Na Channels from Phyla to Function

650 Pages·2016·33.155 MB·English

by  Robert J. French and Sergei Yu. Noskov (Eds.)

VOLUMESEVENTYEIGHT
C T
URRENT OPICS IN
MEMBRANES
Na Channels from Phyla
to Function
CURRENT TOPICS IN MEMBRANES, VOLUME 78
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 EIGHT
C T
URRENT OPICS IN
MEMBRANES
Na Channels from Phyla
to Function
Edited by
ROBERT J. FRENCH
Department of Physiology and Pharmacology
and the Hotchkiss Brain Institute;
Cumming School of Medicine
University of Calgary, Calgary,
Alberta, Canada
SERGEI YU. NOSKOV
University of Calgary,
Centre for Molecular Simulation,
Department of Biological Sciences, Calgary, Canada
Amsterdam(cid:129)Boston(cid:129)Heidelberg(cid:129)London
NewYork(cid:129)Oxford(cid:129)Paris(cid:129)SanDiego
SanFrancisco(cid:129)Singapore(cid:129)Sydney(cid:129)Tokyo
AcademicPressisanimprintofElsevier
AcademicPressisanimprintofElsevier
50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates
525BStreet,Suite1800,SanDiego,CA92101-4495,UnitedStates
125LondonWall,LondonEC2Y5AS,UnitedKingdom
TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom
Firstedition2016
Copyright(cid:1)2016ElsevierInc.Allrightsreserved.
Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans,
electronicormechanical,includingphotocopying,recording,oranyinformationstorageand
retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek
permission,furtherinformationaboutthePublisher’spermissionspoliciesandour
arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright
LicensingAgency,canbefoundatourwebsite:www..elsevier.com/permissions.
Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby
thePublisher(otherthanasmaybenotedherein).
Notices
Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchand
experiencebroadenourunderstanding,changesinresearchmethods,professionalpractices,
ormedicaltreatmentmaybecomenecessary.
Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgein
evaluatingandusinganyinformation,methods,compounds,orexperimentsdescribed
herein.Inusingsuchinformationormethodstheyshouldbemindfuloftheirownsafetyand
thesafetyofothers,includingpartiesforwhomtheyhaveaprofessionalresponsibility.
Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors,
assumeanyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterof
productsliability,negligenceorotherwise,orfromanyuseoroperationofanymethods,
products,instructions,orideascontainedinthematerialherein.
ISBN:978-0-12-805386-7
ISSN:1063-5823
ForinformationonallAcademicPresspublications
visitourwebsiteathttps://www.elsevier.com
Publisher:ZoeKruze
AcquisitionEditor:AlexWhite
EditorialProjectManager:HeleneKabes
ProductionProjectManager:VigneshTamil
CoverDesigner:GregHarris
TypesetbyTNQBooksandJournals
DEDICATION
WededicatethisvolumetothememoryofHarryA.Fozzard(1931–2014),
an extraordinary physician-scientist, colleague, collaborator, and friend.
Harry made landmark contributions to the understanding of cardiac physi-
ology in general, and of voltage-gated sodium channels, in particular.
CONTRIBUTORS
K.Aimar
DepartmentofBiomedicalPhysiologyandKinesiology,SimonFraserUniversity,Burnaby,
BC,Canada
T.W.Allen
RMITUniversity,Melbourne,VIC,Australia;UniversityofCaliforniaDavis,Davis,CA,
UnitedStates
C.Barbosa
IndianaUniversitySchoolofMedicine,Indianapolis,IN,UnitedStates
C.Boiteux
RMITUniversity,Melbourne,VIC,Australia
E.D.Brodie,III
UniversityofVirginia,Charlottesville,VA,UnitedStates
V.Carnevale
TempleUniversity,Philadelphia,PA,UnitedStates
C.E.Clancy
UniversityofCalifornia,Davis,Davis,CA,UnitedStates
R.B.Clark
UniversityofCalgary,Calgary,AB,Canada
T.R.Cummins
IndianaUniversitySchoolofMedicine,Indianapolis,IN,UnitedStates
0
N.DAvanzo
UniversitédeMontréal,Montréal,QC,Canada
P.G.DeCaen
Children’sHospitalBoston,Boston,MA,UnitedStates;HarvardMedicalSchool,Boston,
MA,UnitedStates;NorthwesternUniversity,Chicago,IL,UnitedStates
K.R.DeMarco
UniversityofCalifornia,Davis,Davis,CA,UnitedStates
C.Domene
King’sCollegeLondon,London,UnitedKingdom;UniversityofOxford,Oxford,United
Kingdom
S.C.Dudley,Jr.
TheWarrenAlpertMedicalSchoolofBrownUniversity,Providence,RI,UnitedStates
S.Furini
UniversityofSiena,Siena,Italy
V.S.Gawali
MedicalUniversityofVienna,Vienna,Austria
j
xv
xvi Contributors
S.Geffeney
UtahStateUniversityUintahBasin,Vernal,UT,UnitedStates
R.Ghadiry-Tavi
DepartmentofBiomedicalPhysiologyandKinesiology,SimonFraserUniversity,Burnaby,
BC,Canada
M-R.Ghovanloo
DepartmentofBiomedicalPhysiologyandKinesiology,SimonFraserUniversity,Burnaby,
BC,Canada
W.R.Giles
UniversityofCalgary,Calgary,AB,Canada
D.Granata
TempleUniversity,Philadelphia,PA,UnitedStates
B.R.Green
UniversityofUtah,SaltLakeCity,UT,UnitedStates;MonashUniversity,Parkville,VIC,
Australia
C.Hanifin
UtahStateUniversityUintahBasin,Vernal,UT,UnitedStates
C.Ing
HospitalforSickChildren,Toronto,ON,Canada;UniversityofToronto,Toronto,ON,
Canada
L.L.Isom
UniversityofMichiganNeuroscienceProgram,AnnArbor,MI,UnitedStates;Universityof
MichiganMedicalSchool,AnnArbor,MI,UnitedStates
B.Joos
UniversityofOttawa,Ottawa,ON,Canada
M.A.Kasimova
TempleUniversity,Philadelphia,PA,UnitedStates
M.Liu
TheWarrenAlpertMedicalSchoolofBrownUniversity,Providence,RI,UnitedStates
E.G.Moczydlowski
CaliforniaNorthstateUniversity,RanchoCordova,CA,UnitedStates
C.E.Morris
OttawaHospitalResearchInstitute,Ottawa,ON,Canada
V.Oakes
King’sCollegeLondon,London,UnitedKingdom
B.M.Olivera
UniversityofUtah,SaltLakeCity,UT,UnitedStates
R.Pom(cid:1)es
HospitalforSickChildren,Toronto,ON,Canada;UniversityofToronto,Toronto,ON,
Canada
Contributors xvii
P.C.Ruben
DepartmentofBiomedicalPhysiologyandKinesiology,SimonFraserUniversity,Burnaby,
BC,Canada
D.B.Tikhonov
RussianAcademyofSciences,St.Petersburg,RussianFederation
H.Todt
MedicalUniversityofVienna,Vienna,Austria
G.Toledo
UniversityofVirginia,Charlottesville,VA,UnitedStates
T.N.Vien
TuftsUniversity,Boston,MA,UnitedStates
J.J.Winters
UniversityofMichiganNeuroscienceProgram,AnnArbor,MI,UnitedStates
K.-C.Yang
TheWarrenAlpertMedicalSchoolofBrownUniversity,Providence,RI,UnitedStates
A.Yu
DepartmentofBiomedicalPhysiologyandKinesiology,SimonFraserUniversity,Burnaby,
BC,Canada
B.S.Zhorov
McMasterUniversity,Hamilton,ON,Canada;RussianAcademyofSciences,St.Petersburg,
RussianFederation
PREFACE
Sodium Channels: Structure, Function, and Beyond
Emerging Views in the 21st Century
In 2012, the entire field of membrane biophysics and physiology celebrated
the 60th anniversary (Catterall, 2012) of seminal papers published by
Hodgkin and Huxley revealing a selective, gated Na+ conductance as an
essential and vital part of the action potential propagation in excitable cells
(Hodgkin & Huxley, 1952a, 1952b; Hodgkin, Huxley, & Katz, 1952). We
now know this conductance to be mediated by members of the family of
voltage-gated sodium channel proteins (Nav). Nav channels have been the
focus of numerous recent reviews, including Ahern, Payandeh, Bosmans,
and Chanda (2016), Catterall (2014a, 2014b), Payandeh and Minor (2015),
which were published in the last 2years. In the past six decades, progress in
the study of ion transport by Na+ channels and various roles played by
theminvirtuallyalltissueshavebeenacceleratedduetoanumberofadvance-
ments in experimental techniques ranging from conventional X-ray crystal-
lography to cryo-EM, spectroscopic techniques including rapidly evolving
FRET and LRET, low-noise electrophysiology, and ultrahigh resolution
microscopy to name a few of many (Ahern et al., 2016; Lacroix, Campos,
Frezza, & Bezanilla, 2013; Payandeh & Minor, 2015)!
The legacy of Hodgkin and Huxley instilling marriage between physics
of ion transport and experimental protocols led to an intimate connection
between experimental studies and mathematical modeling of the action
potential where detailed models of sodium channel function were tightly
coupledtoelectrophysiologicalrecordingsofselectiveiontransport,activa-
tionanddeactivationdynamicsanditsperturbationbymutations,drugs,and
other environmental factors.
With the determination of the first crystal structure at high resolution
(Payandeh, Scheuer, Zheng, & Catterall, 2011), the field received fresh
impetus enabling detailed mapping of the molecular machinery of gating,
locationofdrug-bindingpockets,andprovidingmolecularbasesforvarious
roles played by the sodium channel in disease-linked mutations (Catterall,
2014a; McCusker et al., 2012).
Paralleltothegrowthinexperimentalinsightsandsophisticatedmathe-
matical models of Na+ channel function, the biomolecular simulations of
j
xix
xx Preface
ion channels in model membranes have made significant contributions to
ourunderstandingofselectiveiontransport,drugbinding,andgatingmech-
anisms.Asitisallbutimpossibletoobservetheatomicdetailsresponsiblefor
specific transport processes with existing experimental approaches, compu-
tational studies provide an invaluable window onto these processes, estab-
lishing a basis for formal theories and providing testable predictions.
Therefore,weareinauniquepositiontoobtaindetailedmolecularinsights
into the properties of membrane proteins and directly link experimental
observationstomolecularsimulationsatdifferentscales.Wecannowapply
a combination of modeling and experimental techniques to studies of Na+
channels to provide a multiscale platform linking chemical transitions in
single-ionchannelstothecontrolofprocessessuchasthedynamicvariation
oftheheart’srhythmatthecellularororganlevel.Theunionofmolecular
simulations driving and/or driven by experimental explorations into
membrane proteins has already produced remarkable results, including the
discoveryoffundamentalkineticandthermodynamicmechanismsunderly-
ingselectivetransportcriticalincellularsignalingandtheelucidationofkey
mechanisms of protein function regulation by lipids, to name a few.
Of particular note, experimental and theoretical studies over recent
decades have revealed converging evolutionary mechanisms by which bio-
physical function is coupled to protein structure. Hence, methods that link
slowconformationaldynamicsofproteinswithmembranedynamicssuchas
bendingarecriticaltomakingprogressinourstudyofbiomembranes.This
volume provides a comprehensive discussion on the development of novel
methodologies,multiscalesimulationsandexperimentalstudiesofNachan-
nels in various cells and tissues, and apparent implications to normal heart
andbrainfunction.Thewell-orchestratedopeningandclosingofNachan-
nelsisanessentialcontrolmechanismforelectricalexcitationandrelaxation
in brain and heart tissues. Abnormalities resulting from inherited mutations
and/orpharmacologicalblockadeofNachannelsaretightlyassociatedwith
aberrations in action potentials, leading to the development of severe
arrhythmias and neurological disorders such as neonatal epilepsy.
The first structures of Na channels opened an avenue for detailed
computationalstudiesofselectivetransportmechanismsprovidingunprece-
dented insights into the bases of Nav channel function and roles.
This present issue of Current Topics in Membranes entitled Na-Channels,
From Phyla to Function presents a collection of articles that summarizes the
cuttingedgeofinvestigationsintostructureandfunctionforthisremarkable
class of membrane proteins from the excitable cells. Although there are