2023
Cutting Edge: IL-21 and Tissue-Specific Signals Instruct Tbet+CD11c+ B Cell Development following Viral Infection.
Song W, Sanchez G, Mayer D, Blackburn H, Chernova I, Flavell R, Weinstein J, Craft J. Cutting Edge: IL-21 and Tissue-Specific Signals Instruct Tbet+CD11c+ B Cell Development following Viral Infection. The Journal Of Immunology 2023, 210: 1861-1865. PMID: 37133336, PMCID: PMC10247523, DOI: 10.4049/jimmunol.2300027.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsCell DifferentiationInterleukinsLymphocytic ChoriomeningitisMiceMice, Inbred C57BLMice, KnockoutConceptsAge-associated B cellsIL-21Acute lymphocytic choriomeningitis virus infectionB cellsLymphocytic choriomeningitis virus infectionB cell activationHumoral immunityLymphoid organsVirus infectionMouse modelViral infectionB cell developmentCell activationLymphotoxin αVivo generationTissue-specific signalsInfectionDe novo generationOrgan contributionIFNTissue microenvironmentCell developmentLiverPivotal contributorStage-specific rolesAP-1–independent NFAT signaling maintains follicular T cell function in infection and autoimmunity
Seth A, Yokokura Y, Choi J, Shyer J, Vidyarthi A, Craft J. AP-1–independent NFAT signaling maintains follicular T cell function in infection and autoimmunity. Journal Of Experimental Medicine 2023, 220: e20211110. PMID: 36820828, PMCID: PMC9998660, DOI: 10.1084/jem.20211110.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAutoimmunityB-LymphocytesCell DifferentiationGerminal CenterMiceT-Lymphocytes, Helper-InducerTranscription Factor AP-1ConceptsTfh cellsT cellsFollicular helper T cellsLupus-prone miceT cell subsetsTfh cell developmentHelper T cellsHumoral immune responseT cell functionGerminal center B cellsT cell statesRenal injuryAutoantibody productionCell subsetsPrimary T cellsImmune responseB cellsPharmacologic inhibitionTherapeutic insightsCell functionGenetic disruptionNFATCell developmentCellsGene expression
2022
Spatial profiling of chromatin accessibility in mouse and human tissues
Deng Y, Bartosovic M, Ma S, Zhang D, Kukanja P, Xiao Y, Su G, Liu Y, Qin X, Rosoklija GB, Dwork AJ, Mann JJ, Xu ML, Halene S, Craft JE, Leong KW, Boldrini M, Castelo-Branco G, Fan R. Spatial profiling of chromatin accessibility in mouse and human tissues. Nature 2022, 609: 375-383. PMID: 35978191, PMCID: PMC9452302, DOI: 10.1038/s41586-022-05094-1.Peer-Reviewed Original ResearchConceptsChromatin accessibilityATAC-seqSpecific epigenetic landscapesChromatin accessibility profilingCell fate decisionsEpigenetic informationEpigenetic landscapeGenome scaleFate decisionsAccessible genomeCell identityEpigenetic underpinningsNext-generation sequencingGene regulatorsCell statesMouse embryosSpatial biologySpatial transcriptomicsCell typesCellular levelImmune cell typesDistinct organizationHuman tissuesProfilingSpatial profilingDevelopment of Tbet- and CD11c-expressing B cells in a viral infection requires T follicular helper cells outside of germinal centers
Song W, Antao OQ, Condiff E, Sanchez GM, Chernova I, Zembrzuski K, Steach H, Rubtsova K, Angeletti D, Lemenze A, Laidlaw BJ, Craft J, Weinstein JS. Development of Tbet- and CD11c-expressing B cells in a viral infection requires T follicular helper cells outside of germinal centers. Immunity 2022, 55: 290-307.e5. PMID: 35090581, PMCID: PMC8965751, DOI: 10.1016/j.immuni.2022.01.002.Peer-Reviewed Original ResearchConceptsFollicular helper cellsB cellsGC B cellsHelper cellsMemory subsetsRobust recall responsesB cell subsetsGerminal center formationB cell generationAcute infectionCell subsetsRecall responsesTh1 cellsProximal deliveryCD11cGerminal centersIntegrin LFA-1Viral infectionAntibody productionVLA-4Splenic retentionLFA-1TbetBCL6 expressionInfection
2021
CD4+ T cells that help B cells – a proposal for uniform nomenclature
Eisenbarth SC, Baumjohann D, Craft J, Fazilleau N, Ma CS, Tangye SG, Vinuesa CG, Linterman MA. CD4+ T cells that help B cells – a proposal for uniform nomenclature. Trends In Immunology 2021, 42: 658-669. PMID: 34244056, PMCID: PMC8324560, DOI: 10.1016/j.it.2021.06.003.Peer-Reviewed Original ResearchMeSH KeywordsB-LymphocytesCell DifferentiationGerminal CenterImmunity, HumoralLymphocyte ActivationT-Lymphocytes, Helper-InducerConceptsTfh-like cellsB cellsT cellsFollicular helper cellsAntigen-primed B cellsSecondary lymphoid tissuesTranscription factor Bcl6B cell differentiationHelper cellsHumoral immunityLymphoid tissueChemokine receptorsAnatomical sitesImmune challengeDistinct subsetsDifferent isotypesCD4TfhCellular plasticityCellsCell differentiationUniform nomenclatureCytokinesImmunityAntibodies
2019
Distinct modes of mitochondrial metabolism uncouple T cell differentiation and function
Bailis W, Shyer JA, Zhao J, Canaveras JCG, Al Khazal FJ, Qu R, Steach HR, Bielecki P, Khan O, Jackson R, Kluger Y, Maher LJ, Rabinowitz J, Craft J, Flavell RA. Distinct modes of mitochondrial metabolism uncouple T cell differentiation and function. Nature 2019, 571: 403-407. PMID: 31217581, PMCID: PMC6939459, DOI: 10.1038/s41586-019-1311-3.Peer-Reviewed Original ResearchConceptsMitochondrial citrate exportTerminal effector functionsMalate-aspartate shuttleCitrate exportHistone acetylationCell differentiationComplex ICellular biochemical compositionT cell differentiationSuccinate dehydrogenaseT cell activationExpression of genesElectron transport chainTricarboxylic acid cycleT cell receptor ligationAnabolic programTranscriptional remodellingTranscriptional programmingEpigenetic remodellingSignal transductionCell activationMetabolic reprogrammingCell statesDistinct modesEffector functionsT follicular helper cell heterogeneity: Time, space, and function
Song W, Craft J. T follicular helper cell heterogeneity: Time, space, and function. Immunological Reviews 2019, 288: 85-96. PMID: 30874350, PMCID: PMC6422039, DOI: 10.1111/imr.12740.Peer-Reviewed Original Research
2017
STAT4 and T-bet control follicular helper T cell development in viral infections
Weinstein JS, Laidlaw BJ, Lu Y, Wang JK, Schulz VP, Li N, Herman EI, Kaech SM, Gallagher PG, Craft J. STAT4 and T-bet control follicular helper T cell development in viral infections. Journal Of Experimental Medicine 2017, 215: 337-355. PMID: 29212666, PMCID: PMC5748849, DOI: 10.1084/jem.20170457.Peer-Reviewed Original ResearchConceptsIL-21Tfh cellsT-betViral infectionFollicular helper T cellsHelper T cell developmentAcute viral infectionIFN-γ productionHelper T cellsGerminal center B cell survivalB cell survivalT cell developmentIL-4Viral challengeIL-9T cellsImmunoglobulin isotypesIFNSoluble factorsGC responseInfectionGC reactionSTAT4BCL6Cell survivalInterleukin-10 from CD4+ follicular regulatory T cells promotes the germinal center response
Laidlaw BJ, Lu Y, Amezquita RA, Weinstein JS, Vander Heiden JA, Gupta NT, Kleinstein SH, Kaech SM, Craft J. Interleukin-10 from CD4+ follicular regulatory T cells promotes the germinal center response. Science Immunology 2017, 2 PMID: 29054998, PMCID: PMC5846620, DOI: 10.1126/sciimmunol.aan4767.Peer-Reviewed Original ResearchConceptsFollicular regulatory T cellsRegulatory T cellsIL-10Lymphocytic choriomeningitis virusT cellsB cellsInterleukin-10GC responseCell-derived IL-10Follicular helper T cellsHelper T cellsB cell responsesGerminal center responseGerminal center developmentActivated B cellsBox protein 1GC B cellsAcute infectionCenter responseCell responsesImportant mediatorNuclear translocationGC reactionProtein 1Forkhead box protein 1
2016
TFH cells progressively differentiate to regulate the germinal center response
Weinstein JS, Herman EI, Lainez B, Licona-Limón P, Esplugues E, Flavell R, Craft J. TFH cells progressively differentiate to regulate the germinal center response. Nature Immunology 2016, 17: 1197-1205. PMID: 27573866, PMCID: PMC5030190, DOI: 10.1038/ni.3554.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAntibody AffinityB-LymphocytesCD4 AntigensCell CommunicationCell DifferentiationCells, CulturedGene Expression RegulationGerminal CenterHumansInterleukin-4InterleukinsMiceMice, Inbred C57BLMice, Mutant StrainsMutationNippostrongylusPositive Regulatory Domain I-Binding Factor 1Strongylida InfectionsT-Lymphocytes, Helper-InducerTranscription Factors
2015
IL-21 Promotes Pulmonary Fibrosis through the Induction of Profibrotic CD8+ T Cells
Brodeur TY, Robidoux TE, Weinstein JS, Craft J, Swain SL, Marshak-Rothstein A. IL-21 Promotes Pulmonary Fibrosis through the Induction of Profibrotic CD8+ T Cells. The Journal Of Immunology 2015, 195: 5251-5260. PMID: 26519529, PMCID: PMC4655158, DOI: 10.4049/jimmunol.1500777.Peer-Reviewed Original ResearchLocal Triggering of the ICOS Coreceptor by CD11c+ Myeloid Cells Drives Organ Inflammation in Lupus
Teichmann LL, Cullen JL, Kashgarian M, Dong C, Craft J, Shlomchik MJ. Local Triggering of the ICOS Coreceptor by CD11c+ Myeloid Cells Drives Organ Inflammation in Lupus. Immunity 2015, 42: 552-565. PMID: 25786178, PMCID: PMC4456685, DOI: 10.1016/j.immuni.2015.02.015.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsApoptosisAutoantibodiesCD11c AntigenCell DifferentiationFemaleGene Expression RegulationHumansInducible T-Cell Co-Stimulator LigandInducible T-Cell Co-Stimulator ProteinKidneyLungLupus NephritisMice, TransgenicPhosphatidylinositol 3-KinasesProto-Oncogene Proteins c-aktSignal TransductionT-Lymphocytes, Helper-InducerConceptsInducible T-cell costimulatorOrgan inflammationICOS ligandFollicular helper cell differentiationLupus-prone MRLT-cell costimulatorHelper cell differentiationLupus pathologyLung inflammationAutoantibody formationAutoantibody productionMurine lupusInflamed organsLymphoid tissueT cellsB cellsPathogenic relevanceInflammationLupusPI3K-AktSelective ablationCell differentiationNonredundant rolePotent promoterCellsThe transforming growth factor beta signaling pathway is critical for the formation of CD4 T follicular helper cells and isotype-switched antibody responses in the lung mucosa
Marshall HD, Ray JP, Laidlaw BJ, Zhang N, Gawande D, Staron MM, Craft J, Kaech SM. The transforming growth factor beta signaling pathway is critical for the formation of CD4 T follicular helper cells and isotype-switched antibody responses in the lung mucosa. ELife 2015, 4: e04851. PMID: 25569154, PMCID: PMC4337607, DOI: 10.7554/elife.04851.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAntibody FormationB-LymphocytesCell DifferentiationGene Expression ProfilingGerminal CenterImmunoglobulin Class SwitchingLungMiceMucous MembraneOrthomyxoviridaeOrthomyxoviridae InfectionsSignal TransductionSpecies SpecificityT-Lymphocytes, Helper-InducerTOR Serine-Threonine KinasesTransforming Growth Factor betaConceptsCD4 T cellsFollicular helper cellsTfh cellsAntibody responseT cellsHelper cellsViral infectionCD4 T follicular helper cellsVirus-specific CD4 T cellsIL-2 receptor α chainT Follicular Helper CellsRespiratory viral infectionsAcute viral infectionGrowth factor betaGerminal center reactionReceptor α chainInhibition of mTORIL-2 signalingLung mucosaTfh differentiationHumoral responseRapamycin (mTOR) activationTGF-βRFactor betaCenter reaction
2014
Transcription Factor STAT3 and Type I Interferons Are Corepressive Insulators for Differentiation of Follicular Helper and T Helper 1 Cells
Ray JP, Marshall HD, Laidlaw BJ, Staron MM, Kaech SM, Craft J. Transcription Factor STAT3 and Type I Interferons Are Corepressive Insulators for Differentiation of Follicular Helper and T Helper 1 Cells. Immunity 2014, 40: 367-377. PMID: 24631156, PMCID: PMC3992517, DOI: 10.1016/j.immuni.2014.02.005.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAntibodies, ViralAntibody SpecificityB-LymphocytesCD4 AntigensCD4-Positive T-LymphocytesCell DifferentiationGene Expression ProfilingGene Expression RegulationGerminal CenterImmunoglobulin Class SwitchingInterferon Type ILymphocytic ChoriomeningitisLymphocytic choriomeningitis virusMiceMice, KnockoutSignal TransductionSTAT1 Transcription FactorSTAT3 Transcription FactorT-Lymphocytes, Helper-InducerTranscriptomeConceptsTfh cellsType I interferonI interferonViral infectionFollicular helper T cellsT helper 1 cellsAntigen-specific antibody productionGC B cell phenotypeHigh affinity antibody-secreting cellsTfh cell differentiationHelper T cellsB cell memoryLymphocytic choriomeningitis virusB-cell phenotypeAntibody-secreting cellsGerminal center B cellsEffector phenotypeReceptor blockadeAcute infectionFollicular helperIFN-inducible genesT cellsTranscription factor STAT3B cellsAntibody production
2013
CD301b+ Dermal Dendritic Cells Drive T Helper 2 Cell-Mediated Immunity
Kumamoto Y, Linehan M, Weinstein JS, Laidlaw BJ, Craft JE, Iwasaki A. CD301b+ Dermal Dendritic Cells Drive T Helper 2 Cell-Mediated Immunity. Immunity 2013, 39: 733-743. PMID: 24076051, PMCID: PMC3819035, DOI: 10.1016/j.immuni.2013.08.029.Peer-Reviewed Original ResearchConceptsDermal dendritic cellsDendritic cellsDermal DCsTh2 cellsT cellsT helper 2 cellsT helper responsesInterleukin-4 productionExpression of CD69Th2 cell developmentDC depletionLymph nodesTh2 immunityHelper responsesSubcutaneous immunizationNippostrongylus brasiliensisKey mediatorTransient depletionCell developmentImmunityOvalbuminDepletion approachCellsParticular subsetCD301b
2012
T cells that promote B‐Cell maturation in systemic autoimmunity
Weinstein JS, Hernandez SG, Craft J. T cells that promote B‐Cell maturation in systemic autoimmunity. Immunological Reviews 2012, 247: 160-171. PMID: 22500839, PMCID: PMC3334351, DOI: 10.1111/j.1600-065x.2012.01122.x.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAutoimmunityB-LymphocytesCell DifferentiationGene Expression RegulationGerminal CenterHumansModels, BiologicalT-Lymphocytes, Helper-InducerConceptsSystemic autoimmunityT cellsB cell maturationExtrafollicular fociGerminal centersB cellsTfh cellsImmune responseFollicular helper T cellsT cell-dependent immune responsesEnd-organ injuryB cell folliclesSystemic autoimmune diseaseTfh cell developmentHuman Tfh cellsSelf-reactive B cellsT helper cellsHelper T cellsSecondary lymphoid organsNormal immune responseT cell helpPlasma cell formationPathogenic autoantibodiesLymph nodesAutoimmune diseasesIL-21 Receptor Is Required for the Systemic Accumulation of Activated B and T Lymphocytes in MRL/MpJ-Faslpr/lpr/J Mice
Rankin AL, Guay H, Herber D, Bertino SA, Duzanski TA, Carrier Y, Keegan S, Senices M, Stedman N, Ryan M, Bloom L, Medley Q, Collins M, Nickerson-Nutter C, Craft J, Young D, Dunussi-Joannopoulos K. IL-21 Receptor Is Required for the Systemic Accumulation of Activated B and T Lymphocytes in MRL/MpJ-Faslpr/lpr/J Mice. The Journal Of Immunology 2012, 188: 1656-1667. PMID: 22231702, PMCID: PMC3618484, DOI: 10.4049/jimmunol.1003871.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAutoantibodiesAutoimmunityB-LymphocytesCD4-Positive T-LymphocytesCell DifferentiationInterferon-gammaInterleukinsLupus Erythematosus, SystemicLymphatic DiseasesLymphocyte ActivationMiceMice, Inbred MRL lprMice, KnockoutReceptors, Interleukin-21SkinSplenomegalyT-Lymphocyte SubsetsT-Lymphocytes, Helper-InducerConceptsT cell effector subsetsIL-21Effector subsetsIL-21RT cellsHelper cellsSpontaneous germinal center formationIL-21-dependent mannerIL-21 receptorMRL/MpJPlasma cell accumulationGerminal center formationTh cell differentiationSignificant reductionAutoantibody titersAutoantibody productionCytokines IFNImmune activationSystemic autoimmunityJ miceDisease manifestationsT lymphocytesPleiotropic cytokineB cellsDisease pathogenesis
2011
An Interleukin-21- Interleukin-10-STAT3 Pathway Is Critical for Functional Maturation of Memory CD8+ T Cells
Cui W, Liu Y, Weinstein JS, Craft J, Kaech SM. An Interleukin-21- Interleukin-10-STAT3 Pathway Is Critical for Functional Maturation of Memory CD8+ T Cells. Immunity 2011, 35: 792-805. PMID: 22118527, PMCID: PMC3431922, DOI: 10.1016/j.immuni.2011.09.017.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsCD8-Positive T-LymphocytesCell DifferentiationGene Expression Regulation, DevelopmentalImmunologic MemoryInterleukin-10InterleukinsMiceMice, KnockoutPositive Regulatory Domain I-Binding Factor 1Proto-Oncogene Proteins c-bcl-6Signal TransductionSTAT3 Transcription FactorSuppressor of Cytokine Signaling 3 ProteinSuppressor of Cytokine Signaling ProteinsT-Box Domain ProteinsTranscription FactorsConceptsMemory T cellsT cellsBCL-6Protective memory T cellsCentral memory T cellsSTAT3 pathwayAcute LCMV infectionExpression of EomesLong-term immunityMemory precursor cellsSTAT3-SOCS3 pathwayMemory cell developmentCell developmentT cell developmentMemory CD8IL-21LCMV infectionIL-12Interleukin-10Inflammatory cytokinesFunctional maturationSOCS3 expressionBlimp-1Precursor cellsSTAT3
2010
In Vivo Regulation of Bcl6 and T Follicular Helper Cell Development
Poholek AC, Hansen K, Hernandez SG, Eto D, Chandele A, Weinstein JS, Dong X, Odegard JM, Kaech SM, Dent AL, Crotty S, Craft J. In Vivo Regulation of Bcl6 and T Follicular Helper Cell Development. The Journal Of Immunology 2010, 185: 313-326. PMID: 20519643, PMCID: PMC2891136, DOI: 10.4049/jimmunol.0904023.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsCell CommunicationCell DifferentiationCricetinaeDNA-Binding ProteinsDown-RegulationFemaleImmunophenotypingLymphocyte CooperationMembrane GlycoproteinsMiceMice, Inbred BALB CMice, Inbred C57BLMice, KnockoutMice, TransgenicProto-Oncogene Proteins c-bcl-6SpleenT-Lymphocyte SubsetsT-Lymphocytes, Helper-InducerUp-RegulationConceptsPD-1 upregulationIL-21IL-6B cellsFollicular helper T cellsFollicular helper cell developmentDeath receptor-1Helper T cellsCytokines IL-6B cell interactionsB cell maturationTranscriptional repressor BCL6Vivo regulationCell developmentP-selectin glycoprotein ligand-1New surface markersT cellsGerminal centersInitial upregulationReceptor 1CXCR5BCL6 upregulationCell maturationSurface markersBCL6 expression
2009
Thymic self-reactivity selects natural interleukin 17–producing T cells that can regulate peripheral inflammation
Marks BR, Nowyhed HN, Choi JY, Poholek AC, Odegard JM, Flavell RA, Craft J. Thymic self-reactivity selects natural interleukin 17–producing T cells that can regulate peripheral inflammation. Nature Immunology 2009, 10: 1125-1132. PMID: 19734905, PMCID: PMC2751862, DOI: 10.1038/ni.1783.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsAutoantigensCD4-Positive T-LymphocytesCell DifferentiationEnzyme-Linked Immunosorbent AssayFlow CytometryInflammationIntegrin alpha4beta1Interleukin-17Interleukin-23Interleukin-6InterleukinsMiceMice, TransgenicNuclear Receptor Subfamily 1, Group F, Member 3Polymerase Chain ReactionReceptors, CCR6Receptors, Retinoic AcidReceptors, Thyroid HormoneThymus GlandT-Lymphocyte SubsetsTransforming Growth Factor beta