DNA methylation meta-analysis reveals cellular alterations in psychosis and markers of treatment-resistant schizophrenia.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
26 02 2021
Historique:
received: 01 05 2020
accepted: 23 02 2021
pubmed: 2 3 2021
medline: 29 1 2022
entrez: 1 3 2021
Statut: epublish

Résumé

We performed a systematic analysis of blood DNA methylation profiles from 4483 participants from seven independent cohorts identifying differentially methylated positions (DMPs) associated with psychosis, schizophrenia, and treatment-resistant schizophrenia. Psychosis cases were characterized by significant differences in measures of blood cell proportions and elevated smoking exposure derived from the DNA methylation data, with the largest differences seen in treatment-resistant schizophrenia patients. We implemented a stringent pipeline to meta-analyze epigenome-wide association study (EWAS) results across datasets, identifying 95 DMPs associated with psychosis and 1048 DMPs associated with schizophrenia, with evidence of colocalization to regions nominated by genetic association studies of disease. Many schizophrenia-associated DNA methylation differences were only present in patients with treatment-resistant schizophrenia, potentially reflecting exposure to the atypical antipsychotic clozapine. Our results highlight how DNA methylation data can be leveraged to identify physiological (e.g., differential cell counts) and environmental (e.g., smoking) factors associated with psychosis and molecular biomarkers of treatment-resistant schizophrenia.

Identifiants

pubmed: 33646943
doi: 10.7554/eLife.58430
pii: 58430
pmc: PMC8009672
doi:
pii:

Banques de données

GEO
['GSE147221', 'GSE80417', 'GSE84727']

Types de publication

Journal Article Meta-Analysis Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Medical Research Council
ID : MR/R005176/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0801418
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : R01 MH077139
Pays : United States
Organisme : Medical Research Council
ID : MR/L010305/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 085475/B/08/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0800509
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 072894/Z/03/Z
Pays : United Kingdom
Organisme : NIMH NIH HHS
ID : R01 MH052857
Pays : United States
Organisme : Medical Research Council
ID : MR/K013807/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 075491/Z/04/B
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/T007818/1
Pays : United Kingdom
Organisme : Department of Health
ID : RP-PG-0606-1049
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 090532/Z/09/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/L011794/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M008924/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : Fellowship (MR/M008436/1)
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 085475/Z/08/Z
Pays : United Kingdom

Informations de copyright

© 2021, Hannon et al.

Déclaration de conflit d'intérêts

EH, ED, GM, JB, NB, MB, AC, CC, DD, TD, GD, MG, AG, CG, HH, CH, VJ, RK, JK, GK, CM, AM, DM, KM, CM, IN, DQ, AR, BR, DS, ST, TT, JV, JW, EV, GB, LS, JM No competing interests declared, MD M Di Forti reports personal fees from Janssen, outside the submitted work. FG Fiona Gaughran has received honoraria from Lundbeck, Otsuka, and Sunovion. She has a family member with professional links to Lilly and GSK, including shares. KK Kaarina Kowalec has consulted with Emerald Lake Safety Ltd. (2017-2018) and has received speaker honoraria from Biogen/Fraser Health Multiple Sclerosis Clinic (2018). Both are unrelated to the work published here. JM James MacCabe has received research funding from H Lundbeck. MO Michael C O'Donovan is supported by a collaborative research grant from Takeda Pharmaceuticals. Takeda played no part in the conception, design, implementation, or interpretation of this study. PS PF Sullivan reports the following potentially competing financial interests. Current: Lundbeck (advisory committee, grant recipient). Past three years: Pfizer (scientific advisory board). DC David A Collier is a full time employee and stockholder of Eli Lilly and Company. RM Robin M Murray reports personal fees from Janssen, Lundbeck, Sunovion, Recordati and Otsuka

Références

Nature. 2008 Sep 11;455(7210):237-41
pubmed: 18668038
JAMA Psychiatry. 2016 May 1;73(5):506-14
pubmed: 27074206
Psychol Med. 2019 Jun;49(8):1378-1391
pubmed: 30282569
Lancet Psychiatry. 2015 Mar;2(3):233-8
pubmed: 26359901
PLoS Med. 2010 Oct 26;7(10):e1000356
pubmed: 21048988
Nature. 2014 Jul 24;511(7510):421-7
pubmed: 25056061
Nat Genet. 2018 Mar;50(3):381-389
pubmed: 29483656
Br J Psychiatry. 2019 Dec;215(6):712-719
pubmed: 31347480
Acta Psychiatr Scand. 2017 Jul;136(1):37-51
pubmed: 28502099
Lancet. 2013 Nov 9;382(9904):1575-86
pubmed: 23993280
Genome Biol. 2016 Aug 30;17(1):176
pubmed: 27572077
N Engl J Med. 1993 Jul 15;329(3):162-7
pubmed: 8515788
BMC Genomics. 2019 May 14;20(1):366
pubmed: 31088362
Genome Med. 2018 Mar 28;10(1):19
pubmed: 29587883
Lancet. 2014 Jun 7;383(9933):1952-4
pubmed: 24630775
BMC Bioinformatics. 2012 May 08;13:86
pubmed: 22568884
Nat Rev Genet. 2013 Aug;14(8):585-94
pubmed: 23817309
Mol Psychiatry. 2011 Mar;16(3):286-92
pubmed: 20157312
Hum Mol Genet. 2011 Dec 15;20(24):4786-96
pubmed: 21908516
Mol Brain. 2019 Jan 28;12(1):7
pubmed: 30691483
Nat Genet. 2011 Sep 18;43(10):977-83
pubmed: 21926972
Genome Biol. 2014;15(10):483
pubmed: 25347937
Aging (Albany NY). 2018 Apr 18;10(4):573-591
pubmed: 29676998
Clin Epigenetics. 2014 Feb 03;6(1):4
pubmed: 24485148
Arch Gen Psychiatry. 1991 Aug;48(8):764-70
pubmed: 1883262
Epigenetics. 2013 Aug;8(8):816-26
pubmed: 23903776
Schizophr Bull. 2020 Feb 26;46(2):363-373
pubmed: 31504969
Schizophr Bull. 2013 Jan;39(1):11-6
pubmed: 23211398
Am J Hum Genet. 2018 Nov 1;103(5):654-665
pubmed: 30401456
Mol Cell. 2013 Jan 24;49(2):359-367
pubmed: 23177740
Genome Biol. 2014 Feb 20;15(2):R37
pubmed: 24555846
Transl Psychiatry. 2019 Feb 15;9(1):92
pubmed: 30770782
Nat Genet. 2011 Sep 18;43(10):969-76
pubmed: 21926974
Am J Med Genet B Neuropsychiatr Genet. 2007 Mar 5;144B(2):129-58
pubmed: 17266109
J Clin Psychiatry. 2002 Sep;63(9):812-6
pubmed: 12363123
JAMA Psychiatry. 2014 Mar;71(3):255-64
pubmed: 24402055
Genome Biol. 2017 Jan 27;18(1):19
pubmed: 28129774
Nat Rev Genet. 2011 Jul 12;12(8):529-41
pubmed: 21747404
J Leukoc Biol. 2012 Nov;92(5):959-75
pubmed: 22875882
JAMA Psychiatry. 2018 Jan 1;75(1):36-46
pubmed: 29214289
Am J Hum Genet. 2011 Jan 7;88(1):76-82
pubmed: 21167468
Arch Gen Psychiatry. 2003 Dec;60(12):1187-92
pubmed: 14662550
JAMA Psychiatry. 2020 Jun 1;77(6):628-636
pubmed: 32049268
Transl Psychiatry. 2014 Jan 07;4:e339
pubmed: 24399042
Psychol Med. 2014 Jan;44(1):9-16
pubmed: 23244442
Nat Neurosci. 2016 Jan;19(1):48-54
pubmed: 26619357
Psychiatry Res. 2018 Feb;260:307-312
pubmed: 29223800
Hum Mol Genet. 2017 Jan 1;26(1):210-225
pubmed: 28011714
Mol Psychiatry. 2010 Jun;15(6):615-28
pubmed: 19048012
Mol Psychiatry. 2018 Nov;23(11):2133-2144
pubmed: 29311653
Biol Psychiatry. 2018 Mar 15;83(6):492-498
pubmed: 28987712
World J Biol Psychiatry. 2020 Jun;21(5):326-338
pubmed: 30806142
Arch Gen Psychiatry. 2003 Jun;60(6):565-71
pubmed: 12796219
Lancet. 2013 Apr 20;381(9875):1371-1379
pubmed: 23453885
Am J Hum Genet. 2017 Jun 1;100(6):954-959
pubmed: 28528868
Nature. 2009 Aug 6;460(7256):748-52
pubmed: 19571811
PLoS Genet. 2018 Aug 9;14(8):e1007544
pubmed: 30091980
Schizophr Res. 2018 Jul;197:294-297
pubmed: 29472163
Science. 2012 Sep 7;337(6099):1190-5
pubmed: 22955828
Psychiatry Res. 2011 Oct 30;189(3):478-9
pubmed: 21367462
Epigenetics. 2015;10(11):1024-32
pubmed: 26457534
Schizophr Res. 2005 Jul 15;76(2-3):135-57
pubmed: 15949648
Schizophr Res. 2019 Apr;206:4-12
pubmed: 30573407
Early Interv Psychiatry. 2019 Feb;13(1):95-100
pubmed: 28786532
Am J Public Health. 2010 Dec;100(12):2464-72
pubmed: 20966369
Genome Med. 2019 Aug 23;11(1):54
pubmed: 31443728
Hum Mol Genet. 2014 Jun 15;23(12):3316-26
pubmed: 24474471
Philos Trans R Soc Lond B Biol Sci. 2019 Apr 15;374(1770):20180120
pubmed: 30966880
Genome Biol. 2013;14(10):R115
pubmed: 24138928
Schizophr Bull. 2019 Jun 18;45(4):846-858
pubmed: 30107610
Transl Psychiatry. 2019 Jun 4;9(1):157
pubmed: 31164630
Nat Neurosci. 2016 Jan;19(1):40-7
pubmed: 26619358
Nature. 2010 Jul 8;466(7303):253-7
pubmed: 20613842
Br J Psychiatry. 2009 Dec;195(6):488-91
pubmed: 19949195
Int Clin Psychopharmacol. 2014 Mar;29(2):63-76
pubmed: 23995856
Neuromolecular Med. 2014 Dec;16(4):697-703
pubmed: 25052007
J Clin Psychiatry. 2012 Apr;73(4):468-75
pubmed: 22579146
BMC Genomics. 2013 May 01;14:293
pubmed: 23631413
Neuropharmacology. 2012 Mar;62(3):1584-97
pubmed: 21856318

Auteurs

Eilis Hannon (E)

University of Exeter Medical School, University of Exeter, Barrack Road, Exeter, United Kingdom.

Emma L Dempster (EL)

University of Exeter Medical School, University of Exeter, Barrack Road, Exeter, United Kingdom.

Georgina Mansell (G)

University of Exeter Medical School, University of Exeter, Barrack Road, Exeter, United Kingdom.

Joe Burrage (J)

University of Exeter Medical School, University of Exeter, Barrack Road, Exeter, United Kingdom.

Nick Bass (N)

Division of Psychiatry, University College London, London, United Kingdom.

Marc M Bohlken (MM)

Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Heidelberglaan, Utrecht, Netherlands.

Aiden Corvin (A)

Department of Psychiatry and Neuropsychiatric Genetics Research Group, Trinity Translational Medicine Institute, Trinity College Dublin, St. James Hospital, Dublin, Ireland.

Charles J Curtis (CJ)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
NIHR BioResource Centre Maudsley, South London and Maudsley NHS Foundation Trust (SLaM), King's College London, London, United Kingdom.

David Dempster (D)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.

Marta Di Forti (M)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
South London and Maudsley NHS Mental Health Foundation Trust, London, United Kingdom.
National Institute for Health Research (NIHR), Mental Health Biomedical Research Centre, South London and Maudsley NHS Foundation Trust and King's College London, London, United Kingdom.

Timothy G Dinan (TG)

APC Microbiome Ireland, University College Cork, Cork, Ireland.

Gary Donohoe (G)

Centre for Neuroimaging and Cognitive Genomics (NICOG), School of Psychology and Discipline of Biochemistry, National University of Ireland Galway, Galway, Ireland.

Fiona Gaughran (F)

Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
National Psychosis Service, South London and Maudsley NHS Foundation Trust, London, United Kingdom.

Michael Gill (M)

Department of Psychiatry and Neuropsychiatric Genetics Research Group, Trinity Translational Medicine Institute, Trinity College Dublin, Dublin, Ireland.

Amy Gillespie (A)

Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
Department of Psychiatry, Medical Sciences Division, University of Oxford, Oxford, United Kingdom.

Cerisse Gunasinghe (C)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.

Hilleke E Hulshoff (HE)

Department of Psychiatry, University Medical Center Utrecht, Utrecht, Netherlands.

Christina M Hultman (CM)

Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.

Viktoria Johansson (V)

Department of Medical Epidemiology and Biostatistics Sweden, Karolinska Institutet, Stockholm, Sweden.
Department of Clinical Neuroscience, Center for Psychiatry Research, Karolinska Institutet and Stockholm Health Care Services, Stockholm, Sweden.

René S Kahn (RS)

Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, Netherlands.
Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, United States.

Jaakko Kaprio (J)

Institute for Molecular Medicine FIMM, University of Helsinki, Helsinki, Finland.
Department of Public Health, University of Helsinki, Helsinki, Finland.

Gunter Kenis (G)

Faculty of Health, Medicine and Life Sciences, Maastricht University, Maastricht, Netherlands.

Kaarina Kowalec (K)

Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
College of Pharmacy, University of Manitoba, Winnipeg, Canada.

James MacCabe (J)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.

Colm McDonald (C)

Centre for Neuroimaging and Cognitive Genomics (NICOG), School of Medicine, National University of Ireland Galway, Galway, Ireland.

Andrew McQuillin (A)

Division of Psychiatry, University College London, London, United Kingdom.
Division of Psychiatry, University College London, London, United Kingdom.

Derek W Morris (DW)

Centre for Neuroimaging and Cognitive Genomics (NICOG), School of Psychology and Discipline of Biochemistry, National University of Ireland Galway, Galway, Ireland.

Kieran C Murphy (KC)

Department of Psychiatry, Royal College of Surgeons in Ireland, Dublin, Ireland.

Colette J Mustard (CJ)

Division of Biomedical Sciences, Institute of Health Research and Innovation, University of the Highlands and Islands, Inverness, United Kingdom.

Igor Nenadic (I)

Department of Psychiatry and Psychotherapy, Jena University Hospital, Jena, Germany.
Department of Psychiatry and Psychotherapy, Philipps University Marburg/ Marburg University Hospital UKGM, Marburg, Germany.

Michael C O'Donovan (MC)

MRC Centre for Neuropsychiatric Genetics and Genomics, School of Medicine, Cardiff University, Cardiff, United Kingdom.

Diego Quattrone (D)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
South London and Maudsley NHS Mental Health Foundation Trust, London, United Kingdom.

Alexander L Richards (AL)

MRC Centre for Neuropsychiatric Genetics and Genomics, School of Medicine, Cardiff University, Cardiff, United Kingdom.

Bart Pf Rutten (BP)

Department of Psychiatry and Neuropsychology, Faculty of Health, Medicine and Life Sciences, Maastricht University, Maastricht, Netherlands.

David St Clair (D)

The Institute of Medical Sciences, Univeristy of Aberdeen, Aberdeen, United Kingdom.

Sebastian Therman (S)

Department of Public Health Solutions, Mental Health Unit, National Institute for Health and Welfare, Helsinki, Finland.

Timothea Toulopoulou (T)

Department of Psychology and National Magnetic Resonance Research Center (UMRAM), Aysel Sabuncu Brain Research Centre (ASBAM), Bilkent University, Ankara, Turkey.

Jim Van Os (J)

Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, Netherlands.

John L Waddington (JL)

Molecular and Cellular Therapeutics, Royal College of Surgeons in Ireland, Dublin, Ireland.

Patrick Sullivan (P)

Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
Departments of Genetics and Psychiatry, University of North Carolina at Chapel Hill, Chapel Hill, United States.

Evangelos Vassos (E)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.

Gerome Breen (G)

Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom.
NIHR BioResource Centre Maudsley, South London and Maudsley NHS Foundation Trust (SLaM), King's College London, London, United Kingdom.

David Andrew Collier (DA)

Neuroscience Genetics, Eli Lilly and Company, Surrey, United Kingdom.

Robin M Murray (RM)

Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, United Kingdom.

Leonard S Schalkwyk (LS)

School of Life Sciences, University of Essex, Colchester, United Kingdom.

Jonathan Mill (J)

University of Exeter Medical School, University of Exeter, Barrack Road, Exeter, United Kingdom.

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