Dynamic Plasma Membranes: Portals Between Cells and Physiology

253 Pages·2016·14.304 MB·English

by  Vann Bennett

VOLUMESEVENTYSEVEN
C T
URRENT OPICS IN
MEMBRANES
Dynamic Plasma Membranes:
Portals Between Cells and
Physiology
CURRENT TOPICS IN MEMBRANES, VOLUME 77
Series Editors
ROBERT BALABAN
National Heart, Lung and Blood Institute
National Institutes of Health
Bethesda, Maryland, USA
SIDNEY A. SIMON
Department of Neurobiology
Duke University Medical Centre
Durham, North Carolina, USA
VOLUME SEVENTY SEVEN
C T
URRENT OPICS IN
MEMBRANES
Dynamic Plasma Membranes:
Portals Between Cells
and Physiology
Edited by
VANN BENNETT
HHMI, and Department of Biochemistry,
Duke University Medical Center,
Durham, NC, USA
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CONTRIBUTORS
Vann Bennett
HHMI and Department of Biochemistry, Duke University Medical Center, Durham,
NC,USA
MaxBerkowitz
Department of Chemistry, University of North Carolinaat ChapelHill, ChapelHill,
NC,USA
AlexisR.Demonbreun
Center for Genetic Medicine, Northwestern University, Chicago,IL, USA
Nicolas Destainville
Laboratoire dePhysique Theorique(IRSAMC), Universite Toulouse 3-PaulSabatier,
UPS/CNRS, Toulouse, France
Masaki Fukata
Division of Membrane Physiology, Department of Cell Physiology, NationalInstitute
for Physiological Sciences, National Institutes of NaturalSciences; Department
of Physiological Sciences, School of Life Science, SOKENDAI (TheGraduate
University for AdvancedStudies), Okazaki,Japan
YukoFukata
Division of Membrane Physiology, Department of Cell Physiology, NationalInstitute
for Physiological Sciences, National Institutes of NaturalSciences; Department
of Physiological Sciences, School of Life Science, SOKENDAI (TheGraduate
University for AdvancedStudies), Okazaki,Japan
Thorsten Lang
Department of Membrane Biochemistry, Life &Medical Sciences (LIMES) Institute,
University of Bonn,Bonn,Germany
Christophe Leterrier
AixMarseille Université, CNRS, CRN2MUMR 7286, Marseille, France
Damaris N. Lorenzo
HHMI and Department of Biochemistry, Duke University Medical Center, Durham,
NC,USA
Elizabeth M.McNally
Center for Genetic Medicine, Northwestern University, Chicago,IL, USA
Tatsuro Murakami
Division of Membrane Physíology, Department of Cell Ph́ysiology, NationalInstitute
for Physiological Sciences, National Institutes of NaturalSciences; Department
of Physiological Sciences, School of Life Science, SOKENDAI (TheGraduate
University for AdvancedStudies), Okazaki,Japan
j
ix
x Contributors
ThomasH.Schmidt
Department of Membrane Biochemistry, Life &Medical Sciences (LIMES) Institute,
University of Bonn,Bonn,Germany
Norihiko Yokoi
Division of Membrane Physiology, Department of CellPhysiology, NationalInstitute
for Physiological Sciences, National Institutesof Natural Sciences; Department
of Physiological Sciences, School of Life Science,SOKENDAI (The Graduate
University for AdvancedStudies), Okazaki, Japan
PREFACE
Plasma membranes provide a critical interface between the interior of cells
and their external environment in all self-replicating organisms on our
planet. Plasma membranes are particularly important in multicellular ani-
mals those lack cell walls, where they are the site of cell–cell and cell
matrix interaction in tissues, as well as receptor-mediated signaling and
transport. At first glance, plasma membranes are deceptively simple: fluid
lipidbilayerswithembeddedproteinswherethedrivingforceforassembly
derives from exclusion of hydrophobic molecules from water. This view
was articulated in 1972 as the fluid mosaic model and has provided a
highly influential conceptual framework for thinking about membranes.
However, it has become abundantly clear that plasma membranes are
topologically quite varied with nano- and micron-scale domains, interact
extensively with intracellular proteins, and overall are much more com-
plex than that imagined 40years ago. The focus of this volume is on
recent advances in understanding plasma membrane organization and
function beginning with simple systems and extending to specialized
membrane domains of vertebrate cells.
The first chaptersby Berkowitz(A Molecular Look at Membranes)and
Destainville et al. (Where Biology Meets PhysicsdA Converging View on
MembraneMicrodomainDynamics)presentcontemporaryviewsofmem-
branes from a physical perspective. Berkowitz discusses insights into phase
separations and membrane–protein interactions based on computational
modeling.Hetermsthis approachcomputational microscopy, whichoper-
atesinatimerangeofmicrosecondsuptomillisecondsandspatialscalesup
to 10–20nm. Destainville et al. take us into the experimental realm and
focusoninsightsderivedfromSNAREproteinsthatformdynamicclusters
essential for exocytosis and neurotransmission. The spatial scale of these
SNARE clusters are100–300nm (referred to as mesoscale). Destainville et
al. also consider the role of membrane curvature, which assumes increasing
importance with larger dimensions.
Plasma membranes are only 4nm thick, yet must be preserved in spite
of potentially disruptive mechanical stresses experienced by active meta-
zoan organisms. Cardiac and skeletal muscles in vertebrates are particularly
j
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xii Preface
vulnerable to mechanical stress, which can result in diseases such as mus-
cular dystrophy and cardiomyopathy resulting from loss of membrane
integrity. Mechanisms are required to rapidly repair punctures or rips in
the plasma membrane to prevent catastrophic consequences of calcium
entryaswellaslossofcellularcontents.ThethirdchapterbyDemonbreun
and McNally (Plasma Membrane Repair in Health and Disease) summa-
rizes amembrane repair pathway required to maintain intact plasma mem-
branes in striated muscles that is based on interactions of ferlin family
members with annexins, EHD proteins, and MG53, which is an E3 ubiq-
uitin ligase.
Plasma membranes initially were conceived as bilayers with cotransla-
tionally inserted membrane-spanning integral proteins. However, cytosolic
proteins also can associate with membrane surfaces in a regulated fashion
through posttranslational modification with long-chain fatty acids such as
palmitic acid. Palmitoylation of proteins was discovered in viral coat pro-
teins in 1979, but remained relatively unstudied until a breakthrough
occurred in identification of palmitoyltransferases in yeast. Fukata et al.
in Chapter 5 (Local Palmitoylation Cycles and Specialized Membrane
DomainOrganization)reviewarapidlygrowingliteratureonnewlyappre-
ciated roles of the 23 mammalian palmitoyltransferases, including their
functions in dynamic regulation of membrane domains such as neuronal
synapses.
ThechapterbyBennettandLorenzo(AnAdaptableSpectrin/Ankyrin-
Based Mechanism for Long-Range Organization of Plasma Membranes in
Vertebrate Tissues) address a critical role of the peripheral membrane pro-
teins ankyrin andspectrininlong-range organization ofplasma membranes
into functional compartments. Ankyrin and spectrin were initially discov-
ered in human erythrocytes where they provide mechanical resilience by
coupling integral proteins through ankyrin to a spectrin–actin network
tightly associated with the cytoplasmic surface of the plasma membrane.
Ankyrin- and spectrin-based domains coordinate functionally related ion
transporters and cell adhesion molecules at sites such as excitable mem-
branes in the nervous system and lateral membranes of epithelial cells.
A mechanism is presented for facile acquisition of ankyrin interactions
with multiple membrane proteins during the evolution of vertebrates. In
the final chapter (The Axon Initial Segment, 50Years Later: A Nexus
for Neuronal Organization and Function) Leterrier discusses the roles of
Preface xiii
ankyrin-G and beta-4 spectrin as well as multiple other proteins in assem-
blyoftheaxoninitialsegment,whichisakeysiteofsignal integrationand
a distinguishing feature of vertebrate nervous systems. We hope these and
the other chapters will provide resources for readers interested in contem-
porary membrane biology and also serve to stimulate future discoveries in
this exciting area.
PREVIOUS VOLUMES IN SERIES
Current Topics in Membranes and Transport
Volume23GenesandMembranes:TransportProteinsandReceptors*(1985)
EditedbyEdwardA.AdelbergandCarolynW.Slayman
Volume24MembraneProteinBiosynthesisandTurnover(1985)
EditedbyPhilipA.KnaufandJohnS.Cook
Volume25RegulationofCalciumTransportacrossMuscleMembranes(1985)
EditedbyAdilE.Shamoo
Volume26Na+eH+Exchange,IntracellularpH,andCellFunction*(1986)
EditedbyPeterS.AronsonandWalterF.Boron
Volume27TheRoleofMembranesinCellGrowthandDifferentiation(1986)
EditedbyLazaroJ.MandelandDaleJ.Benos
Volume28PotassiumTransport:PhysiologyandPathophysiology*(1987)
EditedbyGerhardGiebisch
Volume29MembraneStructureandFunction(1987)
EditedbyRichardD.Klausner,ChristophKempf,andJosvanRenswoude
Volume30CellVolumeControl:FundamentalandComparativeAspectsinAnimal
Cells(1987)
EditedbyR.Gilles,ArnostKleinzeller,andL.Bolis
Volume31MolecularNeurobiology:EndocrineApproaches(1987)
EditedbyJeromeF.Strauss,III,andDonaldW.Pfaff
Volume32MembraneFusioninFertilization,CellularTransport,andViralInfection
(1988)
EditedbyNejatDu€zgu€nesandFelixBronner
Volume33MolecularBiologyofIonicChannels*(1988)
EditedbyWilliamS.Agnew,ToniClaudio,andFrederickJ.Sigworth
Volume34CellularandMolecularBiologyofSodiumTransport*(1989)
EditedbyStanleyG.Schultz
Volume35MechanismsofLeukocyteActivation(1990)
EditedbySergioGrinsteinandOriD.Rotstein
*PartoftheseriesfromtheYaleDepartmentofCellularandMolecularPhysiology
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