Phosphoinositides I: Enzymes of Synthesis and Degradation

362 Pages·2012·5.054 MB·English

by  Shane Minogue, Mark G. Waugh (auth.), Tamas Balla, Matthias Wymann, John D. York (eds.)

Phosphoinositides I: Enzymes of Synthesis
and Degradation
SUBCELLULARBIOCHEMISTRY
SERIESEDITOR
J.ROBINHARRIS,UniversityofMainz,Mainz,Germany
ASSISTANTEDITOR
P.J.QUINN,King’sCollegeLondon,London,U.K.
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Tamas Balla (cid:129) Matthias Wymann (cid:129) John D.York
Editors
Phosphoinositides I:
Enzymes of Synthesis
and Degradation
2123
Editors
Dr.TamasBalla Dr.JohnD.York
NationalInstitutesofHealth DukeUniversityMedicalCenter
NICHD PharmacologyandCancer
Bethesda,MD Biology
USA Durham,NC
USA
Dr.MatthiasWymann
UniversityofBasel
Cancer-andImmunobiology
Basel,Switzerland
ISBN978-94-007-3011-3 e-ISBN978-94-007-3012-0
DOI10.1007/978-94-007-3012-0
SpringerDordrechtHeidelbergLondonNewYork
LibraryofCongressControlNumber:2012931684
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Preface
WhenIwasapproachedtoshapeabookaboutphosphoinositidesignaling,Ifirstfelt
honoredandhumbled. Onsecondthought, thisappearedtobeanimpossibletask.
Phosphoinositideshavegrownfrombeingjustacuriouslipidfractionisolatedfrom
bovinebrain,showingincreasedradioactivemetaboliclabelingduringintensestimu-
lationprotocols,tobecomethefocusofimmenseinterestaskeyregulatorymolecules
thatpenetrateeveryaspectofeukaryoticbiology.Theexpansionofthisfieldinthe
last three decades has been enormous: it turned from a basic science exercise of a
devotedfewtohighlytranslatablesciencerelevanttoalargenumberofhumandis-
eases(isn’tthisthenatureofgoodbasicscience?).Theseincludecancer,metabolic-,
immuno-andneurodegenerativedisorders,tonamejustafew.Reviewingthelarge
numberofenzymesthatconvertphosphoinositideswouldfillabook—letalonethe
diverse biological processes in which phosphoinositides play key regulatory roles.
Giventheinterest, acollectionofup-to-datereviewscompiledinabookisclearly
warranted,whichwasenoughtoswaymetoacceptthisassignment.Asoneeditor
isunabletohandlethisenormoustask,IwasdelightedwhenMatthiasWymannand
JohnYorkwerekindenoughtojoinmeinthisambitiouseffort.
When thinking about potential authors, the obvious choice would have been to
approachthepeoplewhosecontributionshavebeencrucialtopushandelevatethis
fieldtothelevelitistoday.BobMichell,propheticallyplacedphosphoinositidesin
thecenterofsignaltransductionina1975Biochem.Biophys.Actareview(Michell
1975),MichaelBerridgehadakeyroleinlinkingphosphoinositidesandCa2+ sig-
nalingandwhosefascinatingreviewshaveinspiredmanyofus(BerridgeandIrvine
1984). RobinIrvine, whosegroupfoundthatInsP wasamixtureoftwoisomers,
3
theactiveIns(1,4,5)P andaninactiveIns(1,3,4)P , andwhodescribedthetetrak-
3 3
isphosphatepathway(Irvineetal.1986),andwhoalwayschallengesuswithmost
provocativeideas. PhilipMajerus, whohasinsistedontheimportanceofinositide
phosphatases(Majerusetal.1999)veryearlyon.ThegroupofLewisCantley,with
the discovery of PI 3-kinase activities and the mapping of downstream effectors
(Whitman et al. 1988; Franke et al. 1997), or theWaterfield lab where the first PI
3-kinase catalytic subunit was isolated and cloned (Otsu et al. 1991; Hiles et al.
1992). Peter Downes, who recognized the translational value of phosphoinositide
research.JeremyThornerandScottEmr,whoseworkinbaker’syeaststillformsthe
v
vi Preface
foundation of our understanding of the role of inositol lipids in trafficking (Strahl
andThorner2007)orPietroDeCamilli,whosegroupdocumentedthecentralroleof
inositidesinbrainandsynapticbiology(Cremonaetal.1999).Therearemanyothers
whomadevaluableorevengreatercontributionstophosphoinositideresearch.The
abovelistreflectsmybias,astheseresearchershadthelargestimpactonmythinking
andthedirectionsofmywork.Researchis,however,aconstantlyevolvingprocess
and we (now Matthias and John being involved) wanted to involve contributions
ofscientistswhorepresentasecondorthirdwaveofresearchersinfectedwiththe
interest in phosphoinositides. We made an effort to recruit authors who have been
traineesofthesefoundinglaboratories.Withthisselectionourgoalwastosample
the view of the current and future generation. By selecting their trainees, we feel
thatwepaytributetothe“FoundingFathers”, andshowthattheresearchtheyput
inmotionisaliveandcontinueswithfreshideas,newambitionsandatranslational
andtherapeuticvalue.
Phosphoinositideresearchinthe1980swenthandinhandwithresearchonCa2+
signalingpursuedin“non-excitable”cellsandwasalsomarkedwiththediscoveryof
thefamilyofproteinkinaseCenzymes,regulatedbydiacylglycerol,oneoftheprod-
uctsofphosphoinositide-specificphospholipaseCenzymes.Theseareasofresearch
developedandexpandedtoformtheirownfields,andcouldnotbediscussedherein
detail—eventhoughtheyarelinkedhistoricallytothedevelopmentofphosphoinosi-
tidesignaling.TheenormousworkofthegroupsofYasutomiNishizukaonprotein
kinaseC,andKatsuhikoMikoshibaoncloningandcharacterizingtheIns(1,4,5)P
3
receptorsareprimeexamplesoftheseachievements.Althoughwecouldnotcover
alltheseareas,weincludedachapteronCa2+ signalingviatheIns(1,4,5)P recep-
3
torbyColinTaylor, atraineeoftheMichaelBerridge’slab, whereimportantlinks
betweenCa2+releaseandIns(1,4,5)P receptorsignalingwerediscovered.Wealso
3
decided to allocate some space to inositol phosphates, the soluble counterparts of
someofthephosphoinositides.Thesemoleculesforlonghadbeenviewedonlyas
the metabolic products of the second messenger Ins(1,4,5)P but recently gained
3
significantprominenceasregulatorsofimportantphysiologicalprocesses.Withthe
discovery of the highly phosphorylated and pyrophosphorylated inositols and the
enzymesthatproducethem,itbecameclearthatthissystemrepresentsawholenew
regulatoryparadigmwithexcitingnewdevelopments.
Finally, it was a difficult dilemma whether to include a Chapter on the early
historyofphosphoinositides.Wedecidedagainstitforanumberofreasons. First,
thereallyinterestinghistoryistracedbacktostudiesthatprecededthelandmark1975
BobMichellreviewandincludedtheworkoftheHokins(1987),BernardAgranoff
(2009)andotherpioneersofphosphoinositideresearch.Nobodycouldtelltheseearly
developmentsbetterthanBobMichellinhisseveralrecollections(Michell1995)or
RobinIrvinewhocommemoratedthe20yearsofIns(1,4,5)P andtheperiodleading
3
toitsdiscovery(Irvine2003).Weencouragetheyoungreaderstogobackandread
these recollections, as they show several examples of how seemingly uninspiring
observations formed the beginning of something that became huge as it unfolded.
What came after these landmark discoveries is so overwhelming that each one of
us has own views and subjective memories and stories to tell on some aspects of
Preface vii
it. As Editors we felt that our views should not be elevated above others on these
historicalaspects,andleaveittotheauthorsoftheindividualChapterstoelucidate
the diversity in this respect. The only exception is a Chapter on the history of PI
3-kinases byAlexToker that we felt deserves special emphasis as it had the most
transformingimpactonthefieldsincethelate1980s.
Oneneedstounderstandthatselectionofauthorsisasubjectiveprocessanddoes
notalwaysreflectonwhocontributedthemostinaselectedfield.However,weare
confident that proper credit is given in the individual Chapters to each groups and
individualswhoseworkhasmovedthisfieldforward.Itshouldalsobeunderstood
that a field that generates over 10,000 entries in PubMed with each keyword that
relates to phosphoinositides cannot be covered without missing some aspects that
couldbeimportant. However, wetrustthatthiscollectionwillbefoundusefulfor
boththeexpertsandthenovices.
References
AgranoffBW(2009)Turtlesalltheway:Reflectionsonmyo-Inositol.JBiolChem284(32):21121–
21126
BerridgeMJ,IrvineRF(1984)Inositoltrisphosphate,anovelsecondmessengerincellularsignal
transduction.Nature312:315–321
CremonaO,etal(1999)Essentialroleofphosphoinositidemetabolisminsynapticvesiclerecycling.
Cell99:179–188
FrankeTF,KaplanDR,CantleyLC,TokerA(1997)DirectregulationoftheAktprotooncogene
productbyPI3,4P2.Science275:665–668
HilesIDetal(1992)Phosphatidylinositol3-kinase:structureandexpressionofthe110kDacatalytic
subunit.Cell70:419–429
HokinLE(1987)Theroadtothephosphoinositide-generatedsecondmessengers.TrendsPharmacol
Sci8:53–56
IrvineRF(2003)20yearsofIns(1,4,5)P3,and40yearsbefore.NatRevMolCellBiol4(7):586–590
IrvineRF,LetcherAJ,HeslopJP,BerridgeMJ(1986)Theinositoltris/tetrakisphosphatepathway—
demonstrationofinositol(1,4,5)trisphosphate-3-kinaseactivityinmammaliantissues.Nature
320:631–634
Majerus PW, Kisseleva MV, Norris FA (1999) The role of phosphatases in inositol signaling
reactions.J.BiolChem274:10669–10672
MichellB(1995)Earlystepsalongtheroadtoinositol-lipid-basedsignalling.TrendsBiochemSci
20(8):326–329
MichellRH(1975)Inositolphospholipidsandcellsurfacereceptorfunction.BiochimBiophysActa
415:81–147
OtsuMetal(1991)Characterizationoftwo85kDaproteinsthatassociatewithreceptortyrosine
kinases,middle-T/pp60c-srccomplexes,andPI3-kinase.Cell65:91–104
StrahlT,ThornerJ(2007)Synthesisandfunctionofmembranephosphoinositidesinbuddingyeast,
Saccharomycescerevisiae.BiochimBiophysActa1771(3):353–404
WhitmanM,DownesCP,KeelerM,KellerT,CantleyL(1988)Type-Iphosphatidylinositolkinase
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Contents
1 ThePhosphatidylinositol4-Kinases:Don’tCallitaComeback ...... 1
ShaneMinogueandMarkG.Waugh
2 PIPKinasesfromtheCellMembranetotheNucleus............... 25
MarkSchramp,AndrewHedman,WeiminLi,XiaojunTan
andRichardAnderson
3 ThePhospholipaseCIsozymesandTheirRegulation............... 61
AurelieGresset,JohnSondekandT.KendallHarden
4 Phosphoinositide3-Kinases—AHistoricalPerspective.............. 95
AlexToker
5 PI3Ks—DrugTargetsinInflammationandCancer ................ 111
MatthiasWymann
6 Phosphoinositide3-KinasesinHealthandDisease ................. 183
AlessandraGhigo,FulvioMorello,AlessiaPerinoandEmilioHirsch
7 PhosphoinositidePhosphatases:JustasImportantastheKinases ... 215
JenniferM.Dyson,ClareG.Fedele,ElizabethM.Davies,
JelenaBecanovicandChristinaA.Mitchell
8 ThePTENandMyotubularinPhosphoinositide3-Phosphatases:
LinkingLipidSignallingtoHumanDisease ....................... 281
ElizabethM.Davies,DavidA.Sheffield,PriyankaTibarewal,
ClareG.Fedele,ChristinaA.MitchellandNicholasR.Leslie
Erratum.......................................................... E1
Glossary ......................................................... 337
Index ............................................................ 343
ix
Abbreviations
AD Alzheimer’sdisease
AMPK 5(cid:2)-AMP-activatedproteinkinase
ALL Acutelymphocyticleukemia
ALS Amyotrophiclateralsclerosis
AML Acutemyeloblasticleukemia
ARNO Arfnucleotidebindingsiteopener
ASK1 Apoptosissignal-regulatingkinase1
ATM Ataxiatelangiectasiamutated
ATX Arabidopsistrithorax1
Bad Bcl-XL/Bcl-2-associateddeathpromoter
BAFF BcellactivationfactoroftheTNFfamily
BCR Bcellreceptor
Bcr/Abl Breakpointclusterregion/Abelsonkinasefusionprotein
Btk Bruton’styrosinekinase
c-Kit Stemcellgrowthfactorreceptor
CAD CaspaseactivatedDNase
CCR(L) C-Cchemokinereceptor(ligand)type
CDK Cyclin-dependentkinase
CDKN2A Cyclin-dependentkinaseinhibitor2A
CERT Ceramidetransferprotein
CIN85 Cbl-interactin protein of 85kD (also Ruk (regulator of ubiqui-
tous kinase), SETA (SH3 domain-containing gene expressed in
tumorigenicastrocytes))
CML Chronicmyeloidleukemia
CMT Charcot-Marie-Tooth
COPI/II CoatomerproteincomplexI/II
CXCR(L) C-X-Cchemokinereceptor(ligand)type
DAAX Deathdomain-associatedprotein
DAG Diacylglycerol
DGK Diacylglycerolkinase
DH Dbl-homology
DMSO Dimethylsulfoxide
xi