DNA methylation atlas of the mouse brain at single-cell resolution

Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive heterogeneity is poorly understood. Here we carry out a comprehensive assessment of the epigenomes of mouse brain cell types by applying single-nucleus...

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Published in:	Nature (London) Vol. 598; no. 7879; pp. 120 - 128
Main Authors:	Liu, Hanqing, Zhou, Jingtian, Tian, Wei, Luo, Chongyuan, Bartlett, Anna, Aldridge, Andrew, Lucero, Jacinta, Osteen, Julia K., Nery, Joseph R., Chen, Huaming, Rivkin, Angeline, Castanon, Rosa G., Clock, Ben, Li, Yang Eric, Hou, Xiaomeng, Poirion, Olivier B., Preissl, Sebastian, Pinto-Duarte, Antonio, O’Connor, Carolyn, Boggeman, Lara, Fitzpatrick, Conor, Nunn, Michael, Mukamel, Eran A., Zhang, Zhuzhu, Callaway, Edward M., Ren, Bing, Dixon, Jesse R., Behrens, M. Margarita, Ecker, Joseph R.
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 07-10-2021 Nature Publishing Group
Subjects:	631/208/177 631/337/176/1988 631/378/2584 631/378/87 631/61/212/177 Animals Artificial neural networks Atlases as Topic Brain Brain - cytology Brain - metabolism Cerebrum Chromatin Chromatin - chemistry Chromatin - genetics Chromatin - metabolism Conformation Cytosine - chemistry Cytosine - metabolism Datasets Datasets as Topic Dentate Gyrus - cytology Deoxyribonucleic acid DNA DNA Methylation Enhancer Elements, Genetic - genetics Epigenetics Epigenome Epigenomics Forecasting Gene expression Gene Expression Profiling Genomes Globus pallidus Heterogeneity Hippocampus Hippocampus - cytology Hippocampus - metabolism Humanities and Social Sciences Male Mice Mice, Inbred C57BL Models, Biological multidisciplinary Neostriatum Neural networks Neural Pathways Neurons Neurons - classification Neurons - cytology Neurons - metabolism Nuclei (cytology) Regulatory sequences Science Science (multidisciplinary) Single-Cell Analysis Taxonomy Transcription factors
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Abstract	Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive heterogeneity is poorly understood. Here we carry out a comprehensive assessment of the epigenomes of mouse brain cell types by applying single-nucleus DNA methylation sequencing 1 , 2 to profile 103,982 nuclei (including 95,815 neurons and 8,167 non-neuronal cells) from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas. We identified 161 cell clusters with distinct spatial locations and projection targets. We constructed taxonomies of these epigenetic types, annotated with signature genes, regulatory elements and transcription factors. These features indicate the potential regulatory landscape supporting the assignment of putative cell types and reveal repetitive usage of regulators in excitatory and inhibitory cells for determining subtypes. The DNA methylation landscape of excitatory neurons in the cortex and hippocampus varied continuously along spatial gradients. Using this deep dataset, we constructed an artificial neural network model that precisely predicts single neuron cell-type identity and brain area spatial location. Integration of high-resolution DNA methylomes with single-nucleus chromatin accessibility data 3 enabled prediction of high-confidence enhancer–gene interactions for all identified cell types, which were subsequently validated by cell-type-specific chromatin conformation capture experiments 4 . By combining multi-omic datasets (DNA methylation, chromatin contacts, and open chromatin) from single nuclei and annotating the regulatory genome of hundreds of cell types in the mouse brain, our DNA methylation atlas establishes the epigenetic basis for neuronal diversity and spatial organization throughout the mouse cerebrum. A comprehensive survey of the epigenome from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas using single-nucleus DNA methylation sequencing enables identification of 161 cell clusters with distinct locations and projection targets and provides insights into the regulatory landscape underlying neuronal diversity and spatial regulation.
AbstractList	Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive heterogeneity is poorly understood. Here we carry out a comprehensive assessment of the epigenomes of mouse brain cell types by applying single-nucleus DNA methylation sequencing to profile 103,982 nuclei (including 95,815 neurons and 8,167 non-neuronal cells) from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas. We identified 161 cell clusters with distinct spatial locations and projection targets. We constructed taxonomies of these epigenetic types, annotated with signature genes, regulatory elements and transcription factors. These features indicate the potential regulatory landscape supporting the assignment of putative cell types and reveal repetitive usage of regulators in excitatory and inhibitory cells for determining subtypes. The DNA methylation landscape of excitatory neurons in the cortex and hippocampus varied continuously along spatial gradients. Using this deep dataset, we constructed an artificial neural network model that precisely predicts single neuron cell-type identity and brain area spatial location. Integration of high-resolution DNA methylomes with single-nucleus chromatin accessibility data enabled prediction of high-confidence enhancer-gene interactions for all identified cell types, which were subsequently validated by cell-type-specific chromatin conformation capture experiments . By combining multi-omic datasets (DNA methylation, chromatin contacts, and open chromatin) from single nuclei and annotating the regulatory genome of hundreds of cell types in the mouse brain, our DNA methylation atlas establishes the epigenetic basis for neuronal diversity and spatial organization throughout the mouse cerebrum. Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive heterogeneity is poorly understood. Here we carry out a comprehensive assessment of the epigenomes of mouse brain cell types by applying single-nucleus DNA methylation sequencing 1 , 2 to profile 103,982 nuclei (including 95,815 neurons and 8,167 non-neuronal cells) from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas. We identified 161 cell clusters with distinct spatial locations and projection targets. We constructed taxonomies of these epigenetic types, annotated with signature genes, regulatory elements and transcription factors. These features indicate the potential regulatory landscape supporting the assignment of putative cell types and reveal repetitive usage of regulators in excitatory and inhibitory cells for determining subtypes. The DNA methylation landscape of excitatory neurons in the cortex and hippocampus varied continuously along spatial gradients. Using this deep dataset, we constructed an artificial neural network model that precisely predicts single neuron cell-type identity and brain area spatial location. Integration of high-resolution DNA methylomes with single-nucleus chromatin accessibility data 3 enabled prediction of high-confidence enhancer–gene interactions for all identified cell types, which were subsequently validated by cell-type-specific chromatin conformation capture experiments 4 . By combining multi-omic datasets (DNA methylation, chromatin contacts, and open chromatin) from single nuclei and annotating the regulatory genome of hundreds of cell types in the mouse brain, our DNA methylation atlas establishes the epigenetic basis for neuronal diversity and spatial organization throughout the mouse cerebrum. A comprehensive survey of the epigenome from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas using single-nucleus DNA methylation sequencing enables identification of 161 cell clusters with distinct locations and projection targets and provides insights into the regulatory landscape underlying neuronal diversity and spatial regulation. Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive heterogeneity is poorly understood. Here we carry out a comprehensive assessment of the epigenomes of mouse brain cell types by applying single-nucleus DNA methylation sequencing1,2 to profile 103,982 nuclei (including 95,815 neurons and 8,167 non-neuronal cells) from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas. We identified 161 cell clusters with distinct spatial locations and projection targets. We constructed taxonomies of these epigenetic types, annotated with signature genes, regulatory elements and transcription factors. These features indicate the potential regulatory landscape supporting the assignment of putative cell types and reveal repetitive usage of regulators in excitatory and inhibitory cells for determining subtypes. The DNA methylation landscape of excitatory neurons in the cortex and hippocampus varied continuously along spatial gradients. Using this deep dataset, we constructed an artificial neural network model that precisely predicts single neuron cell-type identity and brain area spatial location. Integration of high-resolution DNA methylomes with single-nucleus chromatin accessibility data3 enabled prediction of high-confidence enhancer-gene interactions for all identified cell types, which were subsequently validated by cell-type-specific chromatin conformation capture experiments4. By combining multi-omic datasets (DNA methylation, chromatin contacts, and open chromatin) from single nuclei and annotating the regulatory genome of hundreds of cell types in the mouse brain, our DNA methylation atlas establishes the epigenetic basis for neuronal diversity and spatial organization throughout the mouse cerebrum. Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive heterogeneity is poorly understood. Here we carry out a comprehensive assessment of the epigenomes of mouse brain cell types by applying single-nucleus DNA methylation sequencing 1,2 to profile 103,982 nuclei (including 95,815 neurons and 8,167 non-neuronal cells) from 45 regions of the mouse cortex, hippocampus, striatum, pallidum and olfactory areas. We identified 161 cell clusters with distinct spatial locations and projection targets. We constructed taxonomies of these epigenetic types, annotated with signature genes, regulatory elements and transcription factors. These features indicate the potential regulatory landscape supporting the assignment of putative cell types and reveal repetitive usage of regulators in excitatory and inhibitory cells for determining subtypes. The DNA methylation landscape of excitatory neurons in the cortex and hippocampus varied continuously along spatial gradients. Using this deep dataset, we constructed an artificial neural network model that precisely predicts single neuron cell-type identity and brain area spatial location. Integration of high-resolution DNA methylomes with single-nucleus chromatin accessibility data 3 enabled prediction of high-confidence enhancer–gene interactions for all identified cell types, which were subsequently validated by cell-type-specific chromatin conformation capture experiments 4 . By combining multi-omic datasets (DNA methylation, chromatin contacts, and open chromatin) from single nuclei and annotating the regulatory genome of hundreds of cell types in the mouse brain, our DNA methylation atlas establishes the epigenetic basis for neuronal diversity and spatial organization throughout the mouse cerebrum.
Author	Osteen, Julia K. Behrens, M. Margarita Boggeman, Lara Hou, Xiaomeng Bartlett, Anna Lucero, Jacinta Castanon, Rosa G. Liu, Hanqing Clock, Ben Chen, Huaming O’Connor, Carolyn Rivkin, Angeline Li, Yang Eric Nunn, Michael Preissl, Sebastian Callaway, Edward M. Ren, Bing Dixon, Jesse R. Nery, Joseph R. Zhou, Jingtian Aldridge, Andrew Mukamel, Eran A. Ecker, Joseph R. Tian, Wei Fitzpatrick, Conor Zhang, Zhuzhu Poirion, Olivier B. Pinto-Duarte, Antonio Luo, Chongyuan
Author_xml	– sequence: 1 givenname: Hanqing surname: Liu fullname: Liu, Hanqing organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies, Division of Biological Sciences, University of California, San Diego – sequence: 2 givenname: Jingtian orcidid: 0000-0003-2060-1922 surname: Zhou fullname: Zhou, Jingtian organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies, Bioinformatics and Systems Biology Program, University of California, San Diego – sequence: 3 givenname: Wei surname: Tian fullname: Tian, Wei organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 4 givenname: Chongyuan surname: Luo fullname: Luo, Chongyuan organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies, Department of Human Genetics, University of California Los Angeles – sequence: 5 givenname: Anna surname: Bartlett fullname: Bartlett, Anna organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 6 givenname: Andrew orcidid: 0000-0003-1962-8802 surname: Aldridge fullname: Aldridge, Andrew organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 7 givenname: Jacinta surname: Lucero fullname: Lucero, Jacinta organization: Computational Neurobiology Laboratory, The Salk Institute for Biological Studies – sequence: 8 givenname: Julia K. surname: Osteen fullname: Osteen, Julia K. organization: Computational Neurobiology Laboratory, The Salk Institute for Biological Studies – sequence: 9 givenname: Joseph R. orcidid: 0000-0003-0153-5659 surname: Nery fullname: Nery, Joseph R. organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 10 givenname: Huaming surname: Chen fullname: Chen, Huaming organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 11 givenname: Angeline surname: Rivkin fullname: Rivkin, Angeline organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 12 givenname: Rosa G. surname: Castanon fullname: Castanon, Rosa G. organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 13 givenname: Ben surname: Clock fullname: Clock, Ben organization: Peptide Biology Laboratory, The Salk Institute for Biological Studies – sequence: 14 givenname: Yang Eric orcidid: 0000-0001-6997-6018 surname: Li fullname: Li, Yang Eric organization: Ludwig Institute for Cancer Research – sequence: 15 givenname: Xiaomeng surname: Hou fullname: Hou, Xiaomeng organization: Center for Epigenomics, University of California, San Diego School of Medicine, Department of Cellular and Molecular Medicine, University of California, San Diego School of Medicine, Institute of Genomic Medicine, University of California, San Diego School of Medicine, Moores Cancer Center, University of California, San Diego School of Medicine – sequence: 16 givenname: Olivier B. surname: Poirion fullname: Poirion, Olivier B. organization: Center for Epigenomics, University of California, San Diego School of Medicine, Department of Cellular and Molecular Medicine, University of California, San Diego School of Medicine, Institute of Genomic Medicine, University of California, San Diego School of Medicine, Moores Cancer Center, University of California, San Diego School of Medicine – sequence: 17 givenname: Sebastian surname: Preissl fullname: Preissl, Sebastian organization: Center for Epigenomics, University of California, San Diego School of Medicine, Department of Cellular and Molecular Medicine, University of California, San Diego School of Medicine, Institute of Genomic Medicine, University of California, San Diego School of Medicine, Moores Cancer Center, University of California, San Diego School of Medicine – sequence: 18 givenname: Antonio orcidid: 0000-0002-2215-7653 surname: Pinto-Duarte fullname: Pinto-Duarte, Antonio organization: Computational Neurobiology Laboratory, The Salk Institute for Biological Studies – sequence: 19 givenname: Carolyn surname: O’Connor fullname: O’Connor, Carolyn organization: Flow Cytometry Core Facility, The Salk Institute for Biological Studies – sequence: 20 givenname: Lara surname: Boggeman fullname: Boggeman, Lara organization: Flow Cytometry Core Facility, The Salk Institute for Biological Studies – sequence: 21 givenname: Conor surname: Fitzpatrick fullname: Fitzpatrick, Conor organization: Flow Cytometry Core Facility, The Salk Institute for Biological Studies – sequence: 22 givenname: Michael surname: Nunn fullname: Nunn, Michael organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 23 givenname: Eran A. orcidid: 0000-0003-3203-9535 surname: Mukamel fullname: Mukamel, Eran A. organization: Department of Cognitive Science, University of California, San Diego – sequence: 24 givenname: Zhuzhu surname: Zhang fullname: Zhang, Zhuzhu organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies – sequence: 25 givenname: Edward M. orcidid: 0000-0002-6366-5267 surname: Callaway fullname: Callaway, Edward M. organization: Systems Neurobiology Laboratories, The Salk Institute for Biological Studies – sequence: 26 givenname: Bing orcidid: 0000-0002-5435-1127 surname: Ren fullname: Ren, Bing organization: Ludwig Institute for Cancer Research, Center for Epigenomics, University of California, San Diego School of Medicine, Department of Cellular and Molecular Medicine, University of California, San Diego School of Medicine, Institute of Genomic Medicine, University of California, San Diego School of Medicine, Moores Cancer Center, University of California, San Diego School of Medicine – sequence: 27 givenname: Jesse R. orcidid: 0000-0002-6273-2181 surname: Dixon fullname: Dixon, Jesse R. organization: Peptide Biology Laboratory, The Salk Institute for Biological Studies – sequence: 28 givenname: M. Margarita orcidid: 0000-0002-7168-8186 surname: Behrens fullname: Behrens, M. Margarita organization: Computational Neurobiology Laboratory, The Salk Institute for Biological Studies – sequence: 29 givenname: Joseph R. orcidid: 0000-0001-5799-5895 surname: Ecker fullname: Ecker, Joseph R. email: ecker@salk.edu organization: Genomic Analysis Laboratory, The Salk Institute for Biological Studies, Howard Hughes Medical Institute, The Salk Institute for Biological Studies
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/34616061$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	The Author(s) 2021 2021. The Author(s). Copyright Nature Publishing Group Oct 7, 2021
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Snippet	Mammalian brain cells show remarkable diversity in gene expression, anatomy and function, yet the regulatory DNA landscape underlying this extensive...
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SubjectTerms	631/208/177 631/337/176/1988 631/378/2584 631/378/87 631/61/212/177 Animals Artificial neural networks Atlases as Topic Brain Brain - cytology Brain - metabolism Cerebrum Chromatin Chromatin - chemistry Chromatin - genetics Chromatin - metabolism Conformation Cytosine - chemistry Cytosine - metabolism Datasets Datasets as Topic Dentate Gyrus - cytology Deoxyribonucleic acid DNA DNA Methylation Enhancer Elements, Genetic - genetics Epigenetics Epigenome Epigenomics Forecasting Gene expression Gene Expression Profiling Genomes Globus pallidus Heterogeneity Hippocampus Hippocampus - cytology Hippocampus - metabolism Humanities and Social Sciences Male Mice Mice, Inbred C57BL Models, Biological multidisciplinary Neostriatum Neural networks Neural Pathways Neurons Neurons - classification Neurons - cytology Neurons - metabolism Nuclei (cytology) Regulatory sequences Science Science (multidisciplinary) Single-Cell Analysis Taxonomy Transcription factors
Title	DNA methylation atlas of the mouse brain at single-cell resolution
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