Table Of ContentTranscriptional Regulation by Neuronal Activity
Serena M. Dudek
Editor
Transcriptional Regulation
by Neuronal Activity
To the Nucleus and Back
SerenaM.Dudek
LaboratoryofNeurobiology
Synaptic&DevelopmentalPlasticityGroup
NIEHS/NIH
ResearchTrianglePark,NC27709
USA
[email protected]
ISBN:978-0-387-73608-2 e-ISBN:978-0-387-73609-9
LibraryofCongressControlNumber:2007937950
(cid:2)c 2008SpringerScience+BusinessMedia,LLC
Allrightsreserved.Thisworkmaynotbetranslatedorcopiedinwholeorinpartwithoutthewritten
permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York,
NY 10013, USA),except forbrief excerpts inconnection with reviews orscholarly analysis. Usein
connectionwithanyformofinformationstorageandretrieval,electronicadaptation,computersoftware,
orbysimilarordissimilarmethodologynowknownorhereafterdevelopedisforbidden.
Theuseinthispublicationoftradenames,trademarks,servicemarksandsimilarterms,eveniftheyare
notidentifiedassuch,isnottobetakenasanexpressionofopinionastowhetherornottheyaresubject
toproprietaryrights.
Cover illustration: High resolution confocal projection image from region CA3 of rat hippocampus.
This rat was exposed briefly and sequentially to “environment A” twice, once 30 min and the other
immediatelybeforesacrifice.TheredcolorshowsthedistributionofRNAtotheimmediate-earlygene
Arc. The blue color is the nuclear counterstain DAPI. Arc mRNA can be seen in cytoplasmic and
dendriticregions,andprovidesamarkerofneuronalactivation30minbeforesacrifice.Inaddition,two
strongArctranscriptionfocicanbeseeninthenucleusofthissameneuron.TheArctranscriptionfoci
provideamarkerofneuronalactivationfromwithin2toapproximately10minbeforesacrifice.Image
byJohnGuzowski,usedwithpermission.
Printedonacid-freepaper.
9 8 7 6 5 4 3 2 1
springer.com
Preface
Asyoureadthe chaptersof thisbook,neuronsin yourcentralnervoussystemare
undergoingsignificant changesat the nuclear level. Thanksto these changes, you
maysee,understand,andretain(atleastinpart)whatyouarereading.Oneofthese
nuclearevents,transcriptionalregulation,isimportantnotonlyforrestrictinggenes
to expression in tissue- and cell-specific manners, but also for controlling genes
in response to extracellular and/or environmental stimuli. In the unique case of
excitable cells that include neurons, genes can be and are regulated by neuronal
activity.
Activity-mediated gene regulation may occur as a result of neurotransmitter
releaseandsubsequentpost-orpre-synapticsignaling,oralternatively,itmaycome
in the form of postsynaptic action potentials and the resulting rise in intracellular
calcium or signaling at the membrane due to ion channel activation. What genes
are expressedin response to neuronalactivation?Screens have revealedthat most
of the genes can be described as falling into a few major categories: 1) those
that function to generally normalize the neuronal activity or otherwise facilitate
homeostasis, 2) those recruited for replacement of proteins used up or secreted,
or more rarely, 3) genes related to a particular function, such as for the mainte-
nance of synaptic plasticity. Activity-regulated genes also play important roles in
neuronaldevelopmentthatmayincludesynapsematurationorneuronalphenotype
determination.
TheideaforthebookcameoutofdiscussionsIhadwithAlisonBarthwhilewe
wereplanningamini-symposiumonthetopicforthe2005SocietyforNeuroscience
meeting.Althoughmostofouroriginalspeakersatthesymposiumwereunavailable
to contribute to the book, I was surprised by just how many authors did agree to
participate.Inhindsight,Idon’tknowwhyIwassosurprised.Thetopicisonethat
hasblossomedinto a thrivingfield, andI foundthatthere were manyenthusiastic
would-beauthorswantingtotelltheirstories.Inthisbook,Ihaveattemptedtobring
togetherchaptersthatcoverthreemaintopics:signalinitiationandtransductionto
thenucleus,consequentgeneregulationwithinthenucleus,andpossiblefunctions
oftheactivity-regulatedgenes.Pleasebearwiththeunavoidableoverlapinthegen-
eral topics and omissions of specific ones; as the field is rapidly expanding, it is
becomingincreasingly difficult to cover the field in its entirety. Nevertheless, this
v
vi Preface
bookshouldprovidebothexpertsinthefieldandstudentsofbiologywithanupdate
onwherethelast20yearsofstudyhastakenusinthenascentfieldoftranscriptional
regulationbyneuronalactivity.
SerenaM.Dudek
Contents
PartI Activity-regulatedTranscription:GettingtotheNucleus
1 TranscriptionalRegulationofActivity-DependentGenes
byBirdsong ................................................ 3
TarcisoA.F.VelhoandClaudioV.Mello
2 TotheNucleuswithProteomics................................ 27
BryenA.JordanandEdwardB.Ziff
3 TranscriptionalRegulationofthe Tbr1-CASK-CINAPProtein
ComplexinResponsetoNeuronalActivity ...................... 51
Yi-PingHsueh
4 IntracellularCalciumWavesTransmitSynapticInformation
totheNucleusinHippocampalPyramidalNeurons............... 73
MarkF.Yeckel,AmandaA.Sleeper,JohnS.Fitzpatrick,
DanielN.Hertle,AnnaM.Hagenston,andRobinT.Garner
5 Role of Action Potentials in Regulating Gene Transcription:
RelevancetoLTP ........................................... 91
J.PaigeAdams,RachelA.Robinson,andSerenaM.Dudek
6 L-typeChannelRegulationofGeneExpression .................. 111
NataliaGomez-OspinaandRicardoDolmetsch
PartII Activity-regulatedTranscription:GeneRegulation
7 CREB-DependentTranscriptionandSynapticPlasticity........... 127
AngelBarco,DraganaJancic,andEricR.Kandel
8 Activity-DependentRegulationofBrain-derived
neurotrophicfactorTranscription .............................. 155
AnneE.West
vii
viii Contents
9 Role of Signal-responsive Class IIa Histone Deacetylases in
RegulatingNeuronalActivity-dependentGeneExpression......... 175
BrianYeeHongLamandSangeetaChawla
10 NFAT-Dependent Gene Expression in the Nervous System:
ACriticalMediatorofNeurotrophin-InducedPlasticity........... 187
RachelD.GrothandPaulG.Mermelstein
11 Activity-DependentBigenomic TranscriptionalRegulationof
CytochromecOxidaseinNeurons ............................. 209
MargaretT.T.Wong-Riley,HuanLingLiang,
andSakkapolOngwijitwat
12 NotJustforMuscleAnymore:ActivityandCalciumRegulation
of MEF2-Dependent Transcription in Neuronal Survival
andDifferentiation .......................................... 229
AryamanShaliziandAzadBonni
PartIII Activity-regulatedTranscription:
RoleinNervousSystemFunction
13 SynapticGrowthandTranscriptionalRegulationinDrosophila .... 253
CynthiaBarberandJ.TroyLittleton
14 MMP-9/TIMP-1ExtracellularProteolyticSystemasAP-1
TargetinResponsetoNeuronalActivity ........................ 277
GrzegorzM.WilczynskiandLeszekKaczmarek
15 Activity-dependentGeneTranscriptioninNeurons:
DefiningthePlasticityTranscriptome .......................... 295
AlisonL.BarthandLinaYassin
16 TranscriptionalMechanismsUnderlying
theMammalianCircadianClock .............................. 313
Hai-YingMaryChengandKarlObrietan
17 IntersectingGeneticswithLifestyle:theRoleofExerciseand
DietinSynapticPlasticityandCognitiveEnhancement ........... 337
FernandoGomez-PinillaandShoshannaVaynman
18 CREBResponsiveTranscriptionandMemoryFormation ......... 377
ThomasC.Tubon,Jr.andJerryC.P.Yin
19 Dynamic Transcription of the Immediate-Early Gene Arc in
HippocampalNeuronalNetworks:InsightsintotheMolecular
andCellularBasesofMemoryFormation....................... 399
JohnF.Guzowski,TingNie,andTeikoMiyashita
Index ............................................................ 417
List of Contributors
J.PaigeAdams 77AvenueLouisPasteur
LaboratoryofNeurobiology Boston,MA02115
NationalInstitute USA
ofEnvironmentalHealthSciences
NationalInstitutesofHealth SangeetaChawla
111T.W.AlexanderDrive DepartmentofPharmacology
ResearchTrianglePark, UniversityofCambridge
NC27709 TennisCourtRoad
USA Cambridge,CB21PD
UK
AngelBarco
InstitutodeNeurocienciasdeAlicante Hai-YingMaryCheng
UMH-CSIC DepartmentofNeuroscience
SanJuandeAlicante TheOhioStateUniversity
Alicante,03550 333West10thAvenue
Spain Columbus,OH43210
USA
CynthiaBarber
DepartmentofBiology RicardoDolmetsch
MassachusettsInstituteofTechnology DepartmentofNeurobiology
43VassarStreet StanfordUniversity
Cambridge,MA02139 299CampusDriveD229
USA Stanford,CA94305
USA
AlisonL.Barth
DepartmentofBiologicalSciences SerenaM.Dudek
CarnegieMellonUniversity LaboratoryofNeurobiology
4400FifthAvenue NationalInstituteofEnvironmental
Pittsburgh,PA15213 HealthSciences
USA NationalInstitutesofHealth
111T.W.AlexanderDrive
AzadBonni ResearchTrianglePark,
DepartmentofPathology NC27709
HarvardMedicalSchool USA
ix
x ListofContributors
JohnS.Fitzpatrick AnnaM.Hagenston
DepartmentofNeurobiology DepartmentofNeurobiology
YaleUniversitySchoolofMedicine YaleUniversitySchoolofMedicine
P.O.Box208001 P.O.Box208001
NewHaven,CT06520 NewHaven,CT06520
USA USA
RobinT.Garner
DanielN.Hertle
DepartmentofNeurobiology
DepartmentofNeurobiology
YaleUniversitySchoolofMedicine
YaleUniversitySchoolofMedicine
P.O.Box208001
P.O.Box208001
NewHaven,CT06520
NewHaven,CT06520
USA
USA
NataliaGomez-Ospina
DepartmentofMolecular Yi-PingHsueh
Pharmacology InstituteofMolecularBiology
StanfordUniversity AcademiaSinica
299CampusDrive Taipei115
Stanford,CA94305 Taiwan
USA
DraganaJancic
FernandoGomez-Pinilla InstitutodeNeurocienciasdeAlicante
DepartmentofPhysiologicalSciences UMH-CSICSanJuandeAlicante
UniversityofCalifornia Alicante,03550
621CharlesE.YoungDrive Spain
LosAngeles,CA90095
USA
BryenA.Jordan
DepartmentofBiochemistry
RachelD.Groth
SchoolofMedicine
DepartmentofNeuroscience,
NewYorkUniversity
UniversityofMinnesota
550FirstAve
321ChurchStreet,SE
NewYork,NY10016
Minneapolis,MN55455
USA
USA
JohnF.Guzowski LeszekKaczmarek
DepartmentofNeurobiology DepartmentofMolecularand
andBehavior CellularNeurobiology
UniversityofCalifornia NenckiInstitute
108BonneyResearchLabs Pasteura3
Irvine,CA92697 PL-02-093Warsaw
USA Poland