Characterization of murine amniotic fluid B cells in normal pregnancy and in preterm birth

in Reproduction

Correspondence should be addressed to F Jensen; Email: fjensen@unaj.edu.ar
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The amniotic fluid provides mechanical protection and immune defense against pathogens to the fetus. Indeed, components of the innate and adaptive immunity, including B cells, have been described in the amniotic fluid. However, limited information concerning phenotype and functionality of amniotic fluid B cells is available. Hence, we aimed to perform a full phenotypical and functional characterization of amniotic fluid B cells in normal pregnancy and in a mouse model of preterm birth. Phenotypic analysis depicted the presence of two populations of amniotic fluid B cells: an immature population, resembling B1 progenitor cells and a more mature population. Further isolation and in vitro co-culture with a bone marrow stroma cell line demonstrated the capacity of the immature B cells to mature. This was further supported by spontaneous production of IgM, a feature of the B1 B cell sub-population. An additional in vitro stimulation with lipopolysaccharide induced the activation of amniotic fluid B cells as well as the production of pro and anti-inflammatory cytokines. Furthermore, amniotic fluid B cells were expanded in the acute phase of LPS-induced preterm birth. Overall our data add new insight not only on the phenotype and developmental stage of the amniotic fluid B1 B cells but especially on their functionality. This provides important information for a better understanding of their role within the amniotic fluid as immunological protective barrier, especially with regard to intraamniotic infection and preterm birth.

 

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  • Arenas-HernandezMRomeroRXuYPanaitescuBGarcia-FloresVMillerDAhnHDoneBHassanSSHsuCD et al. 2019 Effector and activated T cells induce preterm labor and birth that is prevented by treatment with progesterone. Journal of Immunology 25852608. (https://doi.org/10.4049/jimmunol.1801350)

    • Search Google Scholar
    • Export Citation
  • BaumgarthN 2011 The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nature Reviews: Immunology 3446. (https://doi.org/10.1038/nri2901)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • BerlandRWortisHH 2002 Origins and functions of B-1 cells with notes on the role of CD5. Annual Review of Immunology 253300. (https://doi.org/10.1146/annurev.immunol.20.100301.064833)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • DavisLEMcLarenLCStewartJAJamesCGLevineMDSkipperBJ 1983 Immunological and microbiological studies of midtrimester amniotic fluid. Gynecologic and Obstetric Investigation 261268. (https://doi.org/10.1159/000299275)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • GalaskRPSnyderIS 1970 Antimicrobial factors in amniotic fluid. American Journal of Obstetrics and Gynecology 5965. (https://doi.org/10.1016/0002-9378(70)90126-2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gomez-LopezNRomeroRArenas-HernandezMAhnHPanaitescuBVadillo-OrtegaFSanchez-TorresCSalisburyKSHassanSS 2016 In vivo T-cell activation by a monoclonal αCD3ε antibody induces preterm labor and birth. American Journal of Reproductive Immunology 386390. (https://doi.org/10.1111/aji.12562)

    • Search Google Scholar
    • Export Citation
  • Gomez-LopezNRomeroRArenas-HernandezMSchwenkelGSt LouisDHassanSSMialTN 2017 In vivo activation of invariant natural killer T cells induces systemic and local alterations in T-cell subsets prior to preterm birth. Clinical and Experimental Immunology 211225. (https://doi.org/10.1111/cei.12968)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gomez-LopezNRomeroRMaymonEKusanovicJPPanaitescuBMillerDPacoraPTarcaALMotomuraKErezO et al. 2018a Clinical chorioamnionitis at term IX: in vivo evidence of intra-amniotic inflammasome activation. Journal of Perinatal Medicine 276287. (https://doi.org/10.1515/jpm-2018-0271)

    • Search Google Scholar
    • Export Citation
  • Gomez-LopezNRomeroRXuYMillerDLengYPanaitescuBSilvaPFaroJAlhousseiniAGilN et al. 2018b The immunophenotype of amniotic fluid leukocytes in normal and complicated pregnancies. American Journal of Reproductive Immunology e12827. (https://doi.org/10.1111/aji.12827)

    • Search Google Scholar
    • Export Citation
  • HardyRRHayakawaK 2001 B cell development pathways. Annual Review of Immunology 595621. (https://doi.org/10.1146/annurev.immunol.19.1.595) (available at: http://www.annualreviews.org/doi/abs/10.1146/annurev.immunol.19.1.595)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • HuangBFaucetteANPawlitzMDPeiBGoyertJWZhouJZEl-HageNGDengJLinJYaoF et al. 2017 Interleukin-33-induced expression of PIBF1 by decidual B cells protects against preterm labor. Nature Medicine 128135. (https://doi.org/10.1038/nm.4244)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • JensenFWallukatGHerseFBudnerOEl-MouslehTCostaSDDechendRZenclussenAC 2012 CD19+CD5+ cells as indicators of preeclampsia. Hypertension 59 861.

  • JiJVijayaragavanKBosseMMenendezPWeiselKBhatiaM 2008 OP9 stroma augments survival of hematopoietic precursors and progenitors during hematopoietic differentiation from human embryonic stem cells. Stem Cells 24852495. (https://doi.org/10.1634/stemcells.2008-0642)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • KagaNKatsukiYObataMShibutaniY 1996 Repeated administration of low-dose lipopolysaccharide induces preterm delivery in mice: a model for human preterm parturition and for assessment of the therapeutic ability of drugs against preterm delivery. American Journal of Obstetrics and Gynecology 754759. (https://doi.org/10.1016/S0002-9378(96)70460-X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • KincadePWMedinaKLSmithsonGScottDC 1994 Pregnancy: a clue to normal regulation of B lymphopoiesis. Immunology Today 15 539.

  • LarsenBChengHFGalaskRP 1979 Bacterial growth inhibition by amniotic fluid. VIII. Evaluation of a radiometric bioassay for rapid, in vitro demonstration of phosphate-sensitive bacterial growth inhibitor in amniotic fluid. American Journal of Obstetrics and Gynecology 1421.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • LengYRomeroRXuYGalazJSlutskyRArenas-HernandezMGarcia-FloresVMotomuraKHassanSSReboldiA et al. 2019 Are B cells altered in the decidua of women with preterm or term labor? American Journal of Reproductive Immunology e13102. (https://doi.org/10.1111/aji.13102)

    • Search Google Scholar
    • Export Citation
  • LundFE 2008 Cytokine-producing B lymphocytes – key regulators of immunity. Current Opinion in Immunology 332338. (https://doi.org/10.1016/j.coi.2008.03.003) (available at: http://linkinghub.elsevier.com/retrieve/pii/S0952791508000277)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • MedinaKLSmithsonGKincadePW 1993 Suppression of B lymphopoiesis during normal pregnancy. Journal of Experimental Medicine 178 15071515.

  • Montecino-RodriguezEDorshkindK 2012 B-1 B cell development in the fetus and adult. Immunity 1321. (https://doi.org/10.1016/j.immuni.2011.11.017)

  • Montecino-RodriguezELeathersHDorshkindK 2006 Identification of a B-1 B cell-specified progenitor. Nature Immunology 293301. (https://doi.org/10.1038/ni1301)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • MuzzioDOSoldatiREhrhardtJUtpatelKEvertMZenclussenACZygmuntMJensenF 2014 B cell development undergoes profound modifications and adaptations during pregnancy in mice. Biology of Reproduction 91 115.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • NguyenTTTElsnerRABaumgarthN 2015 Natural IgM prevents autoimmunity by enforcing B cell central tolerance induction. Journal of Immunology 14891502. (https://doi.org/10.4049/jimmunol.1401880)

    • Search Google Scholar
    • Export Citation
  • NiemeläAKulomaaMViljaPTuohimaaPSaarikoskiS 1989 Lactoferrin in human amniotic fluid. Human Reproduction 99101. (https://doi.org/10.1093/oxfordjournals.humrep.a136854)

    • Search Google Scholar
    • Export Citation
  • PieperKGrimbacherBEibelH 2013 B-cell biology and development. Journal of Allergy and Clinical Immunology 959971. (https://doi.org/10.1016/j.jaci.2013.01.046)

    • Search Google Scholar
    • Export Citation
  • PierceJJacobsonPBenedettiEPetersonEPhibbsJPreslarAReemsJA 2016 Collection and characterization of amniotic fluid from scheduled C-section deliveries. Cell Tissue Bank 413425. (https://doi.org/10.1007/s10561-016-9572-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • RomeroRChaiworapongsaTAlpay SavasanZXuYHusseinYDongZKusanovicJPKimCJHassanSS 2011 Damage-associated molecular patterns (DAMPs) in preterm labor with intact membranes and preterm PROM: a study of the alarmin HMGB1. Journal of Maternal-Fetal and Neonatal Medicine 14441455. (https://doi.org/10.3109/14767058.2011.591460)

    • Search Google Scholar
    • Export Citation
  • SchlievertPJohnsonWGalaskRP 1976 Isolation of a low molecular weight antibacterial system from human amniotic fluid. Infection and Immunity 11561166.

  • SchlievertPJohnsonWGalaskRP 1977 Amniotic fluid antibacterial mechanisms: newer concepts. Seminars in Perinatology 5970. (available at: http://europepmc.org/abstract/MED/370990)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • SchmidtW 1992 The amniotic fluid compartment: the fetal habitat. Advances in Anatomy Embryology and Cell Biology 1100.

  • TafariNRossSMNaeyeRLGalaskRPZaarB 1977 Failure of bacterial growth inhibition by amniotic fluid. American Journal of Obstetrics and Gynecology 187189. (https://doi.org/10.1016/0002-9378(77)90685-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • UnderwoodMAGilbertWMShermanMP 2005 Amniotic fluid: not just fetal urine anymore. Journal of Perinatology 341348. (https://doi.org/10.1038/sj.jp.7211290)

    • Search Google Scholar
    • Export Citation
  • YoshimotoMMontecino-RodriguezEFerkowiczMJPorayettePShelleyWCConwaySJDorshkindKYoderMC 2011 Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. PNAS 14681473. (https://doi.org/10.1073/pnas.1015841108)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • ZieglerKBMuzzioDOMatznerFBommerIVentimigliaMSMalinowskyKEhrhardtJZygmuntMJensenF 2018 Human pregnancy is accompanied by modifications in B cell development and immunoglobulin profile. Journal of Reproductive Immunology 129 4047.

    • Crossref
    • Search Google Scholar
    • Export Citation