2025
Evidence for coopetition at the maternal-fetal interface shaping placental invasion.
Afzal J, Suhail Y, Du W, Liu Y, Ramasamy R, Liu Z, Goyal R, Novin A, Suhail S, Maziarz J, Wali K, Robson P, Wagner G, Kshitiz. Evidence for coopetition at the maternal-fetal interface shaping placental invasion. Proceedings Of The National Academy Of Sciences Of The United States Of America 2025, 122: e2323038122. PMID: 40906814, PMCID: PMC12435225, DOI: 10.1073/pnas.2323038122.Peer-Reviewed Original ResearchConceptsMaternal-fetal interfaceExtravillous trophoblast cellsEndometrial stromal fibroblastsInvasive placentationInvasive extravillous trophoblast cellsExpression of suppressor of cytokine signaling 3IL-11 signalingResistance to invasionTrophoblast stem cellsSuppressor of cytokine signaling 3AP-1 signalingMaternal-fetal conflictMaternal stromaCytokine signaling 3Placental invasionFetal genesCytotrophoblast cellsDecidual transformationEvolutionary interestTrophoblast cellsStromal fibroblastsHemochorial placentationEutherian mammalsIL-11Paracrine signalingIn utero human intestine contains maternally derived bacterial metabolites
Wang W, Gu W, Schweitzer R, Koren O, Khatib S, Tseng G, Konnikova L. In utero human intestine contains maternally derived bacterial metabolites. Microbiome 2025, 13: 116. PMID: 40329366, PMCID: PMC12054239, DOI: 10.1186/s40168-025-02110-0.Peer-Reviewed Original ResearchConceptsImmune systemFetal intestineAryl hydrocarbon receptorFetal immune systemMucosal immune regulationIntestinal immune systemIntestinal metabolomic profilesIntestinal tissueSecondary bile acidsHuman intestinal tissueMaternal deciduaFetal meconiumPlacental villiMicrobial metabolitesPlacental tissueMetabolomic profilesDecidua samplesMeconium samplesImmune regulationAdaptive immunityMicrobial encountersGastrointestinal tractShort-chain fatty acidsDisease prevention strategiesMeconium
2023
Maternal CXCR4 deletion results in placental defects and pregnancy loss mediated by immune dysregulation
Lyu F, Burzynski C, Fang Y, Tal A, Chen A, Kisa J, Agrawal K, Kluger Y, Taylor H, Tal R. Maternal CXCR4 deletion results in placental defects and pregnancy loss mediated by immune dysregulation. JCI Insight 2023, 8: e172216. PMID: 37815869, PMCID: PMC10721256, DOI: 10.1172/jci.insight.172216.Peer-Reviewed Original ResearchConceptsCXCR4-deficient micePlacental vascular developmentNK cellsCxcr4 deletionNormal placental vascular developmentPlacental developmentNK cell dysfunctionNK cell expressionNK cell infiltrationNK cell functionRole of CXCR4Cell functionMaternal-fetal interfaceImmune cell functionEarly placental developmentWt CXCR4Immune dysregulationVascular developmentGiant cell layerImmune toleranceCXCR4 expressionPeripheral bloodPregnancy failureCell infiltrationPregnancy lossDecidualization dampens toll-like receptor mediated inflammatory responses in human endometrial stromal cells by upregulating IκBα
Tong M, Scott J, Whirledge S, Abrahams V. Decidualization dampens toll-like receptor mediated inflammatory responses in human endometrial stromal cells by upregulating IκBα. Journal Of Reproductive Immunology 2023, 159: 103988. PMID: 37451159, PMCID: PMC10530124, DOI: 10.1016/j.jri.2023.103988.Peer-Reviewed Original ResearchConceptsEndometrial stromal cellsInflammatory responseStromal cellsHuman endometrial stromal cellsToll-like receptor signalingSex hormone levelsMenstrual cycle stageToll-like receptorsImmune response changesViral double-stranded RNAHuman EnSCsEndometrial responseProinflammatory cytokinesSuccessful pregnancyMenstrual cycleHuman endometriumHormone levelsMajor cell typesImmune responseNFκB p65Viral infectionDecidualizationBacterial lipopolysaccharideReceptor signalingBacterial components
2022
Renalase and its receptor, PMCA4b, are expressed in the placenta throughout the human gestation
Wang M, Silva T, Toothaker JM, McCourt BT, Shugrue C, Desir G, Gorelick F, Konnikova L. Renalase and its receptor, PMCA4b, are expressed in the placenta throughout the human gestation. Scientific Reports 2022, 12: 4953. PMID: 35322081, PMCID: PMC8943056, DOI: 10.1038/s41598-022-08817-6.Peer-Reviewed Original ResearchConceptsPlacental tissuePlacental villiHofbauer cellsPlacental developmentEndogenous productionAnti-inflammatory milieuPotential roleHuman placental tissueFull-term placentaPlacental factorsFetal interfaceDecidual samplesPlacental functionChorionic plateImmunoreactive cellsPlacental samplesHuman gestationRenalaseBulk RNA sequencingHuman placentaPlacentaQuantification of immunohistochemistryProtein levelsTrophoblastTransmission of nutrientsUterine HOXA11 antisense long non-coding RNA prevents decidualization: A new pathway-regulating pregnancy
Taylor HS. Uterine HOXA11 antisense long non-coding RNA prevents decidualization: A new pathway-regulating pregnancy. Molecular Therapy 2022, 30: 1357-1358. PMID: 35320748, PMCID: PMC9077366, DOI: 10.1016/j.ymthe.2022.03.007.Peer-Reviewed Original ResearchConceptsPregnancy
2021
Single-cell analysis of prostaglandin E2-induced human decidual cell in vitro differentiation: a minimal ancestral deciduogenic signal†
Stadtmauer DJ, Wagner G. Single-cell analysis of prostaglandin E2-induced human decidual cell in vitro differentiation: a minimal ancestral deciduogenic signal†. Biology Of Reproduction 2021, 106: 155-172. PMID: 34591094, PMCID: PMC8757638, DOI: 10.1093/biolre/ioab183.Peer-Reviewed Original ResearchMeSH KeywordsCell DifferentiationCell Line, TransformedCells, CulturedCyclic AMPCyclic AMP-Dependent Protein KinasesDeciduaDinoprostoneEndometriumFemaleFibroblastsGene ExpressionGenome-Wide Association StudyHumansMedroxyprogesterone AcetatePregnancyReceptors, Prostaglandin E, EP2 SubtypeSequence Analysis, RNASingle-Cell AnalysisConceptsPlacental mammalsCore gene regulatory networkCyclic AMP/protein kinase A (cAMP/PKA) pathwayProtein kinase A (PKA) pathwaySenescence-associated genesProgesterone-dependent activationGenome-wide studiesSingle-cell transcriptomicsGene regulatory networksProgesterone-dependent inductionMembrane-permeable cAMPKinase A PathwaySingle-cell analysisUse of PGE2Outgroup taxaCellular statesRegulatory networksPKA axisGene expressionDecidual genesPKA activationPGE2 receptor 2Progestin-dependent inductionA PathwayAdenylyl cyclase activation
2020
Zika Virus-Infected Decidual Cells Elicit a Gestational Age-Dependent Innate Immune Response and Exaggerate Trophoblast Zika Permissiveness: Implication for Vertical Transmission.
Guzeloglu-Kayisli O, Guo X, Tang Z, Semerci N, Ozmen A, Larsen K, Mutluay D, Guller S, Schatz F, Kayisli UA, Lockwood CJ. Zika Virus-Infected Decidual Cells Elicit a Gestational Age-Dependent Innate Immune Response and Exaggerate Trophoblast Zika Permissiveness: Implication for Vertical Transmission. The Journal Of Immunology 2020, 205: 3083-3094. PMID: 33139490, DOI: 10.4049/jimmunol.2000713.Peer-Reviewed Original ResearchConceptsHuman decidual cellsDecidual cellsZika virusViral attachment factorsTerm decidual stromal cellsVertical transmissionDecidual cell supernatantsTerm decidual cellsInnate immune response genesInnate immune responsivenessExact pathogenic mechanismDecidual stromal cellsHuman first trimesterInnate immune responseSevere fetal defectsImmune response genesFetal sequelaeGestational ageFirst trimesterPlacental transmissionZIKV infectionCytotrophoblast culturesImmune responsivenessZika infectionLate pregnancyEvolution of Embryo Implantation Was Enabled by the Origin of Decidual Stromal Cells in Eutherian Mammals
Chavan AR, Griffith OW, Stadtmauer D, Maziarz J, Pavlicev M, Fishman R, Koren L, Romero R, Wagner GP. Evolution of Embryo Implantation Was Enabled by the Origin of Decidual Stromal Cells in Eutherian Mammals. Molecular Biology And Evolution 2020, 38: 1060-1074. PMID: 33185661, PMCID: PMC7947829, DOI: 10.1093/molbev/msaa274.Peer-Reviewed Original ResearchConceptsEutherian mammalsEutherian lineagesDecidual stromal cellsNovel cell typesStromal cellsInflammatory responseStem lineageEutherian pregnancyCommon ancestorEvolutionary mechanismsExtended gestationMost marsupialsEmbryo attachmentEmbryo implantationMarsupialsLineagesCell typesMammalsMechanistic understandingEutheriansHelper T cellsFetal-maternal interfaceMammalian pregnancyMaternal tissuesNeutrophil recruitmentTranscriptomic responses to hypoxia in endometrial and decidual stromal cells
Rytkönen KT, Heinosalo T, Mahmoudian M, Ma X, Perheentupa A, Elo LL, Poutanen M, Wagner G. Transcriptomic responses to hypoxia in endometrial and decidual stromal cells. Reproduction 2020, 160: 39-51. PMID: 32272449, DOI: 10.1530/rep-19-0615.Peer-Reviewed Original ResearchConceptsDecidual stromal cellsEndometrial stromal fibroblastsEndometriotic stromal cellsStromal cellsInflammatory transcription factorsEpithelial-mesenchymal transitionExpression of JunDCEBP transcription factorsCell typesHealthy endometriumEndometriosis lesionsProgesterone receptorDecidualization processUterine endometriumStromal fibroblastsMesenchymal transitionProgesterone signalingEndometriumHypoxiaHypoxia pathwayTranscription factorsHuman reproductive successDistinct transcriptional statesExpression of genesJun/FosImmune Cells in the Placental Villi Contribute to Intra-amniotic Inflammation
Toothaker JM, Presicce P, Cappelletti M, Stras SF, McCourt CC, Chougnet CA, Kallapur SG, Konnikova L. Immune Cells in the Placental Villi Contribute to Intra-amniotic Inflammation. Frontiers In Immunology 2020, 11: 866. PMID: 32528468, PMCID: PMC7256198, DOI: 10.3389/fimmu.2020.00866.Peer-Reviewed Original ResearchConceptsFetal-maternal interfaceIntra-amniotic inflammationImmune cellsVillous placentaT cellsPlacental villiNatural killerTumor necrosis factor alphaAbundance of neutrophilsIA LPS exposureCD8 T cellsMemory T cellsAntigen-presenting cellsRhesus macaque modelNecrosis factor alphaDistinct immunological profilePotential therapeutic targetTNFα blockadeLPS exposureSignificant morbidityMacaque modelProinflammatory cytokinesImmunological profileFactor alphaImmunological responseHuman Chorionic Gonadotropin modulates CXCL10 Expression through Histone Methylation in human decidua
Silasi M, You Y, Simpson S, Kaislasuo J, Pal L, Guller S, Peng G, Ramhorst R, Grasso E, Etemad S, Durosier S, Aldo P, Mor G. Human Chorionic Gonadotropin modulates CXCL10 Expression through Histone Methylation in human decidua. Scientific Reports 2020, 10: 5785. PMID: 32238853, PMCID: PMC7113245, DOI: 10.1038/s41598-020-62593-9.Peer-Reviewed Original ResearchConceptsHuman chorionic gonadotropinCXCL10 expressionChorionic gonadotropinPotent immune-modulatory effectsImmune system undergoesImmune modulatory effectsEndometrial stromal cellsImmune cell recruitmentMaternal-fetal interfaceImmune regulatory functionsProcess of implantationCD8 cellsCytokine profilePregnancy progressesFetal interfaceDecidual samplesImmune populationsImmune factorsHuman deciduaT cellsDecidual cellsCell recruitmentModulatory effectsEarly hormoneStromal cellsDistinctive phenotypes and functions of innate lymphoid cells in human decidua during early pregnancy
Huhn O, Ivarsson M, Gardner L, Hollinshead M, Stinchcombe J, Chen P, Shreeve N, Chazara O, Farrell L, Theorell J, Ghadially H, Parham P, Griffiths G, Horowitz A, Moffett A, Sharkey A, Colucci F. Distinctive phenotypes and functions of innate lymphoid cells in human decidua during early pregnancy. Nature Communications 2020, 11: 381. PMID: 31959757, PMCID: PMC6971012, DOI: 10.1038/s41467-019-14123-z.Peer-Reviewed Original ResearchConceptsDecidual innate lymphoid cellsKiller-cell immunoglobulin-like receptorsFetal extravillous trophoblastsInnate lymphoid cellsExtravillous trophoblastNK cellsEarly pregnancyLymphoid cellsFunction of innate lymphoid cellsPeripheral blood NK cellsHLA class I ligandsMaternal dendritic cellsBlood NK cellsDecidual NK cellsGranzyme B levelsProliferating NK cellsImmunoglobulin-like receptorsClass I ligandsIncreased chemokine productionDecidual NKHuman deciduaMaternal cellsDendritic cellsPlacental developmentChemokine production
2019
Adult bone marrow progenitors become decidual cells and contribute to embryo implantation and pregnancy
Tal R, Shaikh S, Pallavi P, Tal A, López-Giráldez F, Lyu F, Fang YY, Chinchanikar S, Liu Y, Kliman HJ, Alderman M, Pluchino N, Kayani J, Mamillapalli R, Krause DS, Taylor HS. Adult bone marrow progenitors become decidual cells and contribute to embryo implantation and pregnancy. PLOS Biology 2019, 17: e3000421. PMID: 31513564, PMCID: PMC6742226, DOI: 10.1371/journal.pbio.3000421.Peer-Reviewed Original ResearchConceptsBM transplantsDecidual cellsPregnancy lossMesenchymal stem cellsAdult bone marrow progenitorsDecidualization-related genesBone marrow progenitorsAdult bone marrowWT donorsPhysiologic contributionSuccessful pregnancyBMDC recruitmentStromal expansionImmune cellsEndometrial cellsDeficient miceUterine expressionUterine tissueDecidual stromaPregnancyBone marrowNonhematopoietic cellsBMDCsHemochorial placentaMarrow progenitors
2018
The mammalian decidual cell evolved from a cellular stress response
Erkenbrack EM, Maziarz JD, Griffith OW, Liang C, Chavan AR, Nnamani MC, Wagner GP. The mammalian decidual cell evolved from a cellular stress response. PLOS Biology 2018, 16: e2005594. PMID: 30142145, PMCID: PMC6108454, DOI: 10.1371/journal.pbio.2005594.Peer-Reviewed Original ResearchConceptsCellular stress responseNovel cell typesStress responseEndometrial stromal fibroblastsCell typesCell type diversityDecidual stromal cellsCore regulatory genesOxidative stress responseDecidual cell typesEvolutionary noveltyPrecursor cell typesEffector genesRegulatory genesEutherian mammalsTranscription factorsOpossum Monodelphis domesticaOrganismal structureType diversityMolecular mechanismsAnimal speciesMonodelphis domesticaGenesStromal cellsSpecies
2017
Single-cell transcriptomics of the human placenta: inferring the cell communication network of the maternal-fetal interface
Pavličev M, Wagner GP, Chavan AR, Owens K, Maziarz J, Dunn-Fletcher C, Kallapur SG, Muglia L, Jones H. Single-cell transcriptomics of the human placenta: inferring the cell communication network of the maternal-fetal interface. Genome Research 2017, 27: 349-361. PMID: 28174237, PMCID: PMC5340963, DOI: 10.1101/gr.207597.116.Peer-Reviewed Original ResearchConceptsSingle-cell transcriptomicsG protein-coupled receptorsCell communication networksGene expression profilesReceptor-ligand pairsCell type identificationOrganismal functionInteraction hubTrophoblast cellsGene expressionExpression profilesEndometrial stromal fibroblastsSpecific expressionCell typesInteractomeTranscriptomicsRich resourceCell interactionsPlacental trophoblast cellsDecidual cellsImmune signalsStromal cellsGrowth factorStromal fibroblastsEndometrial stromal cells
2016
What was the ancestral function of decidual stromal cells? A model for the evolution of eutherian pregnancy
Chavan AR, Bhullar BA, Wagner GP. What was the ancestral function of decidual stromal cells? A model for the evolution of eutherian pregnancy. Placenta 2016, 40: 40-51. PMID: 27016782, DOI: 10.1016/j.placenta.2016.02.012.Peer-Reviewed Original ResearchConceptsEutherian mammalsDecidual stromal cellsAncestral functionEutherian cladesMajor lineagesStem lineageEutherian pregnancyStromal cellsEutherian speciesStem eutheriansExtended gestationMammalsEutheriansLineagesMaintenance of pregnancyCellsInvasive placentationLaurasiatheriaCladeEuarchontogliresAfrotheriaFetal-maternal interfaceXenarthraDecidual cellsSpecies
2015
Uterine glucocorticoid receptors are critical for fertility in mice through control of embryo implantation and decidualization
Whirledge SD, Oakley RH, Myers PH, Lydon JP, DeMayo F, Cidlowski JA. Uterine glucocorticoid receptors are critical for fertility in mice through control of embryo implantation and decidualization. Proceedings Of The National Academy Of Sciences Of The United States Of America 2015, 112: 15166-15171. PMID: 26598666, PMCID: PMC4679013, DOI: 10.1073/pnas.1508056112.Peer-Reviewed Original ResearchConceptsGlucocorticoid receptorPresence of GRExaggerated inflammatory responseSex steroid receptorsImmune cell recruitmentStromal cell decidualizationFemale reproductive tractAdrenal axisKO miceInflammatory responseUterine physiologyUterine biologyEndocrine organMouse uterusBlastocyst implantationGlucocorticoid signalingMouse modelCell recruitmentEmbryo implantationImmunomodulatory functionsKnockout miceGR signalingSteroid receptorsReproductive tractDecidualizationMechanisms of chorioamnionitis‐associated preterm birth: interleukin‐1β inhibits progesterone receptor expression in decidual cells
Guzeloglu-Kayisli O, Kayisli UA, Semerci N, Basar M, Buchwalder LF, Buhimschi CS, Buhimschi IA, Arcuri F, Larsen K, Huang JS, Schatz F, Lockwood CJ. Mechanisms of chorioamnionitis‐associated preterm birth: interleukin‐1β inhibits progesterone receptor expression in decidual cells. The Journal Of Pathology 2015, 237: 423-434. PMID: 26175191, DOI: 10.1002/path.4589.Peer-Reviewed Original ResearchConceptsProgesterone receptor expressionPreterm birthDecidual cellsPR expressionIL-1βDC culturesReceptor expressionPR levelsIL-1β suppressionLower PR levelsFunctional progesterone withdrawalCOX-2 expressionRelease of cytokinesIL-1β treatmentDecidual prostaglandin productionP38 MAPK signaling cascadesCervical ripeningProgesterone withdrawalCOX inhibitorsImmunohistochemical stainingChorioamnionitisFetal membrane ruptureNF-kBProstaglandin productionPGF2α productionEnhanced Human Decidual Cell–Expressed FKBP51 May Promote Labor-Related Functional Progesterone Withdrawal
Schatz F, Guzeloglu-Kayisli O, Basar M, Buchwalder LF, Ocak N, Guzel E, Guller S, Semerci N, Kayisli UA, Lockwood CJ. Enhanced Human Decidual Cell–Expressed FKBP51 May Promote Labor-Related Functional Progesterone Withdrawal. American Journal Of Pathology 2015, 185: 2402-2411. PMID: 26207680, DOI: 10.1016/j.ajpath.2015.05.014.Peer-Reviewed Original ResearchConceptsTerm decidual cellsDecidual cellsProgesterone receptorP4 withdrawalInterstitial trophoblastMedroxyprogesterone acetateDC culturesHuman term labourLow progesterone receptorsGlucocorticoid receptor expressionFunctional progesterone withdrawalCultured decidual cellsHuman decidual cellsPlasma progesterone levelsThird trimester trophoblastDC nucleiDecidual sectionsOrganon 2058Plasma P4 levelsTerm laborPR expressionProgesterone withdrawalProgesterone levelsReceptor expressionGR expression
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