de Santiago del Estero, Universidad Nacional de
Santiago del Estero-Consejo Nacional de Investigaciones Científicas y Técnicas,
Santiago del Estero, Argentina
Axel Hollmann Laboratorio de Biointerfases y Sistemas Biomimeticos, Centro
de Investigacion y Transferencia de Santiago del Estero, Universidad Nacional de
Santiago del Estero-Consejo Nacional de Investigaciones Científicas y Técnicas,
Santiago del Estero, Argentina
John Katsaras Biology & Soft Matter and Biosciences Division, Oak Ridge
National Laboratory, Oak Ridge, TN, USA

xv
xvi Contributors

Zoltan Kovacs Biomeasurement Technology Laboratory, Kobe University, Kobe,

Japan
Department of Physics and Control, Corvinus University of Budapest, Budapest,
Hungary
Yosuke Kubota Biomeasurement Technology Laboratory, Kobe University, Kobe,
Japan
M. Florencia Martini Instituto de Química y Metabolismo del Fármaco,
IQUIMEFA UBA-CONICET, Facultad de Farmacia y Bioquímica, Universidad de
Buenos Aires, Buenos Aires, Argentina
J.M. Montes de Oca Departamento de Química and INQUISUR-UNS-CONICET,
Universidad Nacional del Sur, Bahía Blanca, Argentina
Marcela A. Morini Departamento de Química and INQUISUR-UNS-CONICET,
Universidad Nacional del Sur, Bahía Blanca, Argentina
Jonathan D. Nickels Joint Institute for Neutron Sciences, Oak Ridge National
Laboratory, Oak Ridge, TN, USA
Department of Physics, University of Tennessee, Knoxville, Knoxville, TN, USA
Viviana I. Pedroni Departamento de Química and INQUISUR-UNS-CONICET,
Universidad Nacional del Sur, Bahía Blanca, Argentina
Helge Pfeiffer Department of Metallurgy and Materials Engineering (MTM),
University of Leuven (KU Leuven), Leuven, Belgium
J.A. Rodríguez Fris Departamento de Química and INQUISUR-UNS-CONICET,
Universidad Nacional del Sur, Bahía Blanca, Argentina
M. Belén Sierra Departamento de Química and INQUISUR-UNS-CONICET,
Universidad Nacional del Sur, Bahía Blanca, Argentina
Stephanie Tristram-Nagle Biological Physics Group, Physics Department,
Carnegie Mellon University, Pittsburgh, PA, USA
Roumiana Tsenkova Biomeasurement Technology Laboratory, Kobe University,
Kobe, Japan
Abbreviations

jF(qz )j Form factor

18:0:22:5PC Stearoyldocosapentaenoyl-phosphatidylcholine
18:0-22:6PC Stearoyldocosahexaenoylphosphatidylcholine
2DC Hydrocarbon thickness
AFM Atomic force microscopy
AL Area/lipid
B Bulk modulus
D, D-space X-ray lamellar D-spacing
d, d-space X-ray wide-angle chain spacing
DB Bilayer thickness
DH 0 Headgroup thickness
DHPC Dihexadecanoyl-phosphatidylcholine
diC22:1PC Dierucoylphosphatidylcholine
diphytanoylPC Diphytanoyl-phosphatidylcholine
DLPC Dilauroylphosphatidylcholine
DLPE Dilauroylphosphatidylethanolamine
DLPG Dilauroylphosphatidylglycerol
DMPC Dimyristoylphosphatidylcholine
DMPE Dimyristoylphosphatidylethanolamine
DMPG Dimyristoylphosphatidylglycerol
DMPS Dimyristoylphosphatidylserine
DOPC Dioleoylphosphatidylcholine
DOPG Dioleoylphosphatidylglycerol
DOPS Dioleoylphosphatidylserine
DPhPC Diphytanoylphosphatidylcholine
DPPC Dipalmitoylphosphatidylcholine
DSC Differential scanning calorimetry
DSPC Distearoylphosphatidylcholine
EggPC Egg phosphatidylcholine
EPR Electron spin resonance
FTIR Fourier transform infrared resonance

xvii
xviii Abbreviations

I(qz ) X-ray intensity

interdig. Interdigitated
KC Bending modulus
MD simulation Molecular dynamics simulation
MLVs Multilamellar vesicles
NIR Near-infrared
NMR Nuclear magnetic resonance
nW Number of waters/lipid
nW 0 Steric number of waters/lipid
OSM Osmotic stress method
PCA Principal component analysis
PLS Partial least squares
POPC Palmitoyloleoylphosphatidylcholine
POPG Palmitoyloleoylphosphatidylglycerol
PPM Piezotropic phase transitions method
PrP Prion protein
SFA Surface force apparatus
SIMCA Soft independent modeling of class analogy
SOPC Stearoyloleoyl-phosphatidylcholine
SOPG Stearoyloleoylphosphatidylglycerol
Tm Main transition melting temperature
TMCL Tetramyristoylcardiolipin
TPM Thermotropic phase transition method
ULVs Unilamellar vesicles
un Vertical displacement
VL Molecular volume/lipid
VW Molecular volume/water
WAMACS Water matrix coordinates
WASP Water spectral pattern
˜ Fluctuation parameter
Chapter 1
Membrane Hydration: A Hint to a New Model
for Biomembranes

E. Anibal Disalvo

Abstract The classical view of a biological membrane is based on the Singer-

Nicholson mosaic fluid model in which the lipid bilayer is the structural backbone.
Under this paradigm, many studies of biological processes such as, permeability,
active transport, enzyme activity and adhesion and fusion processes have been
rationalized considering the lipid membrane as a low dielectric slab of hydrocarbon
chains with polar head groups exposed to water at each side in which oil/water
partition prevails. In spite of several analyses and evidence available in relation to
membrane hydration, water is not taken into account as a functional component.
For this purpose, new insights in the water organization in restricted environments
and the thermodynamical and mechanical properties emerging from them are
specifically analysed and correlated.
This chapter summarizes the progress of the studies of water in membranes along
the book in order to give a more realistic structural and dynamical picture accounting
for the membrane functional properties.

Keywords Water penetration • Interphases • Hydration water • Confined water •

Complex systems • Membrane models

1.1 Introduction

Cell membranes are the physical limit between the living and the non-living
world. If the interior of the cell is considered the actual place of reproduction,
compartmentalization gives the appropriate environment to biological metabolic
reactions and the highly selective kinetic barrier properties of the membrane regulate
the exchange of matter and energy with the surroundings (Yeagle 2004).
Biomembranes are self organized assemblies of lipids and proteins, The classical
view of a biological membrane is based on the Singer-Nicholson mosaic fluid model

E.A. Disalvo ()

Laboratorio de Biointerfases y Sistemas Biomimeticos, Centro de Investigacion y Transferencia
de Santiago del Estero, Universidad Nacional de Santiago del Estero-Consejo Nacional de
Investigaciones Científicas y Técnicas, 4200 Santiago del Estero, Argentina
e-mail: [email protected]

© Springer International Publishing Switzerland 2015 1

E.A. Disalvo (ed.), Membrane Hydration, Subcellular Biochemistry 71,
DOI 10.1007/978-3-319-19060-0_1
2 E.A. Disalvo

in which the lipid bilayer is the structural backbone (Singer and Nicolson 1972). In
this context, the lipid membrane was usually described by a low dielectric slab of
hydrocarbon chains with polar head groups exposed to water at each side in which
oil/water partition prevailed (Overton 1889; Al-Awqati 1999).
Many studies of biological processes such as, permeability, active transport of
ions, enzyme activity and adhesion and fusion have been rationalized under this
paradigmatic model of sticks and balls in which different proteinaceous particles
were inserted to explain biological activity that the single non polar slab could not
explain.
In the last years, several critical reviews have introduced changes in the proposal
of Singer and Nicholson by including lipid mixtures, lipid heterogeneities, rafts,
local curvatures and protein-lipid interactions (Israelachvili 1977; Ti Tien and
Ottova 2001; Bagatolli et al. 2010; Goñi 2014). However, in spite of several
analyses and evidence available in relation to membrane hydration (Jendrasiak
and Hasty 1974; Jendradiak et al. 1996; Israelachvili and Wennerström 1996)
the principal feature of the classical view still remained: water is not taken into
account as a functional component. To put emphasis in the importance of the
structural/thermodynamic properties of water relevant to membrane response, a
thorough revision is imperative.
As said elsewhere, water has been for biologists as the canvas for the painters. All
is stabilized by water but consideration of water incorporated in the final structure
and the dynamical (thermodynamic and mechanical) properties it imposes to the
ensemble is far from being a routine.
As pointed out by Damodaran in Chap. 10, “although it is well recognized
that structural evolution of proteins and formation of lipid vesicles and cell
membranes are simple manifestations of the hydrophobic effect, i.e., a consequence
of energetics of interaction of water with the apolar moieties of these molecules, the
possibility of water playing a vital role in the very functioning of these biological
systems is often overlooked”.
Moreover, a non-negligible number of works deals with biological mechanisms
as they would occur in an anhydrous state or ignoring water in structure and kinetics
processes.
This book is an attempt to organize in a rationale way the progress of the studies
of water in membranes that give place to different biological phenomena.
For this purpose, new insights in the water organization in restricted environ-
ments and the thermodynamical and mechanical properties emerging from them are
specifically analysed and correlated, in order to give a more realistic structural and
dynamical picture accounting for the biological functional properties.
The main points that deserve special attention are:
– water penetration and distribution along the lipid molecules
– water mediation in the interaction between lipid membranes (adhesion, fusion) or
a lipid membrane and a protein (lipid-protein interaction) through water structure
(hydration force, hydration layers)
– surface pressure and its implications in surface water activity.
– water mediation in enzyme activity