The biophysics of cell membranes : biological consequences

224 Pages·2017·5.211 MB·English

by  Epand, Richard M., Ruysschaert, Jean-Marie

Springer Series in Biophysics 19
Richard M. Epand
Jean-Marie Ruysschaert E ditors
The Biophysics
of Cell
Membranes
Biological Consequences
Springer Series in Biophysics
Volume 19
Serieseditor
BorisMartinac
Moreinformationaboutthisseriesathttp://www.springer.com/series/835
Richard M. Epand • Jean-Marie Ruysschaert
Editors
The Biophysics of Cell
Membranes
Biological Consequences
123
Editors
RichardM.Epand Jean-MarieRuysschaert
BiochemistryandBiomedicalSciences SciencesFaculty
McMasterUniversity UniversitéLibredeBruxelles
Hamilton,ON,Canada Bruxelles,Belgium
ISSN0932-2353 ISSN1868-2561 (electronic)
SpringerSeriesinBiophysics
ISBN978-981-10-6243-8 ISBN978-981-10-6244-5 (eBook)
DOI10.1007/978-981-10-6244-5
LibraryofCongressControlNumber:2017952612
©SpringerNatureSingaporePteLtd.2017
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Preface
Chapters in this volume discuss several aspects of the physical properties of
biological membranes and how these properties influence their functioning. The
reviews emphasize the mechanisms that result in these changes in membrane
propertiesandfunction.
Oneoftherapidlydevelopingareasinmembranebiophysicsinrecentyearshas
beentheroleoftransbilayerlipidasymmetry.Itisknownthatthelipidcomposition
ofthebilayerofabiologicalmembraneisverydifferentforthetwomonolayersthat
composethisbilayer.Moststudiesofmodelmembraneshaveemployedmembranes
withidenticalcompositionforthetwomonolayers.Therearetechnicaldifficulties
in making model membranes with transbilayer asymmetry. Chapter 1 describes
the methods that are being developed to facilitate the preparation of asymmetric
modelmembranesandhowthepresenceofthistransbilayerlipidasymmetryaffects
the physical properties of the membrane. The maintenance of transbilayer lipid
asymmetryisintimatelyconnectedwiththeratesoflipidflip-flop,i.e.themovement
of lipid from one face of the bilayer to the opposite side. In model membranes
devoid of protein, flip-flop rates of polar lipids are generally very slow. However,
in biological membranes these rates can be accelerated by specific proteins, in
some cases using an active transport mechanism, as well as through non-specific
disordering of membrane packing compared with a pure lipid membrane. Chapter
2discusseshowtheflippingrateisdependentonboththechemicalstructureofthe
lipidaswellasonthephysicalstateofthemembrane.Resultsofstudiesofflip-flop
ratesobtainedbothfromexperimentsaswellascomputersimulationsarepresented.
Thetwoprinciplecomponentsofbiologicalmembranesareproteinsandlipids.
The function of membrane proteins is modulated by lipids, both by binding to
specific lipid binding sites on the protein as well as by modulating the general
biophysical properties of the membrane. Some of these properties, including the
formation of supercritical fluids as well as long range interactions involving
curvature stress, curvature elasticity and hydrophobicity play key roles in the
coupling of lipids and proteins. The mechanisms of this modulation of membrane
protein function through coupling with the physical properties of the membrane
v
vi Preface
are reviewed in Chap. 3. Chapter 4 describes how mechano-sensitive channels
canbegatedbystretchingofthebilayer(forces-from-lipidsprinciple)and/orbythe
forces conveyed to the channel from the cytoskeleton/extracellular matrix(force-
from filament). The final two Chapters deal with larger scale systems. Chapter 5
discusses mechanisms of changes in cell shape. The factors involved can include
thecytoskeleton,membrane-bendingproteinsandmembranebiophysicalproperties
includingaroleforlipiddomainsincellmembranes.ThefinalChapterconsidersthe
liposomeasaminimalcellularmodelthatcanbeusedtosimulatediverseprocesses
from the origin-of-life to a reconstituted biochemical pathway. The possibility of
applyingsuchsystemsforfuturebiotechnologicalapplicationsisalsoconsidered.
This volume thus summarizes, from diverse points of view, the nature of
membranebiophysicalpropertiesandhowthesepropertiesimpingeonthevarious
functionsofabiologicalmembrane.
Hamilton,ON,USA RichardM.Epand
Bruxelles,Belgium Jean-MarieRuysschaert
Contents
1 Preparation and Physical Properties of Asymmetric Model
MembraneVesicles .......................................................... 1
JohnnaR.St.Clair,QingWang,GuangtaoLi,andErwinLondon
2 SpontaneousLipidFlip-FlopinMembranes:AStillUnsettled
PicturefromExperimentsandSimulations............................... 29
MariaMaddalenaSperottoandAlbertaFerrarini
3 MembraneLipid-ProteinInteractions .................................... 61
MichaelF.Brown,UdeepChawla,andSuchithrangaM.D.C.Perera
4 PrinciplesofMechanosensingattheMembraneInterface.............. 85
Navid Bavi, Yury A. Nikolaev, Omid Bavi, Pietro Ridone,
Adam D. Martinac, Yoshitaka Nakayama, Charles D. Cox,
andBorisMartinac
5 LipidDomainsandMembrane(Re)Shaping:FromBiophysics
toBiology ..................................................................... 121
Catherine Léonard, David Alsteens, Andra C. Dumitru,
Marie-PauleMingeot-Leclercq,andDonatienneTyteca
6 Minimal Cellular Models for Origins-of-Life Studies and
Biotechnology................................................................. 177
PasqualeStano
vii
Chapter 1
Preparation and Physical Properties
of Asymmetric Model Membrane Vesicles
JohnnaR.St.Clair,QingWang,GuangtaoLi,andErwinLondon
Abstract Modelbiomembranevesiclescomposedoflipidshavebeenwidelyused
toinvestigatetheprinciplesofmembraneassemblyandorganization.Alimitationof
thesevesicleshasbeenthattheydonotmimicthetransbilayerlipidasymmetryseen
inmanynaturalmembranes,mostnotablytheasymmetryintheplasmamembrane
of eukaryotic cells. Recently, a number of approaches have been developed to
prepare asymmetric membranes and study their properties. This review describes
methods to prepare asymmetric model membranes, and the physical properties
of asymmetric lipid vesicles. Emphasis is placed on the vesicles prepared by
cyclodextrin-catalyzed exchange, which has proven to be a versatile and powerful
tool,includingforstudiesmanipulatinglipidasymmetryinlivingcells.
Keywords Membrane domains (cid:129) Liquid ordered state (cid:129) Sphingolipids (cid:129)
Phospholipids (cid:129) Cyclodextrins
1.1 LipidAsymmetry:DefinitionandOrigin
When studying biological membrane organization and function, one important
aspect to consider is lipid asymmetry. Lipid asymmetry refers to the difference in
lipidcompositionintheouter(exoplasmic,exofacial)leafletvs.theinner(cytoplas-
mic, cytofacial) leaflet of a membrane. Many cell membranes possess lipid asym-
metry. In mammalian cells, the outer leaflet of the plasma membrane is enriched
in sphingomyelin (SM), glycosphingolipids (GSL) and phosphatidylcholine (PC),
while the inner leaflet is composed mainly of phosphatidylethanolamine (PE),
and anionic lipids such as phosphatidylserine (PS) and phosphatidylinositol (PI)
(Fig. 1.1) [1]. Cholesterol is present in both leaflets, but its distribution is still in
dispute[2,3].
J.R.St.Clair(cid:129)Q.Wang(cid:129)G.Li(cid:129)E.London((cid:2))
DepartmentofBiochemistryandCellBiology,StonyBrookUniversity,
StonyBrook,NY,11794-5215,USA
e-mail:[email protected]
©SpringerNatureSingaporePteLtd.2017 1
R.M.Epand,J.-M.Ruysschaert(eds.),TheBiophysicsofCellMembranes,
SpringerSeriesinBiophysics19,DOI10.1007/978-981-10-6244-5_1
2 J.R.St.Clairetal.
Fig.1.1 Representation of lipid asymmetry in natural biomembranes. In mammalian cells the
outer,orexofacial,leafletisenrichedinsaturatedacyl-chainsphingomyelinandinphosphatidyl-
choline,whiletheinner,orcytofacial,leafletiscomposedprimarilyofphosphatidylethanolamine
andphosphatidylserine.Cholesterol,showningrayispresentinbothleaflets
Incells,lipidasymmetryismaintainedbyflippasesandfloppases,enzymesthat
control the movement of lipids across the bilayer, and by enzymes that synthesize
and degrade lipids in one or the other leaflet [4]. Lipid flip-flop, or the transverse
diffusion of lipids from one leaflet to another, counteracts asymmetry. The rate of
spontaneous phospholipid flip-flop in the absence of proteins is generally slow,
and can take days [5–9]. In contrast, cholesterol with its small and weakly polar
headgroup,cancrossthelipidbilayerinaminuteorless[10].
1.2 BiologicalFunctionofAsymmetry
The full significance of lipid asymmetry remains elusive, but is known to be
important in several biological processes. For example, the loss of PS asymmetry
and the resulting display of PS in the outer leaflet of cell membranes is a signal
which leads to the consumption of apoptotic cells by phagocytes [11], and is also
asignalindicatingthatthemembranehasbeendamaged,promotingbloodclotting
[12]. Some viruses even display PS in their outer leaflet to encourage engulfment
bymacrophagesandachievehostinfection[13,14].
Asymmetry may also affect lipid-protein interaction. Transmembrane (TM)
proteins typically have a higher positive charge at the cytofacial end of their
TM helices relative to their exofacial end. This is known as the positive-inside
rule [15]. Lipid charge asymmetry, with a higher negative surface charge at the
inner leaflet/cytofacial surface, may help determine TM protein orientation, as
wellasinfluencetheconformationofpositivelychargedcytofacialjuxtamembrane
sequences [16]. Importantly, it has recently been observed that plasma membrane
TMsegmentsalsohaveanorientationalpreferenceasjudgedfromtheirabundance
innaturalsequences.ThesegmentsofTMheliceshavingaminoacidswithsmaller
sidechainsexhibitapreferencetobelocatedintheouterleafletrelativetotheinner
leaflet[17].