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Research Article

Epigenetic Signature of Exposure to Maternal Trypanosoma Cruzi Infection in Cord Blood Cells from Uninfected Newborns

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Pages 913-927 | Received 28 Apr 2022, Accepted 05 Aug 2022, Published online: 29 Aug 2022

References

  • WHO . Chagas disease in Latin America: an epidemiological update based on 2010 estimates. Weekly Epidemiol. Record90(6), 33–43 (2015).
  • Rassi A Jr , RassiA , Marin-NetoJA. Chagas disease. Lancet375(9723), 1388–1402 (2010).
  • Pereira Nunes MC , BeatonA , AcquatellaHet al. Chagas cardiomyopathy: an update of current clinical knowledge and management. A scientific statement from the American Heart Association. Circulation138(12), e169–e209 (2018).
  • Lee BY , BaconKM , BottazziME , HotezPJ. Global economic burden of Chagas disease: a computational simulation model. Lancet Infect. Dis.13(4), 342–348 (2013).
  • Bern C . Chagas disease. N. Engl. J. Med.373(5), 456–466 (2015).
  • Howard EJ , XiongX , CarlierY , Sosa-EstaniS , BuekensP. Frequency of the congenital transmission of Trypanosoma cruzi: a systematic review and meta-analysis. BJOG121(1), 22–33 (2014).
  • Howard EJ , BuekensP , CarlierY. Current treatment guidelines for Trypanosoma cruzi infection in pregnant women and infants. Int. J. Antimicrob. Agents39(5), 451–452 (2012).
  • Buekens P , CafferataML , AlgerJet al. Congenital transmission of Trypanosoma cruzi in Argentina, Honduras, and Mexico: an observational prospective study. Am. J. Trop. Med. Hyg.98(2), 478–485 (2018).
  • Bern C , MessengerLA , WhitmanJD , MaguireJH. Chagas disease in the United States: a public health approach. Clin. Microbiol. Rev.33(1), e00023-19 (2019).
  • Carlier Y , TruyensC. Congenital Chagas disease as an ecological model of interactions between Trypanosoma cruzi parasites, pregnant women, placenta and fetuses. Acta Trop.151, 103–115 (2015).
  • Carlier Y , Sosa-EstaniS , LuquettiAO , BuekensP. Congenital Chagas disease: an update. Mem. Inst. Oswaldo Cruz110(3), 363–368 (2015).
  • Cameron N , DemerathEW. Critical periods in human growth and their relationship to diseases of aging. Am. J. Phys. Anthropol.Suppl. 35, 159–184 (2002).
  • Barker DJ . Fetal origins of coronary heart disease. BMJ (Clin. Res. Ed.)311(6998), 171–174 (1995).
  • Barker DJ , ErikssonJG , ForsenT , OsmondC. Fetal origins of adult disease: strength of effects and biological basis. Int. J. Epidemiol.31(6), 1235–1239 (2002).
  • Penkler M , HansonM , BiesmaR , MullerR. DOHaD in science and society: emergent opportunities and novel responsibilities. J. Dev. Orig. Health Dis.10(3), 268–273 (2019).
  • Sly PD . The early origins of asthma: who is really at risk?Curr. Opin. Allergy Clin. Immunol.11(1), 24–28 (2011).
  • Duijts L , ReissIK , BrusselleG , DeJongste JC. Early origins of chronic obstructive lung diseases across the life course. Eur. J. Epidemiol.29(12), 871–885 (2014).
  • Koletzko B , DecsiT , MolnárD , HuntyA. Early Nutrition Programming and Health Outcomes in Later Life: Obesity and Beyond. Springer Science & Business Media, The Netherlands, 646 (2009).
  • Brown AS , DerkitsEJ. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am. J. Psychiatry167(3), 261–280 (2010).
  • Miller BJ , CulpepperN , RapaportMH , BuckleyP. Prenatal inflammation and neurodevelopment in schizophrenia: a review of human studies. Prog. Neuropsychopharmacol. Biol. Psychiatry42, 92–100 (2013).
  • Atladottir HO , HenriksenTB , SchendelDE , ParnerET. Autism after infection, febrile episodes, and antibiotic use during pregnancy: an exploratory study. Pediatrics130(6), e1447–1454 (2012).
  • Brown AS , SouranderA , Hinkka-Yli-SalomakiS , MckeagueIW , SundvallJ , SurcelHM. Elevated maternal C-reactive protein and autism in a national birth cohort. Mol. Psychiatry19(2), 259–264 (2014).
  • Parboosing R , BaoY , ShenL , SchaeferCA , BrownAS. Gestational influenza and bipolar disorder in adult offspring. JAMA Psychiatry70(7), 677–685 (2013).
  • Canetta SE , BaoY , CoMDet al. Serological documentation of maternal influenza exposure and bipolar disorder in adult offspring. Am. J. Psychiatry171(5), 557–563 (2014).
  • Francis DD . Conceptualizing child health disparities: a role for developmental neurogenomics. Pediatrics124(Suppl. 3), S196–S202 (2009).
  • Pepin ME , DrakosS , HaCMet al. DNA methylation reprograms cardiac metabolic gene expression in end-stage human heart failure. Am. J. Physiol. Heart Circ. Physiol.317(4), H674–H684 (2019).
  • Glezeva N , MoranB , CollierPet al. Targeted DNA methylation profiling of human cardiac tissue reveals novel epigenetic traits and gene deregulation across different heart failure patient subtypes. Circ. Heart Fail.12(3), e005765 (2019).
  • Richetto J , MassartR , Weber-StadlbauerU , SzyfM , RivaMA , MeyerU. Genome-wide DNA methylation changes in a mouse model of infection-mediated neurodevelopmental disorders. Biol. Psychiatry81(3), 265–276 (2017).
  • Cheng Q , ZhaoB , HuangZet al. Epigenome-wide study for the offspring exposed to maternal HBV infection during pregnancy, a pilot study. Gene658, 76–85 (2018).
  • Lim AI , McfaddenT , LinkVMet al. Prenatal maternal infection promotes tissue-specific immunity and inflammation in offspring. Science373(6558), eabf3002 (2021).
  • Weber-Stadlbauer U . Epigenetic and transgenerational mechanisms in infection-mediated neurodevelopmental disorders. Transl. Psychiatry7(5), e1113 (2017).
  • Bhagirath AY , MedapatiMR , DeJesus VCet al. Role of maternal infections and inflammatory responses on craniofacial development. Front. Oral Health2(56), 735634 (2021).
  • Anderson D , NeriJ , SouzaCRMet al. Zika virus changes methylation of genes involved in immune response and neural development in Brazilian babies born with congenital microcephaly. J. Infect. Dis.223(3), 435–440 (2021).
  • Neves SF , Eloi-SantosS , RamosR , RigueirinhoS , GazzinelliG , Correa-OliveiraR. In utero sensitization in Chagas disease leads to altered lymphocyte phenotypic patterns in the newborn cord blood mononuclear cells. Parasite Immunol.21(12), 631–639 (1999).
  • Dauby N , Alonso-VegaC , SuarezEet al. Maternal infection with Trypanosoma cruzi and congenital Chagas disease induce a trend to a type 1 polarization of infant immune responses to vaccines. PLOS Negl. Trop. Dis.3(12), e571 (2009).
  • Netea MG , Dominguez-AndresJ , BarreiroLBet al. Defining trained immunity and its role in health and disease. Nat. Rev. Immunol.20(6), 375–388 (2020).
  • Sosa-Estani S , Gamboa-LeonMR , DelCid-Lemus Jet al. Use of a rapid test on umbilical cord blood to screen for Trypanosoma cruzi infection in pregnant women in Argentina, Bolivia, Honduras, and Mexico. Am. J. Trop. Med. Hyg.79(5), 755–759 (2008).
  • Pidsley R , ZotenkoE , PetersTJet al. Critical evaluation of the Illumina MethylationEPIC BeadChip microarray for whole-genome DNA methylation profiling. Genome Biol.17(1), 208 (2016).
  • R: a language and environment for statistical computing. www.R-project.org/
  • Aryee MJ , JaffeAE , Corrada-BravoHet al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics30(10), 1363–1369 (2014).
  • Morris TJ , ButcherLM , FeberAet al. ChAMP: 450k Chip Analysis Methylation Pipeline. Bioinformatics30(3), 428–430 (2014).
  • Rahmani E , SchweigerR , RheadBet al. Cell-type-specific resolution epigenetics without the need for cell sorting or single-cell biology. Nat. Commun.10(1), 3417 (2019).
  • Rahmani E , ZaitlenN , BaranYet al. Sparse PCA corrects for cell type heterogeneity in epigenome-wide association studies. Nat. Methods13(5), 443–445 (2016).
  • Zheng SC , BreezeCE , BeckS , TeschendorffAE. Identification of differentially methylated cell types in epigenome-wide association studies. Nat. Methods15(12), 1059–1066 (2018).
  • Lin X , TanJYL , TehALet al. Cell type-specific DNA methylation in neonatal cord tissue and cord blood: a 850K-reference panel and comparison of cell types. Epigenetics13(9), 941–958 (2018).
  • Ren X , KuanPF. methylGSA: a Bioconductor package and Shiny app for DNA methylation data length bias adjustment in gene set testing. Bioinformatics35(11), 1958–1959 (2019).
  • Szklarczyk D , GableAL , NastouKCet al. The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucl. Acids Res.49(D1), D605–D612 (2021).
  • Nouatin O , GbedandeK , IbitokouSet al. Infants’ peripheral blood lymphocyte composition reflects both maternal and post-natal infection with Plasmodium falciparum. PlOS ONE10(11), e0139606 (2015).
  • Da Paz VRF , SequeiraD , PyrrhoA. Infection by Schistosoma mansoni during pregnancy: effects on offspring immunity. Life Sci.185, 46–52 (2017).
  • Jaime-Perez JC , Colunga-PedrazaJE , Monreal-RoblesRet al. Acute maternal cytomegalovirus infection is associated with significantly decreased numbers of CD34+ cells in umbilical cord blood. Blood Cells Mol. Dis.49(3–4), 166–169 (2012).
  • Borges-Almeida E , MilanezHM , VilelaMMet al. The impact of maternal HIV infection on cord blood lymphocyte subsets and cytokine profile in exposed non-infected newborns. BMC Inf. Dis.11, 38 (2011).
  • Abioye AI , McDonaldEA , ParkSet al. Maternal, placental and cord blood cytokines and the risk of adverse birth outcomes among pregnant women infected with Schistosoma japonicum in the Philippines. PLOS Negl. Trop. Dis.13(6), e0007371 (2019).
  • Miles DJ , GadamaL , GumbiA , NyaloF , MakananiB , HeydermanRS. Human immunodeficiency virus (HIV) infection during pregnancy induces CD4 T-cell differentiation and modulates responses to Bacille Calmette–Guérin (BCG) vaccine in HIV-uninfected infants. Immunology129(3), 446–454 (2010).
  • Vekemans J , TruyensC , TorricoFet al. Maternal Trypanosoma cruzi infection upregulates capacity of uninfected neonate cells to produce pro- and anti-inflammatory cytokines. Infect. Immun.68(9), 5430–5434 (2000).
  • Rose DR , CareagaM , VanDe Water J , McallisterK , BaumanMD , AshwoodP. Long-term altered immune responses following fetal priming in a non-human primate model of maternal immune activation. Brain Behav. Immun.63, 60–70 (2017).
  • Mueller FS , ScarboroughJ , SchalbetterSMet al. Behavioral, neuroanatomical, and molecular correlates of resilience and susceptibility to maternal immune activation. Mol. Psychiatry26(2), 396–410 (2021).
  • Klar K , PerchermeierS , BhattacharjeeSet al. Chronic schistosomiasis during pregnancy epigenetically reprograms T-cell differentiation in offspring of infected mothers. Eur. J. Immunol.47(5), 841–847 (2017).
  • Alfano R , GuidaF , GalobardesBet al. Socioeconomic position during pregnancy and DNA methylation signatures at three stages across early life: epigenome-wide association studies in the ALSPAC birth cohort. Int. J. Epidemiol.48(1), 30–44 (2019).
  • Kupers LK , MonnereauC , SharpGCet al. Meta-analysis of epigenome-wide association studies in neonates reveals widespread differential DNA methylation associated with birthweight. Nat. Commun.10(1), 1893 (2019).
  • De Goede OM , LavoiePM , RobinsonWP. Cord blood hematopoietic cells from preterm infants display altered DNA methylation patterns. Clin. Epigenetics9, 39 (2017).
  • Merid SK , NovoloacaA , SharpGCet al. Epigenome-wide meta-analysis of blood DNA methylation in newborns and children identifies numerous loci related to gestational age. Genome Med.12(1), 25 (2020).
  • Barcelona V , HuangY , BrownKet al. Novel DNA methylation sites associated with cigarette smoking among African Americans. Epigenetics14(4), 383–391 (2019).
  • Hannon E , SchendelD , Ladd-AcostaCet al. Variable DNA methylation in neonates mediates the association between prenatal smoking and birth weight. Philos. Trans. R. Soc. London B Biol. Sci.374(1770), 20180120 (2019).
  • Haertle L , ElHajj N , DittrichMet al. Epigenetic signatures of gestational diabetes mellitus on cord blood methylation. Clin. Epigenetics9, 28 (2017).
  • Kazmi N , SharpGC , ReeseSEet al. Hypertensive disorders of pregnancy and DNA methylation in newborns. Hypertension74(2), 375–383 (2019).
  • Linner A , AlmgrenM. Epigenetic programming – the important first 1000 days. Acta Paediatr.109(3), 443–452 (2020).
  • Shiau S , StrehlauR , WangSet al. Distinct epigenetic profiles in children with perinatally acquired HIV on antiretroviral therapy. Sci. Rep.9(1), 10495 (2019).
  • Bermick J , SchallerM. Epigenetic regulation of pediatric and neonatal immune responses. Pediatr. Res.91(2), 297–327 (2021).
  • Rivera MT , Marquesde Araujo S , LucasRet al. High tumor necrosis factor alpha (TNF-alpha) production in Trypanosoma cruzi-infected pregnant mice and increased TNF-alpha gene transcription in their offspring. Infect. Immun.63(2), 591–595 (1995).

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