Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients

Abstract The epigenomic landscape of Parkinson's disease (PD) remains unknown. We performed a genomewide DNA methylation and a transcriptome studies in induced pluripotent stem cell (iPSC)‐derived dopaminergic neurons (DAn) generated by cell reprogramming of somatic skin cells from patients wit...

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Main Authors: Rubén Fernández‐Santiago, Iria Carballo‐Carbajal, Giancarlo Castellano, Roger Torrent, Yvonne Richaud, Adriana Sánchez‐Danés, Roser Vilarrasa‐Blasi, Alex Sánchez‐Pla, José Luis Mosquera, Jordi Soriano, José López‐Barneo, Josep M Canals, Jordi Alberch, Ángel Raya, Miquel Vila, Antonella Consiglio, José I Martín‐Subero, Mario Ezquerra, Eduardo Tolosa
Format: Article
Language:English
Published: Springer Nature 2015-10-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201505439
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author Rubén Fernández‐Santiago
Iria Carballo‐Carbajal
Giancarlo Castellano
Roger Torrent
Yvonne Richaud
Adriana Sánchez‐Danés
Roser Vilarrasa‐Blasi
Alex Sánchez‐Pla
José Luis Mosquera
Jordi Soriano
José López‐Barneo
Josep M Canals
Jordi Alberch
Ángel Raya
Miquel Vila
Antonella Consiglio
José I Martín‐Subero
Mario Ezquerra
Eduardo Tolosa
author_facet Rubén Fernández‐Santiago
Iria Carballo‐Carbajal
Giancarlo Castellano
Roger Torrent
Yvonne Richaud
Adriana Sánchez‐Danés
Roser Vilarrasa‐Blasi
Alex Sánchez‐Pla
José Luis Mosquera
Jordi Soriano
José López‐Barneo
Josep M Canals
Jordi Alberch
Ángel Raya
Miquel Vila
Antonella Consiglio
José I Martín‐Subero
Mario Ezquerra
Eduardo Tolosa
author_sort Rubén Fernández‐Santiago
collection DOAJ
description Abstract The epigenomic landscape of Parkinson's disease (PD) remains unknown. We performed a genomewide DNA methylation and a transcriptome studies in induced pluripotent stem cell (iPSC)‐derived dopaminergic neurons (DAn) generated by cell reprogramming of somatic skin cells from patients with monogenic LRRK2‐associated PD (L2PD) or sporadic PD (sPD), and healthy subjects. We observed extensive DNA methylation changes in PD DAn, and of RNA expression, which were common in L2PD and sPD. No significant methylation differences were present in parental skin cells, undifferentiated iPSCs nor iPSC‐derived neural cultures not‐enriched‐in‐DAn. These findings suggest the presence of molecular defects in PD somatic cells which manifest only upon differentiation into the DAn cells targeted in PD. The methylation profile from PD DAn, but not from controls, resembled that of neural cultures not‐enriched‐in‐DAn indicating a failure to fully acquire the epigenetic identity own to healthy DAn in PD. The PD‐associated hypermethylation was prominent in gene regulatory regions such as enhancers and was related to the RNA and/or protein downregulation of a network of transcription factors relevant to PD (FOXA1, NR3C1, HNF4A, and FOSL2). Using a patient‐specific iPSC‐based DAn model, our study provides the first evidence that epigenetic deregulation is associated with monogenic and sporadic PD.
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spelling doaj-art-007509ba6a4d4d19940a0fff72f98b852025-08-20T03:43:21ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842015-10-017121529154610.15252/emmm.201505439Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patientsRubén Fernández‐Santiago0Iria Carballo‐Carbajal1Giancarlo Castellano2Roger Torrent3Yvonne Richaud4Adriana Sánchez‐Danés5Roser Vilarrasa‐Blasi6Alex Sánchez‐Pla7José Luis Mosquera8Jordi Soriano9José López‐Barneo10Josep M Canals11Jordi Alberch12Ángel Raya13Miquel Vila14Antonella Consiglio15José I Martín‐Subero16Mario Ezquerra17Eduardo Tolosa18Laboratory of Neurodegenerative Disorders, Department of Neurology, Hospital Clínic of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona (UB)Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED)Department of Pathological Anatomy, Pharmacology and Microbiology, University of Barcelona (UB), Institut d'investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Institute for Biomedicine (IBUB), University of Barcelona (UB)Control of Stem Cell Potency Group, Institute for Bioengineering of Catalonia (IBEC)Institute for Biomedicine (IBUB), University of Barcelona (UB)Department of Pathological Anatomy, Pharmacology and Microbiology, University of Barcelona (UB), Institut d'investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Department of Statistics, University of Barcelona (UB)Department of Statistics, University of Barcelona (UB)Departament d'Estructura i Constituents de la Matèria (ECM), Facultat de Física, University of Barcelona (UB)Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED)Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED)Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED)Control of Stem Cell Potency Group, Institute for Bioengineering of Catalonia (IBEC)Centro de Investigación Biomédica en Red de Enfermedades Neurodegenerativas (CIBERNED)Institute for Biomedicine (IBUB), University of Barcelona (UB)Department of Pathological Anatomy, Pharmacology and Microbiology, University of Barcelona (UB), Institut d'investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)Laboratory of Neurodegenerative Disorders, Department of Neurology, Hospital Clínic of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona (UB)Laboratory of Neurodegenerative Disorders, Department of Neurology, Hospital Clínic of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), University of Barcelona (UB)Abstract The epigenomic landscape of Parkinson's disease (PD) remains unknown. We performed a genomewide DNA methylation and a transcriptome studies in induced pluripotent stem cell (iPSC)‐derived dopaminergic neurons (DAn) generated by cell reprogramming of somatic skin cells from patients with monogenic LRRK2‐associated PD (L2PD) or sporadic PD (sPD), and healthy subjects. We observed extensive DNA methylation changes in PD DAn, and of RNA expression, which were common in L2PD and sPD. No significant methylation differences were present in parental skin cells, undifferentiated iPSCs nor iPSC‐derived neural cultures not‐enriched‐in‐DAn. These findings suggest the presence of molecular defects in PD somatic cells which manifest only upon differentiation into the DAn cells targeted in PD. The methylation profile from PD DAn, but not from controls, resembled that of neural cultures not‐enriched‐in‐DAn indicating a failure to fully acquire the epigenetic identity own to healthy DAn in PD. The PD‐associated hypermethylation was prominent in gene regulatory regions such as enhancers and was related to the RNA and/or protein downregulation of a network of transcription factors relevant to PD (FOXA1, NR3C1, HNF4A, and FOSL2). Using a patient‐specific iPSC‐based DAn model, our study provides the first evidence that epigenetic deregulation is associated with monogenic and sporadic PD.https://doi.org/10.15252/emmm.201505439DNA methylationdopaminergic neuroninduced pluripotent stem cellParkinson's diseasetranscription factor
spellingShingle Rubén Fernández‐Santiago
Iria Carballo‐Carbajal
Giancarlo Castellano
Roger Torrent
Yvonne Richaud
Adriana Sánchez‐Danés
Roser Vilarrasa‐Blasi
Alex Sánchez‐Pla
José Luis Mosquera
Jordi Soriano
José López‐Barneo
Josep M Canals
Jordi Alberch
Ángel Raya
Miquel Vila
Antonella Consiglio
José I Martín‐Subero
Mario Ezquerra
Eduardo Tolosa
Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients
EMBO Molecular Medicine
DNA methylation
dopaminergic neuron
induced pluripotent stem cell
Parkinson's disease
transcription factor
title Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients
title_full Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients
title_fullStr Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients
title_full_unstemmed Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients
title_short Aberrant epigenome in iPSC‐derived dopaminergic neurons from Parkinson's disease patients
title_sort aberrant epigenome in ipsc derived dopaminergic neurons from parkinson s disease patients
topic DNA methylation
dopaminergic neuron
induced pluripotent stem cell
Parkinson's disease
transcription factor
url https://doi.org/10.15252/emmm.201505439
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