Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy
Chagas disease, caused by the protozoan Trypanosoma cruzi, is an endemic parasitic disease of Latin America, affecting 7 million people. Although most patients are asymptomatic, 30% develop complications, including the often-fatal Chronic Chagasic Cardiomyopathy (CCC). Although previous studies have...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.958200/full |
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| author | Pauline Brochet Barbara Maria Ianni Laurie Laugier Amanda Farage Frade Amanda Farage Frade Amanda Farage Frade João Paulo Silva Nunes João Paulo Silva Nunes João Paulo Silva Nunes João Paulo Silva Nunes Priscila Camillo Teixeira Priscila Camillo Teixeira Priscila Camillo Teixeira Charles Mady Ludmila Rodrigues Pinto Ferreira Quentin Ferré Ronaldo Honorato Barros Santos Andreia Kuramoto Sandrine Cabantous Samuel Steffen Samuel Steffen Antonio Noedir Stolf Pablo Pomerantzeff Alfredo Inacio Fiorelli Edimar Alcides Bocchi Cristina Wide Pissetti Bruno Saba Darlan da Silva Cândido Darlan da Silva Cândido Darlan da Silva Cândido Fabrício C. Dias Marcelo Ferraz Sampaio Fabio Antônio Gaiotto Fabio Antônio Gaiotto José Antonio Marin-Neto Abílio Fragata Ricardo Costa Fernandes Zaniratto Sergio Siqueira Giselle De Lima Peixoto Vagner Oliveira-Carvalho Rigaud Vagner Oliveira-Carvalho Rigaud Fernando Bacal Paula Buck Rafael Ribeiro Almeida Rafael Ribeiro Almeida Rafael Ribeiro Almeida Hui Tzu Lin-Wang André Schmidt Martino Martinelli Mario Hiroyuki Hirata Eduardo Antonio Donadi Alexandre Costa Pereira Virmondes Rodrigues Junior Denis Puthier Jorge Kalil Jorge Kalil Jorge Kalil Lionel Spinelli Lionel Spinelli Edecio Cunha-Neto Edecio Cunha-Neto Edecio Cunha-Neto Christophe Chevillard |
| author_facet | Pauline Brochet Barbara Maria Ianni Laurie Laugier Amanda Farage Frade Amanda Farage Frade Amanda Farage Frade João Paulo Silva Nunes João Paulo Silva Nunes João Paulo Silva Nunes João Paulo Silva Nunes Priscila Camillo Teixeira Priscila Camillo Teixeira Priscila Camillo Teixeira Charles Mady Ludmila Rodrigues Pinto Ferreira Quentin Ferré Ronaldo Honorato Barros Santos Andreia Kuramoto Sandrine Cabantous Samuel Steffen Samuel Steffen Antonio Noedir Stolf Pablo Pomerantzeff Alfredo Inacio Fiorelli Edimar Alcides Bocchi Cristina Wide Pissetti Bruno Saba Darlan da Silva Cândido Darlan da Silva Cândido Darlan da Silva Cândido Fabrício C. Dias Marcelo Ferraz Sampaio Fabio Antônio Gaiotto Fabio Antônio Gaiotto José Antonio Marin-Neto Abílio Fragata Ricardo Costa Fernandes Zaniratto Sergio Siqueira Giselle De Lima Peixoto Vagner Oliveira-Carvalho Rigaud Vagner Oliveira-Carvalho Rigaud Fernando Bacal Paula Buck Rafael Ribeiro Almeida Rafael Ribeiro Almeida Rafael Ribeiro Almeida Hui Tzu Lin-Wang André Schmidt Martino Martinelli Mario Hiroyuki Hirata Eduardo Antonio Donadi Alexandre Costa Pereira Virmondes Rodrigues Junior Denis Puthier Jorge Kalil Jorge Kalil Jorge Kalil Lionel Spinelli Lionel Spinelli Edecio Cunha-Neto Edecio Cunha-Neto Edecio Cunha-Neto Christophe Chevillard |
| author_sort | Pauline Brochet |
| collection | DOAJ |
| description | Chagas disease, caused by the protozoan Trypanosoma cruzi, is an endemic parasitic disease of Latin America, affecting 7 million people. Although most patients are asymptomatic, 30% develop complications, including the often-fatal Chronic Chagasic Cardiomyopathy (CCC). Although previous studies have demonstrated some genetic deregulations associated with CCCs, the causes of their deregulations remain poorly described. Based on bulk RNA-seq and whole genome DNA methylation data, we investigated the genetic and epigenetic deregulations present in the moderate and severe stages of CCC. Analysis of heart tissue gene expression profile allowed us to identify 1407 differentially expressed transcripts (DEGs) specific from CCC patients. A tissue DNA methylation analysis done on the same tissue has permitted the identification of 92 regulatory Differentially Methylated Regions (DMR) localized in the promoter of DEGs. An in-depth study of the transcription factors binding sites (TFBS) in the DMRs corroborated the importance of TFBS’s DNA methylation for gene expression in CCC myocardium. TBX21, RUNX3 and EBF1 are the transcription factors whose binding motif appears to be affected by DNA methylation in the largest number of genes. By combining both transcriptomic and methylomic analysis on heart tissue, and methylomic analysis on blood, 4 biological processes affected by severe CCC have been identified, including immune response, ion transport, cardiac muscle processes and nervous system. An additional study on blood methylation of moderate CCC samples put forward the importance of ion transport and nervous system in the development of the disease. |
| first_indexed | 2024-04-13T18:48:13Z |
| format | Article |
| id | doaj.art-65fdda843b04496390e425c5897c4f93 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-13T18:48:13Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-65fdda843b04496390e425c5897c4f932022-12-22T02:34:31ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-08-011310.3389/fimmu.2022.958200958200Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathyPauline Brochet0Barbara Maria Ianni1Laurie Laugier2Amanda Farage Frade3Amanda Farage Frade4Amanda Farage Frade5João Paulo Silva Nunes6João Paulo Silva Nunes7João Paulo Silva Nunes8João Paulo Silva Nunes9Priscila Camillo Teixeira10Priscila Camillo Teixeira11Priscila Camillo Teixeira12Charles Mady13Ludmila Rodrigues Pinto Ferreira14Quentin Ferré15Ronaldo Honorato Barros Santos16Andreia Kuramoto17Sandrine Cabantous18Samuel Steffen19Samuel Steffen20Antonio Noedir Stolf21Pablo Pomerantzeff22Alfredo Inacio Fiorelli23Edimar Alcides Bocchi24Cristina Wide Pissetti25Bruno Saba26Darlan da Silva Cândido27Darlan da Silva Cândido28Darlan da Silva Cândido29Fabrício C. Dias30Marcelo Ferraz Sampaio31Fabio Antônio Gaiotto32Fabio Antônio Gaiotto33José Antonio Marin-Neto34Abílio Fragata35Ricardo Costa Fernandes Zaniratto36Sergio Siqueira37Giselle De Lima Peixoto38Vagner Oliveira-Carvalho Rigaud39Vagner Oliveira-Carvalho Rigaud40Fernando Bacal41Paula Buck42Rafael Ribeiro Almeida43Rafael Ribeiro Almeida44Rafael Ribeiro Almeida45Hui Tzu Lin-Wang46André Schmidt47Martino Martinelli48Mario Hiroyuki Hirata49Eduardo Antonio Donadi50Alexandre Costa Pereira51Virmondes Rodrigues Junior52Denis Puthier53Jorge Kalil54Jorge Kalil55Jorge Kalil56Lionel Spinelli57Lionel Spinelli58Edecio Cunha-Neto59Edecio Cunha-Neto60Edecio Cunha-Neto61Christophe Chevillard62Institut National de la Santé Et de la Recherche Médicale (INSERM), Unité Mixte de Recherche (UMR)_1090, Aix Marseille Université, TAGC Theories and Approaches of Genomic Complexity, Institut MarMaRa, Marseille, FranceLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilAix Marseille Université, Génétique et Immunologie des Maladies Parasitaires, Inserm, UMR_906, Marseille, FranceLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, BrazilInstitut National de la Santé Et de la Recherche Médicale (INSERM), Unité Mixte de Recherche (UMR)_1090, Aix Marseille Université, TAGC Theories and Approaches of Genomic Complexity, Institut MarMaRa, Marseille, FranceLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, BrazilLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, BrazilMyocardiopathies and Aortic Diseases Unit, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, BrazilRNA Systems Biology Laboratory (RSBL), Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, BrazilInstitut National de la Santé Et de la Recherche Médicale (INSERM), Unité Mixte de Recherche (UMR)_1090, Aix Marseille Université, TAGC Theories and Approaches of Genomic Complexity, Institut MarMaRa, Marseille, FranceDivision of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilAix Marseille Université, Génétique et Immunologie des Maladies Parasitaires, Inserm, UMR_906, Marseille, FranceDivision of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil0Heart Institute (InCor), School of Medicine, University of São Paulo, São Paulo, São Paulo, BrazilDivision of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil1Laboratory of Immunology, Universidade Federal Do Triângulo Mineiro (UFTM), Uberaba, Brazil2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, BrazilLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, BrazilDivision of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, BrazilLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil4Pacemaker Clinic, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, Brazil4Pacemaker Clinic, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, BrazilLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil5Heart Failure Unit, Heart Institute Instituto do Coração (InCor) School of Medicine, University of Sao Paulo, Sao Paulo, BrazilDivision of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil0Heart Institute (InCor), School of Medicine, University of São Paulo, São Paulo, São Paulo, BrazilLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, Brazil3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil4Pacemaker Clinic, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, Brazil6Department of Clinical and Toxicological Analyses, Faculty of Pharmaceutical Sciences, University of São Paulo (USP), São Paulo, Brazil3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil0Heart Institute (InCor), School of Medicine, University of São Paulo, São Paulo, São Paulo, Brazil1Laboratory of Immunology, Universidade Federal Do Triângulo Mineiro (UFTM), Uberaba, BrazilInstitut National de la Santé Et de la Recherche Médicale (INSERM), Unité Mixte de Recherche (UMR)_1090, Aix Marseille Université, TAGC Theories and Approaches of Genomic Complexity, Institut MarMaRa, Marseille, FranceLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, BrazilInstitut National de la Santé Et de la Recherche Médicale (INSERM), Unité Mixte de Recherche (UMR)_1090, Aix Marseille Université, TAGC Theories and Approaches of Genomic Complexity, Institut MarMaRa, Marseille, France7Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy, Marseille, FranceLaboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, BrazilDivision of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, BrazilInstituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, BrazilInstitut National de la Santé Et de la Recherche Médicale (INSERM), Unité Mixte de Recherche (UMR)_1090, Aix Marseille Université, TAGC Theories and Approaches of Genomic Complexity, Institut MarMaRa, Marseille, FranceChagas disease, caused by the protozoan Trypanosoma cruzi, is an endemic parasitic disease of Latin America, affecting 7 million people. Although most patients are asymptomatic, 30% develop complications, including the often-fatal Chronic Chagasic Cardiomyopathy (CCC). Although previous studies have demonstrated some genetic deregulations associated with CCCs, the causes of their deregulations remain poorly described. Based on bulk RNA-seq and whole genome DNA methylation data, we investigated the genetic and epigenetic deregulations present in the moderate and severe stages of CCC. Analysis of heart tissue gene expression profile allowed us to identify 1407 differentially expressed transcripts (DEGs) specific from CCC patients. A tissue DNA methylation analysis done on the same tissue has permitted the identification of 92 regulatory Differentially Methylated Regions (DMR) localized in the promoter of DEGs. An in-depth study of the transcription factors binding sites (TFBS) in the DMRs corroborated the importance of TFBS’s DNA methylation for gene expression in CCC myocardium. TBX21, RUNX3 and EBF1 are the transcription factors whose binding motif appears to be affected by DNA methylation in the largest number of genes. By combining both transcriptomic and methylomic analysis on heart tissue, and methylomic analysis on blood, 4 biological processes affected by severe CCC have been identified, including immune response, ion transport, cardiac muscle processes and nervous system. An additional study on blood methylation of moderate CCC samples put forward the importance of ion transport and nervous system in the development of the disease.https://www.frontiersin.org/articles/10.3389/fimmu.2022.958200/fulldilated cardiomyopathyChagas diseaseepigeneticmethylationTh1 responsetranscription factors |
| spellingShingle | Pauline Brochet Barbara Maria Ianni Laurie Laugier Amanda Farage Frade Amanda Farage Frade Amanda Farage Frade João Paulo Silva Nunes João Paulo Silva Nunes João Paulo Silva Nunes João Paulo Silva Nunes Priscila Camillo Teixeira Priscila Camillo Teixeira Priscila Camillo Teixeira Charles Mady Ludmila Rodrigues Pinto Ferreira Quentin Ferré Ronaldo Honorato Barros Santos Andreia Kuramoto Sandrine Cabantous Samuel Steffen Samuel Steffen Antonio Noedir Stolf Pablo Pomerantzeff Alfredo Inacio Fiorelli Edimar Alcides Bocchi Cristina Wide Pissetti Bruno Saba Darlan da Silva Cândido Darlan da Silva Cândido Darlan da Silva Cândido Fabrício C. Dias Marcelo Ferraz Sampaio Fabio Antônio Gaiotto Fabio Antônio Gaiotto José Antonio Marin-Neto Abílio Fragata Ricardo Costa Fernandes Zaniratto Sergio Siqueira Giselle De Lima Peixoto Vagner Oliveira-Carvalho Rigaud Vagner Oliveira-Carvalho Rigaud Fernando Bacal Paula Buck Rafael Ribeiro Almeida Rafael Ribeiro Almeida Rafael Ribeiro Almeida Hui Tzu Lin-Wang André Schmidt Martino Martinelli Mario Hiroyuki Hirata Eduardo Antonio Donadi Alexandre Costa Pereira Virmondes Rodrigues Junior Denis Puthier Jorge Kalil Jorge Kalil Jorge Kalil Lionel Spinelli Lionel Spinelli Edecio Cunha-Neto Edecio Cunha-Neto Edecio Cunha-Neto Christophe Chevillard Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy Frontiers in Immunology dilated cardiomyopathy Chagas disease epigenetic methylation Th1 response transcription factors |
| title | Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy |
| title_full | Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy |
| title_fullStr | Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy |
| title_full_unstemmed | Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy |
| title_short | Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy |
| title_sort | epigenetic regulation of transcription factor binding motifs promotes th1 response in chagas disease cardiomyopathy |
| topic | dilated cardiomyopathy Chagas disease epigenetic methylation Th1 response transcription factors |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.958200/full |
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