An Integrative Analysis of DNA Methylation Pattern in Myotonic Dystrophy Type 1 Samples Reveals a Distinct DNA Methylation Profile between Tissues and a Novel Muscle-Associated Epigenetic Dysregulation


Por: Koehorst E, Odria R, Capó J, Núñez-Manchón J, Arbex A, Almendrote M, Linares-Pardo I, Natera-de Benito D, Saez V, Nascimento-Osorio A, Ortez-Gonzalez CI, Rubio MÁ, Díaz-Manera J, Alonso-Pérez J, Lucente G, Rodriguez-Palmero A, Ramos-Fransi A, Martínez-Piñeiro A, Nogales-Gadea G and Suelves M

Publicada: 1 jun 2022 Ahead of Print: 10 jun 2022
Resumen:
Myotonic dystrophy type 1 (DM1) is a progressive, non-treatable, multi-systemic disorder. To investigate the contribution of epigenetics to the complexity of DM1, we compared DNA methylation profiles of four annotated CpG islands (CpGis) in the DMPK locus and neighbouring genes, in distinct DM1 tissues and derived cells, representing six DM1 subtypes, by bisulphite sequencing. In blood, we found no differences in CpGi 74, 43 and 36 in DNA methylation profile. In contrast, a CTCF1 DNA methylation gradient was found with 100% methylation in congenital cases, 50% in childhood cases and 13% in juvenile cases. CTCF1 methylation correlated to disease severity and CTG expansion size. Notably, 50% of CTCF1 methylated cases showed methylation in the CTCF2 regions. Additionally, methylation was associated with maternal transmission. Interestingly, the evaluation of seven families showed that unmethylated mothers passed on an expansion of the CTG repeat, whereas the methylated mothers transmitted a contraction. The analysis of patient-derived cells showed that DNA methylation profiles were highly preserved, validating their use as faithful DM1 cellular models. Importantly, the comparison of DNA methylation levels of distinct DM1 tissues revealed a novel muscle-specific epigenetic signature with methylation of the CTCF1 region accompanied by demethylation of CpGi 43, a region containing an alternative DMPK promoter, which may decrease the canonical promoter activity. Altogether, our results showed a distinct DNA methylation profile across DM1 tissues and uncovered a novel and dual epigenetic signature in DM1 muscle samples, providing novel insights into the epigenetic changes associated with DM1.

Filiaciones:
Koehorst E:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Odria R:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Capó J:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Núñez-Manchón J:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Arbex A:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

 Neuromuscular Pathology Unit, Neurology Service, Neuroscience Department, Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain

Almendrote M:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

 Neuromuscular Pathology Unit, Neurology Service, Neuroscience Department, Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain

Linares-Pardo I:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Natera-de Benito D:
 Neuromuscular Unit, Neuropediatric Department, Institut de Recerca Pediàtrica Hospital Sant Joan de Déu, L'Hospitalet de Llobregat, 08950 Barcelona, Spain

Saez V:
 Neuromuscular Unit, Neuropediatric Department, Institut de Recerca Pediàtrica Hospital Sant Joan de Déu, L'Hospitalet de Llobregat, 08950 Barcelona, Spain

Nascimento-Osorio A:
 Neuromuscular Unit, Neuropediatric Department, Institut de Recerca Pediàtrica Hospital Sant Joan de Déu, L'Hospitalet de Llobregat, 08950 Barcelona, Spain

Ortez-Gonzalez CI:
 Neuromuscular Unit, Neuropediatric Department, Institut de Recerca Pediàtrica Hospital Sant Joan de Déu, L'Hospitalet de Llobregat, 08950 Barcelona, Spain

Rubio MÁ:
 Neuromuscular Unit, Department of Neurology, Hospital del Mar, 08003 Barcelona, Spain

Díaz-Manera J:
 Neuromuscular Diseases Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau, 08025 Barcelona, Spain

 John Walton Muscular Dystrophy Research Centre, Newcastle University and Newcastle Hospitals NHS Foundation Trust, Newcastle upon Tyne NE1 3BZ, UK

Alonso-Pérez J:
 Neuromuscular Diseases Unit, Department of Neurology, Hospital de la Santa Creu i Sant Pau, 08025 Barcelona, Spain

Lucente G:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

 Neuromuscular Pathology Unit, Neurology Service, Neuroscience Department, Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain

Rodriguez-Palmero A:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

 Pediatric Neurology Unit, Department of Pediatrics, Hospital Universitari Germans Trias i Pujol, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Ramos-Fransi A:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

 Neuromuscular Pathology Unit, Neurology Service, Neuroscience Department, Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain

Martínez-Piñeiro A:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

 Neuromuscular Pathology Unit, Neurology Service, Neuroscience Department, Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain

Nogales-Gadea G:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain

Suelves M:
 Neuromuscular and Neuropediatric Research Group, Institut d'Investigació en Ciències de la Salut Germans Trias i Pujol (IGTP), Campus Can Ruti, Universitat Autònoma de Barcelona, 08916 Badalona, Spain
ISSN: 22279059





Biomedicines
Editorial
MDPI, MDPI AG, Grosspeteranlage 5, CH-4052 BASEL, SWITZERLAND, Suiza
Tipo de documento: Article
Volumen: 10 Número: 6
Páginas: 1372
WOS Id: 000816551200001
ID de PubMed: 35740394
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