2023
T follicular helper cells in cancer, tertiary lymphoid structures, and beyond
Cui C, Craft J, Joshi N. T follicular helper cells in cancer, tertiary lymphoid structures, and beyond. Seminars In Immunology 2023, 69: 101797. PMID: 37343412, DOI: 10.1016/j.smim.2023.101797.Peer-Reviewed Reviews, Practice Guidelines, Standards, and Consensus StatementsConceptsTumor-associated tertiary lymphoid structuresFollicular helper cellsCD8 T cellsTertiary lymphoid structuresSecondary lymphoid organsT cellsHelper cellsLymphoid structuresImmune cellsB cellsCD4 T follicular helper cellsT Follicular Helper CellsTumor-infiltrating immune cellsCurrent immunotherapy regimensCheckpoint blockade immunotherapyCD4 T cellsImmune cell componentsLimited response rateFunctional immune cellsNovel therapeutic targetPotential therapeutic benefitT cell-B cell interactionsBlockade immunotherapyImmunotherapy regimensLymphoid organsCutting 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 ResearchConceptsAge-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 ResearchConceptsTfh 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 expressionThe ion transporter Na+-K+-ATPase enables pathological B cell survival in the kidney microenvironment of lupus nephritis
Chernova I, Song W, Steach H, Hafez O, Al Souz J, Chen P, Chandra N, Cantley L, Veselits M, Clark M, Craft J. The ion transporter Na+-K+-ATPase enables pathological B cell survival in the kidney microenvironment of lupus nephritis. Science Advances 2023, 9: eadf8156. PMID: 36724234, PMCID: PMC9891690, DOI: 10.1126/sciadv.adf8156.Peer-Reviewed Original ResearchConceptsB cellsAutoimmune diseasesAmelioration of proteinuriaLupus nephritis biopsiesB cell infiltrationSodium-potassium adenosine triphosphataseB cell survivalPotassium adenosine triphosphataseLupus nephritisCell infiltrationKidney microenvironmentTissue injuryTherapeutic targetPharmacological inhibitionElevated sodium concentrationLupusHostile microenvironmentHigh expressionKidneySodium concentrationGenetic knockoutCell survivalDiseaseCellsAdenosine triphosphatase
2022
Development 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
Neoantigen-driven B cell and CD4 T follicular helper cell collaboration promotes anti-tumor CD8 T cell responses
Cui C, Wang J, Fagerberg E, Chen PM, Connolly KA, Damo M, Cheung JF, Mao T, Askari AS, Chen S, Fitzgerald B, Foster GG, Eisenbarth SC, Zhao H, Craft J, Joshi NS. Neoantigen-driven B cell and CD4 T follicular helper cell collaboration promotes anti-tumor CD8 T cell responses. Cell 2021, 184: 6101-6118.e13. PMID: 34852236, PMCID: PMC8671355, DOI: 10.1016/j.cell.2021.11.007.Peer-Reviewed Original ResearchConceptsCD8 TB cellsTfh cellsLung adenocarcinomaTfh-B cell interactionsTumor-specific B cellsFollicular helper cellsAnti-tumor immunityB cell signaturesCell effector functionsGerminal center formationGC B cellsCD4 THelper cellsTumor controlTumor neoantigensEffector functionsCell collaborationCell responsesCell signatureTumor cellsSignature correlatesNeoantigensCell functionCD4Intrarenal B Cells in Systemic Lupus Erythematosus Upregulate Na+-K+-ATPase to Facilitate Survival in a High-Sodium Environment
Chernova I, Craft J. Intrarenal B Cells in Systemic Lupus Erythematosus Upregulate Na+-K+-ATPase to Facilitate Survival in a High-Sodium Environment. Journal Of The American Society Of Nephrology 2021, 32: 452-452. DOI: 10.1681/asn.20213210s1452a.Peer-Reviewed Original ResearchCD4+ 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 ResearchConceptsTfh-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 nomenclatureCytokinesImmunityAntibodiesNeoantigen driven B cell and CD4+ T follicular helper cell collaboration promotes robust anti-tumor CD8+ T cell responses
Cui C, Joshi N, Craft J. Neoantigen driven B cell and CD4+ T follicular helper cell collaboration promotes robust anti-tumor CD8+ T cell responses. The Journal Of Immunology 2021, 206: 57.01-57.01. DOI: 10.4049/jimmunol.206.supp.57.01.Peer-Reviewed Original ResearchT cell responsesAnti-tumor CD8Tfh cellsB cellsCell responsesIL-21Cell collaborationProtective anti-tumor responsesTfh-B cell interactionsTumor-specific B cellsGC B cell responsesTumor-specific CD4Anti-tumor immunityFavorable clinical outcomeAnti-tumor responseIL-21 receptorB cell responsesLung adenocarcinoma patientsAnalysis of survivalT cell-B cell interactionsGerminal center formationCell interactionsGC B cellsAbstract CD4Effector CD8
2019
Impaired ATM activation in B cells is associated with bone resorption in rheumatoid arthritis
Mensah KA, Chen JW, Schickel JN, Isnardi I, Yamakawa N, Vega-Loza A, Anolik JH, Gatti RA, Gelfand EW, Montgomery RR, Horowitz MC, Craft JE, Meffre E. Impaired ATM activation in B cells is associated with bone resorption in rheumatoid arthritis. Science Translational Medicine 2019, 11 PMID: 31748230, PMCID: PMC7167286, DOI: 10.1126/scitranslmed.aaw4626.Peer-Reviewed Original ResearchConceptsRheumatoid arthritisB cellsHealthy donor controlsGroup of patientsHumanized mouse modelImmature B cellsGene segment usageErosive diseaseRA pathophysiologyBone erosionBone lossBone resorptionHigh prevalenceRANKL productionBone densityMouse modelReceptor activatorBone marrowPatientsDonor controlsCD21Segment usageArthritisElevated frequencyAtaxia telangiectasiaIdentification of a T follicular helper cell subset that drives anaphylactic IgE
Gowthaman U, Chen JS, Zhang B, Flynn WF, Lu Y, Song W, Joseph J, Gertie JA, Xu L, Collet MA, Grassmann JDS, Simoneau T, Chiang D, Berin MC, Craft JE, Weinstein JS, Williams A, Eisenbarth SC. Identification of a T follicular helper cell subset that drives anaphylactic IgE. Science 2019, 365 PMID: 31371561, PMCID: PMC6901029, DOI: 10.1126/science.aaw6433.Peer-Reviewed Original ResearchConceptsInterleukin-4B cellsFollicular Helper Cell SubsetsLow-affinity IgEFollicular helper cellsAllergen-specific IgEHelper cell subsetsIsotypes of antibodiesAlternative therapeutic targetsTranscription factor Bcl6Anaphylactic IgECytokine profileIgE productionCell subsetsHelper cellsImmunoglobulin ETherapeutic targetIgEAnaphylaxisAllergensCellular mechanismsRare populationCellsMiceGATA3T 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
2018
Human Extrafollicular CD4+ Th Cells Help Memory B Cells Produce Igs.
Kim ST, Choi JY, Lainez B, Schulz VP, Karas DE, Baum ED, Setlur J, Gallagher PG, Craft J. Human Extrafollicular CD4+ Th Cells Help Memory B Cells Produce Igs. The Journal Of Immunology 2018, 201: 1359-1372. PMID: 30030323, PMCID: PMC6112860, DOI: 10.4049/jimmunol.1701217.Peer-Reviewed Original ResearchConceptsMemory B cellsHumoral recall responsesB cell folliclesT cell subsetsB cellsTfh cellsCell subsetsRecall responsesT cellsInhibitory receptor PD-1Follicular helper T cellsGerminal center B-cell maturationIL-21 secretionChemokine receptor expressionReceptor PD-1Helper T cellsT cell zonesPrimary immune responseChemokine receptor CXCR5Transcription factor Bcl6B cell maturationTonsillar CD4IL-10IL-21PD-1
2017
Interleukin-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
2015
Progressive differentiation of follicular B helper T cells regulates the germinal center response (IRC11P.430)
Herman E, Weinstein J, Lainez B, Licona-Limón P, Esplugues E, Flavell R, Craft J. Progressive differentiation of follicular B helper T cells regulates the germinal center response (IRC11P.430). The Journal Of Immunology 2015, 194: 197.12-197.12. DOI: 10.4049/jimmunol.194.supp.197.12.Peer-Reviewed Original ResearchFollicular B helper T cellsHelper T cellsTfh cellsGerminal centersT cellsIL-21IL-4Thymus-dependent humoral immune responsesIL-21 mRNAB cell folliclesTfh cell differentiationCD4 T cellsHumoral immune responseSecondary lymphoid organsEffective antibody responseGerminal center responseAntibody-secreting cellsActivated B cellsTranscription factor Bcl6B cell maturationAntibody responseLymphoid organsImmune responseB cellsCenter responseLocal 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 promoterCells
2014
Dynamic signaling by T follicular helper cells during germinal center B cell selection
Shulman Z, Gitlin AD, Weinstein JS, Lainez B, Esplugues E, Flavell RA, Craft JE, Nussenzweig MC. Dynamic signaling by T follicular helper cells during germinal center B cell selection. Science 2014, 345: 1058-1062. PMID: 25170154, PMCID: PMC4519234, DOI: 10.1126/science.1257861.Peer-Reviewed Original ResearchConceptsFollicular helper cellsB cellsGC B cellsHelper cellsGerminal centersAntibody-producing B cellsCytokine interleukin-4B cell selectionGerminal center B cell selectionInterleukin-4Transient elevationMajor histocompatibilitySustained increaseFree calciumClonal expansionCognate peptideIntravital imagingCell migrationCellsIntracellularCell selectionHigh levelsHistocompatibilityPPARγ Negatively Regulates T Cell Activation to Prevent Follicular Helper T Cells and Germinal Center Formation
Park HJ, Kim DH, Choi JY, Kim WJ, Kim JY, Senejani AG, Hwang SS, Kim LK, Tobiasova Z, Lee GR, Craft J, Bothwell AL, Choi JM. PPARγ Negatively Regulates T Cell Activation to Prevent Follicular Helper T Cells and Germinal Center Formation. PLOS ONE 2014, 9: e99127. PMID: 24921943, PMCID: PMC4055678, DOI: 10.1371/journal.pone.0099127.Peer-Reviewed Original ResearchConceptsFollicular helper T cellsHelper T cellsT cellsGerminal center reactionTfh cellsSheep red blood cell immunizationRed blood cell immunizationCenter reactionPeroxisome proliferator-activated receptor gammaIL-21 expressionProliferator-activated receptor gammaWild-type T cellsType T cellsGerminal center formationGerminal center B cellsT cell activationCell immunizationAutoantibody productionGlomerular inflammationSignature cytokinesAdaptive immunityGerminal centersGlucose metabolismNF-κBB cellsAberant expansion of CXCR5+ memory CD4 T cells in SLE patients (HUM7P.307)
Choi J, Kim S, Kang I, Craft J. Aberant expansion of CXCR5+ memory CD4 T cells in SLE patients (HUM7P.307). The Journal Of Immunology 2014, 192: 184.16-184.16. DOI: 10.4049/jimmunol.192.supp.184.16.Peer-Reviewed Original ResearchCD4 T cellsSLE patientsT cellsTfh cellsB cellsB collaborationB cell helper functionFollicular helper T cellsMemory CD4 T cellsMemory Tfh cellsTh17-like subsetsAnti-nuclear antibodiesHelper T cellsB cell responsesHuman lupus patientsSecondary lymphoid organsMemory B cellsAutoreactive B cellsSuch cellsDistinct Th1Autoantibody titersDisease activityLupus patientsIL-21Lymphoid organsTranscription factor Ascl2 limits Tfh cell differentiation and function (IRC8P.493)
Bertino S, Dong X, Laidlaw B, Craft J. Transcription factor Ascl2 limits Tfh cell differentiation and function (IRC8P.493). The Journal Of Immunology 2014, 192: 190.21-190.21. DOI: 10.4049/jimmunol.192.supp.190.21.Peer-Reviewed Original ResearchTfh cellsIL-4T cellsAntibody productionCD4 T cell compartmentFollicular helper T cellsTfh cell subsetsTfh cell differentiationTfh cell developmentIL-4 productionT cell compartmentHelper T cellsLarge germinal centersGerminal center responseSecretion of cytokinesGerminal center formationB cell maturationGC B cellsIL-21Germinal centersB cellsCenter responseCell maturationConditional deletionMice