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扫描下载送金币co-regulators,theDELLAproteins(12),whichpotentiatetheabilityofSPL9(directly)andLFY(indirectly)toinduceAP1andtotriggertheonsetofflowerformation(fig.S9).LFYinitiatesthereductioningibberellinlevels—whichresultsinincreasedDELLAaccumulation—atleastinpartbyinducingexpressionofthegibberellincatab-olismenzymeELA1.
Ourfindingsmayhelpexplainthepreviouslyparadoxicalobservationthatgibberellinactspos-itivelyintheswitchtoreproductivedevelopmentinmostplantsbutnegativelyinsomewoodyplantspecies,suchasgrapevine(29).Inaddition,ourdatamakegibberellinaprimecandidatefora“branching”factorpredictedbymathematicalmod-elingofinflorescencearchitectures(30).Finally,ourresultssuggestthatthedegreeofinflorescencebranching,whichdeterminesseedyieldand,thus,reproductivesuccess,couldbeadjustedbyalter-inggibberellinaccumulationbeforetheinflores-cenceformsortherateofgibberellincatabolismthereafter.
ReferencesandNotes
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12.A.Dill,H.S.Jung,T.P.Sun,Proc.Natl.Acad.Sci.U.S.A.
98,1(2001).
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Development139,(2012).
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Development139,(2012).
18.S.Yuetal.,PlantCell24,(2012).
19.R.N.Wilson,J.W.Heckman,C.R.Somerville,PlantPhysiol.
100,403–408(1992).
20.M.Koornneef,C.J.Hanhart,J.H.vanderVeen,
Mol.Gen.Genet.229,57–66(1991).
21.W.Rademacher,Annu.Rev.PlantPhysiol.PlantMol.Biol.
51,501–531(2000).
22.J.M.Davière,P.Achard,Development140,
23.X.Hou,L.Y.Lee,K.Xia,Y.Yan,H.Yu,Dev.Cell19,
884–894(2010).
24.K.Hiranoetal.,PlantJ.71,443–453(2012).
25.J.W.Wang,B.Czech,D.Weigel,Cell138,738–749
26.N.Yuetal.,PlantCell22,(2010).27.M.A.Blázquez,D.Weigel,Nature404,889–892
28.S.Eriksson,H.B?hlenius,T.Moritz,O.Nilsson,PlantCell
18,(2006).
29.P.K.Boss,M.R.Thomas,Nature416,847–850(2002).30.P.Prusinkiewicz,Y.Erasmus,B.Lane,L.D.Harder,
E.Coen,Science316,(2007).Acknowledgments:WearegratefultoWagnerlaboratorymembersandK.Gallagher,R.S.Poethig,andJ.D.Wagnerforcriticalcomments.WethankR.AustinfortheLFYbindingmotiffunctionaldepthanalyses,T.SunforpRGA:RGA-GFPandGApathwaymutantseeds,X.Chenfor35S:AlcRpAlcA:MIR156fandpRGA:RGA-HAseeds,M.SchmidforRGL1andrgl1delta17constructs,S.PoethigforpSPL9:rSPL9-FLAGand35S:SPL9-GRseeds,H.Yuforga1-3rgl2-1rga-235S:RGA-GRseeds,G.AngenentforpAP1:AP1-GFPseeds,andtheArabidopsisBiologicalResourceCenterforinsertionmutantseedsandtheF6A4bacterialartificialchromosomeclone.ThisworkwassupportedbyNSFgrantsIOS0849298and1257111toD.W.andtraininggrantT32-HD007516(DevelopmentalBiology)supporttoC.M.W.
SupplementaryMaterials
www.sciencemag.org/content/344//suppl/DC1MaterialsandMethodsFigs.S1toS9TablesS1andS2References(31–65)
7January2014;accepted2April6/science.1250498
CancerImmunotherapyBasedonMutation-SpecificCD4+TCellsinaPatientwithEpithelialCancer
EricTran,1SimonTurcotte,1*AlenaGros,1PaulF.Robbins,1Yong-ChenLu,1MarkE.Dudley,1+JohnR.Wunderlich,1RobertP.Somerville,1KatherineHogan,1ChristianS.Hinrichs,1MariaR.Parkhurst,1JamesC.Yang,1StevenA.Rosenberg1?
Limitedevidenceexiststhathumansmountamutation-specificTcellresponsetoepithelialcancers.Weusedawhole-exomic-sequencing-basedapproachtodemonstratethattumor-infiltratinglymphocytes(TIL)fromapatientwithmetastaticcholangiocarcinomacontainedCD4+Thelper1(TH1)cellsrecognizingamutationinerbb2interactingprotein(ERBB2IP)expressedbythecancer.AfteradoptivetransferofTILcontainingabout25%
mutation-specificpolyfunctionalTH1cells,thepatientachievedadecreaseintargetlesionswithprolongedstabilizationofdisease.Upondiseaseprogression,thepatientwasretreatedwitha&95%purepopulationofmutation-reactiveTH1cellsandagainexperiencedtumorregression.TheseresultsprovideevidencethataCD4+Tcellresponseagainstamutatedantigencanbeharnessedtomediateregressionofametastaticepithelialcancer.hehumanimmunesystemhasevolvedtorecognizeandeliminatecellsexpress-ingforeign,nonselfantigens.Allmalig-nanttumorsharbornonsynonymousmutationsorothergeneticalterations(1),someofwhichmaygenerateneo-“nonself”epitopesthatcouldpotentiallytriggeranantitumorTcellresponse.Indeed,mutation-reactiveTcellscanfrequent-lybefoundinfiltratinghumanmelanomas(2)andlikelyplayacriticalroleintheclinicalefficacyofadoptivecelltherapy(ACT)andotherimmunotherapiesinmelanoma(3–7).
However,limitedevidenceexistsdemonstrat-ingthatthehumanimmunesystemcanmountanendogenous,mutation-specificTcellresponseagainstepithelialcancersthatcompriseover80%ofallhumanmalignancies(8-11),anditisunclearwhetherthisresponsecanbehar-nessedtodevelopeffectivepersonalizedcancerimmunotherapies(12).Moreover,epithelialcancersoftencontainfewermutationsthanmelanoma(1),whichmaydecreasetheprob-abilityofelicitingamutation-specificTcellresponse.Wethusfirstsetouttodetermine
whethertumor-infiltratinglymphocytes(TIL)recognizingpatient-specificmutationscanbeidentifiedinpatientswithmetastaticgastro-intestinal(GI)cancers.
Tothisend,a43-year-oldwomanwithwidelymetastaticcholangiocarcinoma(patient3737,tableS1)whoprogressedthroughmultipleche-motherapyregimenswasenrolledinaTIL-basedACTprotocolforpatientswithGIcancers(NCT).Lungmetastaseswerere-sectedandusedasasourceforwhole-exomicse-quencingandgenerationofTcellsfortreatment.Whole-exomicsequencingrevealed26nonsynon-ymousmutations(tableS2).Totestwhetherthepatient’sTILrecognizedanyofthesemutations,weusedaminigeneapproach.Briefly,foreachmutationwedesignedaminigeneconstructthatencodedforthemutatedaminoacidflankedoneachsideby12aminoacidsfromtheendoge-nousprotein(fig.S1).Multipleminigenesweresynthesizedintandemtogeneratetandemminigene(TMG)constructs(fig.S1andtableS3),whichwerethenusedastemplatesforthegenerationofinvitrotranscribed(IVT)RNA(13).EachoftheseIVTTMGRNAswasthen
SurgeryBranch,NationalCancerInstitute(NCI),NationalInstitutesofHealth,Bethesda,MD20892,USA.
*Presentaddress:DepartmentofSurgery,UniversitédeMontréal,andInstitutduCancerdeMontréal,CentredeRechercheduCentreHospitalierdel’UniversitédeMontréal,Montréal,QCH2X0A9,Canada.
+Presentaddress:CellandGeneTherapies,NovartisInstitutesforBioMedicalResearchIncorporated,Cambridge,MA02139,USA.
?Correspondingauthor.E-mail:sar@nih.gov
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Downloaded from http://science.sciencemag.org/ on February 7, 2017
Fig.1.Patient3737–TILharborERBB2IPmutation–specific
CD4+Tcells.(AtoC)Patient3737–TILwerecoculturedwith
dendriticcells(DCs)transfectedwithnothing(Mock),greenfluo-
rescentprotein(GFP)RNA,ortheindicatedTMGconstructencod-
ingthevariousmutationsidentifiedbywhole-exomicsequencing.
(A)“cytometric&”IFN-denotesgenzyme-linkedimmunosorbentspotassayat20hours.analysisgreateratthan24hours.500spotsDataperare1e3gatedcells.on(BliveandCD3+C)Flow-cells
and,for(C),furthergatedonCD4+cells.(D)ACD4+Vb22+clone
wasco-culturedfor6hourswithautologousBcellspulsedover-
nightwithwild-type(wt)ERBB2IP,mutated(mut)anaplasticlymphoma
receptortyrosinekinase(ALK),ormutERBB2IP25–aminoacid–
longpeptides.FlowcytometrywasusedtodetectintracellularIFN-g
productionintheCD4+population.Dataarerepresentativeof
twoclonessharingthesameTCR-Vbsequence.(E)Autologous
open-repertoireperipheralbloodTcellsweretransduced(Td)
withnothing(Mock)ortheTCRderivedfromtheVb22+clone
andthenassessedforreactivityasdescribedin(D).Theendog-
enousVb22+TCRconstantregionswereswappedwithmouseconstantregions,allowingforthedetectionoftheintroducedTCRusingantibodiesagainstthemouseTCRbconstantregion(mTCRb).Plate-boundOKT3wasusedasacontrolinallassays.Alldataarerepresentativeofatleasttwoindependentexperiments.ErrorbarsareSD.
individuallytransfectedintoautologousantigen-tionwasrevertedbacktothewild-typesequence,6/6Vb22+clonestested(tableS4),suggestingthatpresentingcells,followedbyacoculturewithindicating
TILtodeterminewhetheranyoftheprocessedE805GthattheTILspecificallyrecognizedthethemajorityoftheERBB2IPmutation–reactiveERBB2IPmutation(Fig.1C).TheresponseTcellswascomposedofadominantVb22+TcellandpresentedmutatedantigenswererecognizedwasrestrictedbyHLA-DQB1*0601,andthemini-clone.TcellclonesexpressingthisVb22TCRspe-byTIL.Weobservedreactivityof3737-TILtoamalepitopewaslocatedwithinthe13–aminocificallyproducedthecytokineinterferon(IFN)–gmutatedantigenpresentinTMG-1butnotTMG-acidsequenceNSKEETGHLENGN(whereEuponstimulationwiththemutatedERBB2IPpep-2orTMG-3(Fig.1A).Moreover,thereactivityisGG,GH,HK,LL,LN,AS,tide(Fig.1D).Moreover,autologousopenreper-predominatedintheCD4+Tcellpopulation,asSandT,Thr)(fig.S2).toireperipheralbloodTcellsgeneticallymodifieddemonstratedbyup-regulationoftheactivationWenextcharacterizedtheclonalityofthewiththisTCR-Vb22chainmatchedwithitsalphamarkersOX40and4-1BB(Fig.1B).AlthoughmutatedERBB2IP-specificCD4+Tcellsbychain(tableS5)conferredspecificreactivitytosome4-1BBup-regulationwasobservedinthesortingthemafterantigen-specificactivation,themutatedERBB2IPpeptide(Fig.1E),demon-CD4-negative(CD8+)Tcellpopulation,wesortedusingOX40asamarkerofactivation(fig.S3A).stratingthat
thesecellsandfoundnoreactivityagainsttheThesecellswerethenbulk-expandedandclonedE805GthisTCRspecificallyrecognizedtheERBB2IPmutation.
TMG.Todeterminewhichoftheninemutationsbylimitingdilution.Aflowcytometry–basedsur-Thepatientunderwentadoptivetransferof42.4inTMG-1wasbeingrecognizedby3737-TIL,veyoftheTcellreceptor–Vb(TCR-Vb)repertoirebillionTILcontainingCD4+ERBB2IPmutation-wesynthesizednineadditionalTMG-1constructs,demonstratedthatthebulk-expandedpopu-reactiveTcellsfollowedbyfourdosesofinter-eachonecontainingareversionofoneofthemu-lationwas&95%Vb22+andthat10/11clonesleukin(IL)–2toenhanceTcellproliferationandtationsbacktothewild-typesequence.ReactivityassessedwerepurelyVb22+(fig.S3,BandC).function(fig.S4).Flowcytometryanalysisdem-of3737-TILtoTMG-1wasabrogatedonlywhenTCRsequenceanalysisrevealedthesameTCRbonstratedthatabout25%oftheentire3737-theerbb2interactingprotein(ERBB2IP)muta-variable,diversity,joining(V-D-J)sequenceinTILproductadministeredwascomposedof
the6429MAY2014VOL344SCIENCEwww.sciencemag.orgDownloaded from http://science.sciencemag.org/ on February 7, 2017
Fig.2.AdoptivetransferofTILcontainingERBB2IPmutation–reactiveTcells.(A)Flow-cytometricanaly-sisoftheTCR-Vbreper-toireof3737-TIL,gatedonliveCD4+orCD8+Tcells.(B)Patient3737–TILwerecoculturedwithDCstrans-fectedwithTMG-1or
encodingthewtERBB2IPreversion,andflowcytometrywasusedtoassessOX40andVb22expressiononCD4+Tcellsat24hourspost-stimulation.Plate-boundOKT3stimulationwasusedasapositivecontrol.(A)and(B)arerepresentativeofatleasttwoindependentex-periments.(C)IFN-genzyme-linkedimmuno-sorbentassayonpatient3737serumsamplespre–andpost–adoptivecelltransferof3737-TIL.ErrorbarsareSEM.(D)Tumorgrowthcurves
[ResponseEvaluationCriteriainSolidTumorssumofmaximumdiameters]beforeandafterinfusion3737-TIL.Dataareexpressedasachangeinpercentfrompretreatmentbaselineandstratifiedonlung,liver,andtotal
Vb22+,mutation-reactiveTcells(Fig.2,AandB),equatingtotheinfusionofover10billionERBB2IPmutation–specificCD4+Tcells.Ele-vatedlevelsofIFN-gweredetectedinthepa-tient’sserumforthefirst5daysaftercellinfusion(Fig.2C).Althoughthepatienthadclearevi-denceofprogressivediseasebeforethecellinfusion,tumorregressionwasobservedbythe2-monthfollow-up,andalltargetlungandliverlesionscontinuedtoregress,reachingamaximumreductionof30%at7monthspost-treatment(Fig.2D).Thepatientexperienceddiseasestabilizationforabout13monthsaftercellinfusion,afterwhichdiseaseprogressionwasobservedonlyinthelungsbutnotliver.
TodeterminewhethertherewasevidencethattheCD4+ERBB2IPmutation–reactiveTcellsplayedaroleinthediseasestabilization,weeval-uatedtheinvitrophenotypeandfunctionandinvivopersistenceofthesecells.Anumberofpre-clinicalstudies(14–20)andonecasereportinmelanoma(21)havedemonstratedthatThelper1(TH1)cells,throughavarietyofmechanismsincludingthesecretionofthepleiotropiccyto-kinesIFN-gandtumornecrosisfactor(TNF)(22,23),canmediatetumorregression.More-over,CD4+Tcellsthatcansimultaneouslyproducemultipleeffectorcytokines(polyfunc-tionalTcells)havebeencorrelatedwitheffec-tiveantitumorTcellresponses(19,24).WefoundthattheVb22+ERBB2IPmutation–reactiveCD4+TcellswerepolyfunctionalTH1cells,becausestimulationwiththemutatedERBB2IPpep-tideinducedtherobustcoexpressionofIFN-g,TNF,andIL-2(Fig.3A)butlittletonoIL-4orIL-17.Furtherphenotypiccharacterizationre-vealedthatthesecellswerepredominantlyeffectormemoryCD4+Tcellswithcytolyticpotential(fig.S5,AandB).
Fig.3.FunctionalphenotypeandpersistenceofERBB2IPmutation–specificCD4+Tcells.(A)Patient3737–TILwerecoculturedfor6hourswithautologousBcellspulsedovernightwithwtERBB2IP,mutALK,ormutERBB2IP25–aminoacid–longpeptides.FlowcytometrywasusedtoassessexpressionofVb22andtodetectintracellularproductionofIL-2,TNF,andIFN-gintheCD4+population.PiechartsdisplaythepercentageofVb22+cellsthatexpressedtheindicatednumberofcytokines.Dataarerepresentativeofatleastthreeindependentexperiments.(B)TCR-Vbdeepsequencingof3737-TILandbloodandtumorsofpatient3737atvarioustimespre–andpost–adoptivecelltransferwith3737-TIL.DatashowthefrequencyofthetwoERBB2IPmutation–specificTCRb-CDR3clonotypes.?,notdetected.
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