2024
MIF and CD74 as Emerging Biomarkers for Immune Checkpoint Blockade Therapy
Fey R, Nichols R, Tran T, Vandenbark A, Kulkarni R. MIF and CD74 as Emerging Biomarkers for Immune Checkpoint Blockade Therapy. Cancers 2024, 16: 1773. PMID: 38730725, PMCID: PMC11082995, DOI: 10.3390/cancers16091773.Peer-Reviewed Original ResearchImmune-related adverse eventsImmune-related adverse events developmentResponse to ICB therapyImmune checkpoint blockade therapyImmune checkpoint blockadePredictive biomarkersICB therapyCheckpoint blockade therapySerum MIF levelsBlockade therapyCheckpoint blockadeMIF levelsMalignant melanomaTreatment resistanceSolid tumorsAdverse eventsAutoimmune diseasesContext of cancerPrognostic biomarkerCancer progressionCognate receptor CD74Receptor CD74TherapyCD74Cancer
2021
MIF but not MIF-2 recruits inflammatory macrophages in an experimental polymicrobial sepsis model
Tilstam PV, Schulte W, Holowka T, Kim BS, Nouws J, Sauler M, Piecychna M, Pantouris G, Lolis E, Leng L, Bernhagen J, Fingerle-Rowson G, Bucala R. MIF but not MIF-2 recruits inflammatory macrophages in an experimental polymicrobial sepsis model. Journal Of Clinical Investigation 2021, 131: e127171. PMID: 34850744, PMCID: PMC8631602, DOI: 10.1172/jci127171.Peer-Reviewed Original ResearchMeSH KeywordsAnimalsCytokinesDisease Models, AnimalFemaleFlow CytometryGene Expression ProfilingInflammationIntramolecular OxidoreductasesLeukocyte CountMacrophage Migration-Inhibitory FactorsMacrophagesMacrophages, PeritonealMaleMiceMice, Inbred C57BLMice, TransgenicPeritoneal LavagePhenotypeProtein BindingRNA-SeqSepsisSignal TransductionConceptsMacrophage migration inhibitory factorSmall peritoneal macrophagesLarge peritoneal macrophagesPolymicrobial sepsisPeritoneal macrophagesMIF receptor CD74MIF promoter polymorphismsMIF-2Migration inhibitory factorPolymicrobial sepsis modelMIF deficiencyAdoptive transferSeptic shockSurvival benefitInfectious insultsMIF antibodyExcessive inflammationInflammatory cytokinesReceptor CD74Sepsis modelProtective effectPeritoneal cavityDifferent infectionsPromoter polymorphismInflammatory macrophagesMacrophage migration inhibitory factor exerts pro‐proliferative and anti‐apoptotic effects via CD74 in murine hepatocellular carcinoma
Wirtz TH, Saal A, Bergmann I, Fischer P, Heinrichs D, Brandt EF, Koenen MT, Djudjaj S, Schneider KM, Boor P, Bucala R, Weiskirchen R, Bernhagen J, Trautwein C, Berres M. Macrophage migration inhibitory factor exerts pro‐proliferative and anti‐apoptotic effects via CD74 in murine hepatocellular carcinoma. British Journal Of Pharmacology 2021, 178: 4452-4467. PMID: 34250589, DOI: 10.1111/bph.15622.Peer-Reviewed Original ResearchConceptsMacrophage migration inhibitory factorMIF/CD74 axisMigration inhibitory factorHepatocellular carcinomaRole of MIFInhibitory factorReduced tumor burdenAnti-CD74 antibodiesNew pharmacological therapiesDEN/CClDifferent inflammatory diseasesChemokine-like proteinTherapy-induced cell deathMurine hepatocellular carcinomaPro-tumorigenic roleAnti-apoptotic effectsCarbon tetrachloride modelTherapy-induced apoptosisMIF knockoutMIF receptorPharmacological therapyTumor burdenControl miceReceptor CD74CD74 antibodyIntravesical CD74 and CXCR4, macrophage migration inhibitory factor (MIF) receptors, mediate bladder pain
Ye S, Ma F, Mahmood DFD, Meyer-Siegler KL, Menard RE, Hunt DE, Leng L, Bucala R, Vera PL. Intravesical CD74 and CXCR4, macrophage migration inhibitory factor (MIF) receptors, mediate bladder pain. PLOS ONE 2021, 16: e0255975. PMID: 34424927, PMCID: PMC8382170, DOI: 10.1371/journal.pone.0255975.Peer-Reviewed Original ResearchConceptsMacrophage migration inhibitory factorHigh mobility group box 1Bladder painMIF receptorHMGB1 releaseBladder hyperalgesiaMobility group box 1MIF receptor CD74Migration inhibitory factorGroup box 1Primary urothelial cellsInhibitory factor receptorWarrants further investigationCD74 receptorReceptor CD74Micturition parametersReceptor antagonistReceptor 4Box 1PainInhibitory factorHyperalgesiaCD74Urothelial cellsNovel target
2020
Balance between macrophage migration inhibitory factor and sCD74 predicts outcome in patients with acute decompensation of cirrhosis
Wirtz TH, Reuken PA, Jansen C, Fischer P, Bergmann I, Backhaus C, Emontzpohl C, Reißing J, Brandt EF, Koenen MT, Schneider KM, Schierwagen R, Brol MJ, Chang J, Zimmermann HW, Köse-Vogel N, Eggermann T, Kurth I, Stoppe C, Bucala R, Bernhagen J, Praktiknjo M, Stallmach A, Trautwein C, Trebicka J, Bruns T, Berres ML. Balance between macrophage migration inhibitory factor and sCD74 predicts outcome in patients with acute decompensation of cirrhosis. JHEP Reports 2020, 3: 100221. PMID: 33659891, PMCID: PMC7890204, DOI: 10.1016/j.jhepr.2020.100221.Peer-Reviewed Original ResearchMacrophage migration inhibitory factorConcentrations of MIFMigration inhibitory factorTransplant-free survivalAcute decompensationInhibitory factorSystemic inflammationReceptor CD74Serum concentrationsHigher macrophage migration inhibitory factorTransjugular intrahepatic portosystemic shunt insertionInflammatory cytokine macrophage migration inhibitory factorCytokine macrophage migration inhibitory factorHigher MIF concentrationsRight atrial bloodWorsening of ascitesChronic liver failureLiver function parametersShort-term mortalityHigher serum levelsMIF promoter polymorphismsRisk of deathPortal venous bloodInnate immune responseClassical scoring systems
2019
Selective Recruitment of Lethal Pro-inflammatory Macrophages in Sepsis by MIF but not D-DT (MIF-2)
Tilstam P, Schulte W, Holowka T, Kim B, Piecychna M, Pantouris G, Lolis E, Leng L, Bernhagen J, Bucala R. Selective Recruitment of Lethal Pro-inflammatory Macrophages in Sepsis by MIF but not D-DT (MIF-2). The Journal Of Immunology 2019, 202: 51.9-51.9. DOI: 10.4049/jimmunol.202.supp.51.9.Peer-Reviewed Original ResearchMacrophage migration inhibitory factorSmall peritoneal macrophagesLarge peritoneal macrophagesPolymicrobial sepsisPeritoneal macrophagesMIF receptor CD74MIF promoter polymorphismsMigration inhibitory factorPro-inflammatory macrophagesSelective roleDate interventionsMIF deficiencyAdoptive transferSurvival benefitInfectious insultsMIF antibodyInflammatory cytokinesPeritoneal inflammationReceptor CD74Inflammatory pathwaysLeading causeSepsis lethalityInflammatory responseAbstract SepsisGlobal incidenceMIF and MIF2 have distinct but synergistic roles in CIA pathogenesis
Doherty E, Tilstam P, Bucala R. MIF and MIF2 have distinct but synergistic roles in CIA pathogenesis. The Journal Of Immunology 2019, 202: 180.13-180.13. DOI: 10.4049/jimmunol.202.supp.180.13.Peer-Reviewed Original ResearchMacrophage migration inhibitory factorRheumatoid arthritisT cellsCIA inductionCollagen-induced arthritis (CIA) mouse modelSevere erosive rheumatoid arthritisEffector memory T cellsCytokine macrophage migration inhibitory factorRelapsing autoimmune diseaseErosive rheumatoid arthritisProgressive joint destructionT cell infiltrationMemory T cellsAbstract Rheumatoid arthritisArthritis mouse modelSecondary lymphoid organsMigration inhibitory factorCIA pathogenesisHigh expression alleleJoint inflammationJoint destructionLymph nodesWT miceAutoimmune diseasesReceptor CD74
2017
Parasite MIF Orthologs
Holowka T, Bucala R. Parasite MIF Orthologs. Progress In Inflammation Research 2017, 221-239. DOI: 10.1007/978-3-319-52354-5_14.Peer-Reviewed Original ResearchMacrophage migration inhibitory factorHuman macrophage migration inhibitory factorImmune responseMIF receptor CD74Adaptive immune responsesMigration inhibitory factorPro-inflammatory activityAnimal model studiesInflammatory cytokinesReceptor CD74IL-8Novel treatmentsSmall molecule inhibitorsTherapeutic interventionsInhibitory factorInfectious diseasesMacrophage migrationHost macrophagesMIF orthologsPathogenic impactMolecule inhibitorsTautomerase activitySignal transduction pathwaysTransduction pathwaysNematode parasites
2016
D‐dopachrome tautomerase in adipose tissue inflammation and wound repair
Kim B, Tilstam PV, Hwang SS, Simons D, Schulte W, Leng L, Sauler M, Ganse B, Averdunk L, Kopp R, Stoppe C, Bernhagen J, Pallua N, Bucala R. D‐dopachrome tautomerase in adipose tissue inflammation and wound repair. Journal Of Cellular And Molecular Medicine 2016, 21: 35-45. PMID: 27605340, PMCID: PMC5192814, DOI: 10.1111/jcmm.12936.Peer-Reviewed Original ResearchMeSH KeywordsAdipose TissueAnimalsAntigens, Differentiation, B-LymphocyteCell MovementCell ProliferationDown-RegulationFibroblastsHistocompatibility Antigens Class IIHumansInflammationIntramolecular OxidoreductasesMacrophagesMaleMiceMice, Inbred C57BLObesityReceptors, CXCR4Receptors, Interleukin-8BUp-RegulationWound HealingConceptsAdipose tissue inflammationSubcutaneous adipose tissueD-DTAdipose tissueTissue inflammationWound repairEpididymal fat padsDopachrome tautomeraseReceptor CXCR2MIF antibodyInflammatory cellsReceptor CD74Healthy donorsReceptor expressionFat padMRNA expressionProtein levelsWound healingFibroblast survivalMIFInflammationHealingTissueCell migrationFibroblast wound healingMacrophage Migration Inhibitory Factor-CXCR4 Receptor Interactions*
Rajasekaran D, Gröning S, Schmitz C, Zierow S, Drucker N, Bakou M, Kohl K, Mertens A, Lue H, Weber C, Xiao A, Luker G, Kapurniotu A, Lolis E, Bernhagen J. Macrophage Migration Inhibitory Factor-CXCR4 Receptor Interactions*. Journal Of Biological Chemistry 2016, 291: 15881-15895. PMID: 27226569, PMCID: PMC4957068, DOI: 10.1074/jbc.m116.717751.Peer-Reviewed Original ResearchConceptsMacrophage migration inhibitory factorChemokine receptorsCXCR4 receptorRole of MIFMIF's biological activityMigration inhibitory factorChemokine receptor interactionsFunctional CXCR4 receptorsClassical chemokine receptorsChemokine-like activityPartial allosteric agonistRegions of CXCR4Inflammatory cytokinesReceptor CD74Leukocyte recruitmentAllosteric agonistInhibitory factorCXCR4Non-cognate interactionsReceptorsPharmacological reagentsReceptor interactionArray analysisGenetic strainsCritical biological responsesThe clinical significance of the MIF homolog d-dopachrome tautomerase (MIF-2) and its circulating receptor (sCD74) in burn
Kim BS, Stoppe C, Grieb G, Leng L, Sauler M, Assis D, Simons D, Boecker AH, Schulte W, Piecychna M, Hager S, Bernhagen J, Pallua N, Bucala R. The clinical significance of the MIF homolog d-dopachrome tautomerase (MIF-2) and its circulating receptor (sCD74) in burn. Burns 2016, 42: 1265-1276. PMID: 27209369, PMCID: PMC5010466, DOI: 10.1016/j.burns.2016.02.005.Peer-Reviewed Original ResearchConceptsTotal body surface areaMacrophage migration inhibitory factorSerum levelsClinical significanceCytokine macrophage migration inhibitory factorEarly post-burn periodPrediction of sepsisBody surface areaMigration inhibitory factorPost-burn periodBurn severity indexDopachrome tautomeraseClinical outcomesBurn patientsReceptor CD74Healthy controlsBurn injuryEarly predictorMember DPatientsPotential biomarkersCD74Inhibitory factorSoluble CD74Severity Index
2015
Endothelial CD74 mediates macrophage migration inhibitory factor protection in hyperoxic lung injury
Sauler M, Zhang Y, Min J, Leng L, Shan P, Roberts S, Jorgensen WL, Bucala R, Lee PJ. Endothelial CD74 mediates macrophage migration inhibitory factor protection in hyperoxic lung injury. The FASEB Journal 2015, 29: 1940-1949. PMID: 25609432, PMCID: PMC4415022, DOI: 10.1096/fj.14-260299.Peer-Reviewed Original ResearchConceptsMacrophage migration inhibitory factorLung endothelial cellsMurine lung endothelial cellsLung injuryEndothelial cellsProtective effectExogenous MIFCD74 deficient miceCD74-dependent mannerHours of hyperoxiaMIF receptor CD74Acute lung injuryHyperoxic lung injuryBronchoalveolar lavage proteinMigration inhibitory factorBronchoalveolar proteinMIF deficiencyMedian survivalEndothelial injuryWT miceAcute oxidative stressReceptor CD74Lavage proteinReceptor antagonistReceptor inhibitors
2014
Crystallographic and Receptor Binding Characterization of Plasmodium falciparum Macrophage Migration Inhibitory Factor Complexed to Two Potent Inhibitors
Pantouris G, Rajasekaran D, Garcia AB, Ruiz VG, Leng L, Jorgensen WL, Bucala R, Lolis EJ. Crystallographic and Receptor Binding Characterization of Plasmodium falciparum Macrophage Migration Inhibitory Factor Complexed to Two Potent Inhibitors. Journal Of Medicinal Chemistry 2014, 57: 8652-8656. PMID: 25268646, PMCID: PMC4207548, DOI: 10.1021/jm501168q.Peer-Reviewed Original ResearchMacrophage migration inhibitory factor deficiency in chronic obstructive pulmonary disease
Sauler M, Leng L, Trentalange M, Haslip M, Shan P, Piecychna M, Zhang Y, Andrews N, Mannam P, Allore H, Fried T, Bucala R, Lee PJ. Macrophage migration inhibitory factor deficiency in chronic obstructive pulmonary disease. American Journal Of Physiology - Lung Cellular And Molecular Physiology 2014, 306: l487-l496. PMID: 24441872, PMCID: PMC3949087, DOI: 10.1152/ajplung.00284.2013.Peer-Reviewed Original ResearchMeSH KeywordsAdolescentAdultAge FactorsAgedAged, 80 and overAnimalsApoptosisCellular SenescenceCyclin-Dependent Kinase Inhibitor p16Cyclin-Dependent Kinase Inhibitor p21EmphysemaFemaleHumansIntramolecular OxidoreductasesLungMacrophage Migration-Inhibitory FactorsMaleMiceMice, Inbred C57BLMice, KnockoutMiddle AgedNicotianaPulmonary Disease, Chronic ObstructiveReceptors, ImmunologicSmokeSmokingTumor Suppressor Protein p53Young AdultConceptsChronic obstructive pulmonary diseaseMacrophage migration inhibitory factorPathogenesis of COPDDevelopment of COPDMIF receptor CD74Obstructive pulmonary diseasePulmonary diseaseWT miceReceptor CD74Role of MIFMacrophage migration inhibitory factor deficiencyMigration inhibitory factorNormal alveolar structureMo of ageWild-type controlsMIF concentrationsFormer smokersLung volumePlasma concentrationsSpontaneous emphysemaFactor deficiencyCigarette smokePleiotropic cytokineInhibitory factorAlveolar structures
2010
Optimization of N-benzyl-benzoxazol-2-ones as receptor antagonists of macrophage migration inhibitory factor (MIF)
Hare AA, Leng L, Gandavadi S, Du X, Cournia Z, Bucala R, Jorgensen WL. Optimization of N-benzyl-benzoxazol-2-ones as receptor antagonists of macrophage migration inhibitory factor (MIF). Bioorganic & Medicinal Chemistry Letters 2010, 20: 5811-5814. PMID: 20728358, PMCID: PMC2939296, DOI: 10.1016/j.bmcl.2010.07.129.Peer-Reviewed Original ResearchConceptsMacrophage migration inhibitory factorCytokine macrophage migration inhibitory factorMigration inhibitory factorHuman synovial fibroblastsReceptor CD74Receptor antagonistSynovial fibroblastsInhibitory factorAdditional studiesERK1/2 phosphorylationCell proliferationTautomerase activityAntagonistPotent inhibitorBinding assaysInhibitorsAssaysInflammationCD74
2007
Structural and Functional Characterization of a Secreted Hookworm Macrophage Migration Inhibitory Factor (MIF) That Interacts with the Human MIF Receptor CD74*
Cho Y, Jones BF, Vermeire JJ, Leng L, DiFedele L, Harrison LM, Xiong H, Kwong YK, Chen Y, Bucala R, Lolis E, Cappello M. Structural and Functional Characterization of a Secreted Hookworm Macrophage Migration Inhibitory Factor (MIF) That Interacts with the Human MIF Receptor CD74*. Journal Of Biological Chemistry 2007, 282: 23447-23456. PMID: 17567581, PMCID: PMC3707627, DOI: 10.1074/jbc.m702950200.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceAncylostomaAnimalsAntigens, Differentiation, B-LymphocyteCricetinaeCytokinesHistocompatibility Antigens Class IIHumansIntestinal MucosaMacrophage Migration-Inhibitory FactorsMesocricetusMolecular Sequence DataProtein BindingRabbitsRecombinant ProteinsSequence Homology, Amino AcidConceptsMacrophage migration inhibitory factorMIF receptor CD74Migration inhibitory factorReceptor CD74Inhibitory factorHost immune responseHuman macrophage migration inhibitory factorMIF proteinHookworm Ancylostoma ceylanicumImmune responseDisease pathogenesisHuman cytokinesMacrophage migrationAncylostoma ceylanicumMajor causeWorm survivalParasite survivalISO-1Significant differencesTautomerase activityHookworm proteinsCytokinesCD74HookwormRelative bioactivity
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