Frontiers in Immunology (Aug 2022)
Epigenetic regulation of transcription factor binding motifs promotes Th1 response in Chagas disease cardiomyopathy
- 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
Affiliations
- Pauline Brochet
- Institut 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, France
- Barbara Maria Ianni
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Laurie Laugier
- Aix Marseille Université, Génétique et Immunologie des Maladies Parasitaires, Inserm, UMR_906, Marseille, France
- Amanda Farage Frade
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Amanda Farage Frade
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- Amanda Farage Frade
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- João Paulo Silva Nunes
- Institut 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, France
- João Paulo Silva Nunes
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- João Paulo Silva Nunes
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- João Paulo Silva Nunes
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- Priscila Camillo Teixeira
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Priscila Camillo Teixeira
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- Priscila Camillo Teixeira
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- Charles Mady
- Myocardiopathies and Aortic Diseases Unit, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, Brazil
- Ludmila Rodrigues Pinto Ferreira
- RNA Systems Biology Laboratory (RSBL), Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
- Quentin Ferré
- Institut 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, France
- Ronaldo Honorato Barros Santos
- Division of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Andreia Kuramoto
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Sandrine Cabantous
- Aix Marseille Université, Génétique et Immunologie des Maladies Parasitaires, Inserm, UMR_906, Marseille, France
- Samuel Steffen
- Division of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Samuel Steffen
- Division of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Antonio Noedir Stolf
- Division of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Pablo Pomerantzeff
- 0Heart Institute (InCor), School of Medicine, University of São Paulo, São Paulo, São Paulo, Brazil
- Alfredo Inacio Fiorelli
- Division of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Edimar Alcides Bocchi
- Division of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Cristina Wide Pissetti
- 1Laboratory of Immunology, Universidade Federal Do Triângulo Mineiro (UFTM), Uberaba, Brazil
- Bruno Saba
- 2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, Brazil
- Darlan da Silva Cândido
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Darlan da Silva Cândido
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- Darlan da Silva Cândido
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- Fabrício C. Dias
- 3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil
- Marcelo Ferraz Sampaio
- 2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, Brazil
- Fabio Antônio Gaiotto
- Division of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Fabio Antônio Gaiotto
- Division of Surgery, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- José Antonio Marin-Neto
- 3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil
- Abílio Fragata
- 2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, Brazil
- Ricardo Costa Fernandes Zaniratto
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Sergio Siqueira
- 4Pacemaker Clinic, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, Brazil
- Giselle De Lima Peixoto
- 4Pacemaker Clinic, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, Brazil
- Vagner Oliveira-Carvalho Rigaud
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Vagner Oliveira-Carvalho Rigaud
- 5Heart Failure Unit, Heart Institute Instituto do Coração (InCor) School of Medicine, University of Sao Paulo, Sao Paulo, Brazil
- Fernando Bacal
- Division of Transplantation, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Paula Buck
- 0Heart Institute (InCor), School of Medicine, University of São Paulo, São Paulo, São Paulo, Brazil
- Rafael Ribeiro Almeida
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Rafael Ribeiro Almeida
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- Rafael Ribeiro Almeida
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- Hui Tzu Lin-Wang
- 2Laboratório de Investigação Molecular em Cardiologia, Instituto de Cardiologia Dante Pazzanese (IDPC), São Paulo, Brazil
- André Schmidt
- 3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil
- Martino Martinelli
- 4Pacemaker Clinic, Heart Institute Instituto do Coração (InCor), School of Medicine, University of São Paulo, São Paulo, Brazil
- Mario Hiroyuki Hirata
- 6Department of Clinical and Toxicological Analyses, Faculty of Pharmaceutical Sciences, University of São Paulo (USP), São Paulo, Brazil
- Eduardo Antonio Donadi
- 3School of Medicine of Ribeirão Preto Faculdade de Medicina de Ribeirão Preto (FMRP), University of São Paulo, Ribeirão Preto, Brazil
- Alexandre Costa Pereira
- 0Heart Institute (InCor), School of Medicine, University of São Paulo, São Paulo, São Paulo, Brazil
- Virmondes Rodrigues Junior
- 1Laboratory of Immunology, Universidade Federal Do Triângulo Mineiro (UFTM), Uberaba, Brazil
- Denis Puthier
- Institut 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, France
- Jorge Kalil
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Jorge Kalil
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- Jorge Kalil
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- Lionel Spinelli
- Institut 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, France
- Lionel Spinelli
- 7Aix Marseille Université, CNRS, INSERM, Centre d'Immunologie de Marseille-Luminy, Marseille, France
- Edecio Cunha-Neto
- Laboratory of Immunology, Heart Institute Instituto do Coração (InCor), University of São Paulo, School of Medicine, São Paulo, Brazil
- Edecio Cunha-Neto
- Division of Clinical Immunology and Allergy, University of São Paulo, School of Medicine, São Paulo, Brazil
- Edecio Cunha-Neto
- Instituto Nacional de Ciência e Tecnologia, INCT, III- Institute for Investigation in Immunology, São Paulo, Brazil
- Christophe Chevillard
- Institut 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, France
- DOI
- https://doi.org/10.3389/fimmu.2022.958200
- Journal volume & issue
-
Vol. 13
Abstract
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.
Keywords