Chromatin domain alterations linked to 3D genome organization in a large cohort of schizophrenia and bipolar disorder brains

Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-en...

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Published in	Nature neuroscience Vol. 25; no. 4; pp. 474 - 483
Main Authors	Girdhar, Kiran, Hoffman, Gabriel E., Bendl, Jaroslav, Rahman, Samir, Dong, Pengfei, Liao, Will, Hauberg, Mads E., Sloofman, Laura, Brown, Leanne, Devillers, Olivia, Kassim, Bibi S., Wiseman, Jennifer R., Park, Royce, Zharovsky, Elizabeth, Jacobov, Rivky, Flatow, Elie, Kozlenkov, Alexey, Gilgenast, Thomas, Johnson, Jessica S., Couto, Lizette, Peters, Mette A., Phillips-Cremins, Jennifer E., Hahn, Chang-Gyu, Gur, Raquel E., Tamminga, Carol A., Lewis, David A., Haroutunian, Vahram, Dracheva, Stella, Lipska, Barbara K., Marenco, Stefano, Kundakovic, Marija, Fullard, John F., Jiang, Yan, Roussos, Panos, Akbarian, Schahram
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.04.2022 Nature Publishing Group
Subjects	631/114/1314 631/208/177 631/378/1689/1333 692/699/476/1799 Acetylation Adult Animal Genetics and Genomics Behavioral Sciences Biological Techniques Biomedical and Life Sciences Biomedicine Bipolar disorder Bipolar Disorder - genetics Brain Chromatin Domains Fetuses Gene mapping Glutamatergic transmission Heritability Histones Humans Lysine Lysine - genetics Mental disorders Methylation Neurobiology Neurosciences Prefrontal cortex Regulatory sequences Schizophrenia Schizophrenia - genetics Transcription
Online Access	Get full text
ISSN	1097-6256 1546-1726 1546-1726
DOI	10.1038/s41593-022-01032-6

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Abstract	Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-enriched nucleosomal histone modification landscapes for adult prefrontal cortex from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from 388 controls and 351 individuals diagnosed with schizophrenia (SCZ) or bipolar disorder (BD) ( n = 739). We mapped thousands of cis -regulatory domains (CRDs), revealing fine-grained, 10 4 –10 6 -bp chromosomal organization, firmly integrated into Hi-C topologically associating domain stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyper-acetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilobase- to megabase-scaling chromosomal domains. Girdhar et al. constructed chromosomal domains from prefrontal histone acetylation and methylation maps and discovered, in a large cohort of schizophrenia and bipolar brains, converging alignment by genetic risk, neuronal function and three-dimensional genomics.
AbstractList	Chromosomal organization, scaling from the 147 base pair nucleosome to megabase-ranging domains encompassing multiple transcriptional units including heritability loci for psychiatric traits, remains largely unexplored in the human brain. Here, we construct promoter and enhancer enriched nucleosomal histone modification landscapes for adult prefrontal cortex (PFC) from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from (n=739) 388 controls and 351 subjects diagnosed with schizophrenia (SCZ) or bipolar disorder (BD). We mapped thousands of cis-regulatory domains (CRDs), revealing fine-grained, 10 4 -10 6 bp chromosomal organization, firmly integrated into Hi-C topologically associating domain (TAD) stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyperacetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilo- to megabase-scaling chromosomal domains. Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-enriched nucleosomal histone modification landscapes for adult prefrontal cortex from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from 388 controls and 351 individuals diagnosed with schizophrenia (SCZ) or bipolar disorder (BD) (n = 739). We mapped thousands of cis-regulatory domains (CRDs), revealing fine-grained, 104–106-bp chromosomal organization, firmly integrated into Hi-C topologically associating domain stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyper-acetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilobase- to megabase-scaling chromosomal domains.Girdhar et al. constructed chromosomal domains from prefrontal histone acetylation and methylation maps and discovered, in a large cohort of schizophrenia and bipolar brains, converging alignment by genetic risk, neuronal function and three-dimensional genomics. Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-enriched nucleosomal histone modification landscapes for adult prefrontal cortex from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from 388 controls and 351 individuals diagnosed with schizophrenia (SCZ) or bipolar disorder (BD) ( n = 739). We mapped thousands of cis -regulatory domains (CRDs), revealing fine-grained, 10 4 –10 6 -bp chromosomal organization, firmly integrated into Hi-C topologically associating domain stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyper-acetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilobase- to megabase-scaling chromosomal domains. Girdhar et al. constructed chromosomal domains from prefrontal histone acetylation and methylation maps and discovered, in a large cohort of schizophrenia and bipolar brains, converging alignment by genetic risk, neuronal function and three-dimensional genomics. Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-enriched nucleosomal histone modification landscapes for adult prefrontal cortex from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from 388 controls and 351 individuals diagnosed with schizophrenia (SCZ) or bipolar disorder (BD) (n = 739). We mapped thousands of cis-regulatory domains (CRDs), revealing fine-grained, 104-106-bp chromosomal organization, firmly integrated into Hi-C topologically associating domain stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyper-acetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilobase- to megabase-scaling chromosomal domains.Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-enriched nucleosomal histone modification landscapes for adult prefrontal cortex from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from 388 controls and 351 individuals diagnosed with schizophrenia (SCZ) or bipolar disorder (BD) (n = 739). We mapped thousands of cis-regulatory domains (CRDs), revealing fine-grained, 104-106-bp chromosomal organization, firmly integrated into Hi-C topologically associating domain stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyper-acetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilobase- to megabase-scaling chromosomal domains. Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including heritability loci for psychiatric traits, remains largely unexplored in the human brain. In this study, we constructed promoter- and enhancer-enriched nucleosomal histone modification landscapes for adult prefrontal cortex from H3-lysine 27 acetylation and H3-lysine 4 trimethylation profiles, generated from 388 controls and 351 individuals diagnosed with schizophrenia (SCZ) or bipolar disorder (BD) (n = 739). We mapped thousands of cis-regulatory domains (CRDs), revealing fine-grained, 10 -10 -bp chromosomal organization, firmly integrated into Hi-C topologically associating domain stratification by open/repressive chromosomal environments and nuclear topography. Large clusters of hyper-acetylated CRDs were enriched for SCZ heritability, with prominent representation of regulatory sequences governing fetal development and glutamatergic neuron signaling. Therefore, SCZ and BD brains show coordinated dysregulation of risk-associated regulatory sequences assembled into kilobase- to megabase-scaling chromosomal domains.
Author	Rahman, Samir Kundakovic, Marija Lewis, David A. Zharovsky, Elizabeth Brown, Leanne Jacobov, Rivky Tamminga, Carol A. Marenco, Stefano Dracheva, Stella Hauberg, Mads E. Devillers, Olivia Akbarian, Schahram Girdhar, Kiran Bendl, Jaroslav Kozlenkov, Alexey Johnson, Jessica S. Phillips-Cremins, Jennifer E. Flatow, Elie Haroutunian, Vahram Jiang, Yan Couto, Lizette Wiseman, Jennifer R. Gilgenast, Thomas Lipska, Barbara K. Fullard, John F. Hoffman, Gabriel E. Sloofman, Laura Park, Royce Roussos, Panos Kassim, Bibi S. Peters, Mette A. Gur, Raquel E. Liao, Will Hahn, Chang-Gyu Dong, Pengfei
AuthorAffiliation	20 iPSYCH, The Lundbeck Foundation Initiative for Integrative Psychiatric Research, Aarhus, Denmark 11 Sage Bionetworks, Seattle, Washington 98121, USA 9 Department of Biological Sciences, Fordham University, Bronx, NY 10458, USA 13 Mental Illness Research Education and Clinical Center (MIRECC), James J. Peters VA Medical Center, Bronx, New York, 10468, USA 6 Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 17 Department of Bioengineering, University of Pennsylvania, Philadelphia, PA 19104, USA 3 Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 15 Jefferson University, Philadelphia, PA 19107, USA 7 Seaver Autism Center for Research and Treatment, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 14 Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science, Fudan University, 200032, Shanghai, China 4 Departme
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ContentType	Journal Article
Copyright	The Author(s), under exclusive licence to Springer Nature America, Inc. 2022 2022. The Author(s), under exclusive licence to Springer Nature America, Inc. The Author(s), under exclusive licence to Springer Nature America, Inc. 2022.
Copyright_xml	– notice: The Author(s), under exclusive licence to Springer Nature America, Inc. 2022 – notice: 2022. The Author(s), under exclusive licence to Springer Nature America, Inc. – notice: The Author(s), under exclusive licence to Springer Nature America, Inc. 2022.
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 List of PsychENCODE consortium authors is provided in the appendix Wet lab work including tissue processing, sorting of nuclei and ChIP-seq and Hi-C library generation: Y.J., L.B., M.K., E.Z., R.J., J.R.W., R.P., B.S.K., L.C., O.D., S.R., J.F., E.F., A.K. Data processing and coordination: Y.J., M.K.,M.A.P., J.S.J. Bioinformatics and computational genomics: KG., G.E.H., J.B., S.R., T.G., J.P.-C., P.D., W.L., M.E.H., L.S., L.C. Provision of brain tissue and resources: C.A.T., S.M.,, B.K.L., D.A.L., V.H. , C.-G. H., R.E.G., S.D., P.C. Conception of study and design: P.R., S.A., K.G., G.E.H., J.B. Writing of the paper: K.G., S.A., P.R. Authors Contributions Statement Equally contributing senior authors.
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Snippet	Chromosomal organization, scaling from the 147-base pair (bp) nucleosome to megabase-ranging domains encompassing multiple transcriptional units, including... Chromosomal organization, scaling from the 147 base pair nucleosome to megabase-ranging domains encompassing multiple transcriptional units including...
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SubjectTerms	631/114/1314 631/208/177 631/378/1689/1333 692/699/476/1799 Acetylation Adult Animal Genetics and Genomics Behavioral Sciences Biological Techniques Biomedical and Life Sciences Biomedicine Bipolar disorder Bipolar Disorder - genetics Brain Chromatin Domains Fetuses Gene mapping Glutamatergic transmission Heritability Histones Humans Lysine Lysine - genetics Mental disorders Methylation Neurobiology Neurosciences Prefrontal cortex Regulatory sequences Schizophrenia Schizophrenia - genetics Transcription
Title	Chromatin domain alterations linked to 3D genome organization in a large cohort of schizophrenia and bipolar disorder brains
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