Spatiotemporal transcriptomic divergence across human and macaque brain development
Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative a...
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| Published in | Science (American Association for the Advancement of Science) Vol. 362; no. 6420 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
14.12.2018
American Association for the Advancement of Science (AAAS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders. |
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| AbstractList | INTRODUCTIONImproved understanding of how the developing human nervous system differs from that of closely related nonhuman primates is fundamental for teasing out human-specific aspects of behavior, cognition, and disorders.RATIONALEThe shared and unique functional properties of the human nervous system are rooted in the complex transcriptional programs governing the development of distinct cell types, neural circuits, and regions. However, the precise molecular mechanisms underlying shared and unique features of the developing human nervous system have been only minimally characterized.RESULTSWe generated complementary tissue-level and single-cell transcriptomic datasets from up to 16 brain regions covering prenatal and postnatal development in humans and rhesus macaques (Macaca mulatta), a closely related species and the most commonly studied nonhuman primate. We created and applied TranscriptomeAge and TempShift algorithms to age-match developing specimens between the species and to more rigorously identify temporal differences in gene expression within and across the species. By analyzing regional and temporal patterns of gene expression in both the developing human and macaque brain, and comparing these patterns to a complementary dataset that included transcriptomic information from the adult chimpanzee, we identified shared and divergent transcriptomic features of human brain development. Furthermore, integration with single-cell and single-nucleus transcriptomic data covering prenatal and adult periods of both species revealed that the developmental divergence between humans and macaques can be traced to distinct cell types enriched in different developmental times and brain regions, including the prefrontal cortex, a region of the brain associated with distinctly human aspects of cognition and behavior.We found two phases of prominent species differences: embryonic to late midfetal development and adolescence/young adulthood. This evolutionary cup-shaped or hourglass-like pattern, with high divergence in prenatal development and adolescence/young adulthood and lower divergence in early postnatal development, resembles the developmental cup-shaped pattern described in the accompanying study by Li et al. Even though the developmental (ontogenetic) and evolutionary (phylogenetic) patterns have similar profiles, the overlap of genes driving these two patterns is not substantial, indicating the existence of different molecular mechanisms and constraints for regional specification and species divergence.Notably, we also identified numerous genes and gene coexpression modules exhibiting human-distinct patterns in either temporal (heterochronic) or spatial (heterotopic) gene expression, as well as genes with human-distinct developmental expression, linked to autism spectrum disorder, schizophrenia, and other neurological or psychiatric diseases. This finding potentially suggests mechanistic underpinnings of these disorders.CONCLUSIONOur study provides insights into the evolution of gene expression in the developing human brain and may shed some light on potentially human-specific underpinnings of certain neuropsychiatric disorders.Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders. Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders.Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders. Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders. INTRODUCTION Improved understanding of how the developing human nervous system differs from that of closely related nonhuman primates is fundamental for teasing out human-specific aspects of behavior, cognition, and disorders. RATIONALE The shared and unique functional properties of the human nervous system are rooted in the complex transcriptional programs governing the development of distinct cell types, neural circuits, and regions. However, the precise molecular mechanisms underlying shared and unique features of the developing human nervous system have been only minimally characterized. RESULTS We generated complementary tissue-level and single-cell transcriptomic datasets from up to 16 brain regions covering prenatal and postnatal development in humans and rhesus macaques ( Macaca mulatta ), a closely related species and the most commonly studied nonhuman primate. We created and applied TranscriptomeAge and TempShift algorithms to age-match developing specimens between the species and to more rigorously identify temporal differences in gene expression within and across the species. By analyzing regional and temporal patterns of gene expression in both the developing human and macaque brain, and comparing these patterns to a complementary dataset that included transcriptomic information from the adult chimpanzee, we identified shared and divergent transcriptomic features of human brain development. Furthermore, integration with single-cell and single-nucleus transcriptomic data covering prenatal and adult periods of both species revealed that the developmental divergence between humans and macaques can be traced to distinct cell types enriched in different developmental times and brain regions, including the prefrontal cortex, a region of the brain associated with distinctly human aspects of cognition and behavior. We found two phases of prominent species differences: embryonic to late midfetal development and adolescence/young adulthood. This evolutionary cup-shaped or hourglass-like pattern, with high divergence in prenatal development and adolescence/young adulthood and lower divergence in early postnatal development, resembles the developmental cup-shaped pattern described in the accompanying study by Li et al . Even though the developmental (ontogenetic) and evolutionary (phylogenetic) patterns have similar profiles, the overlap of genes driving these two patterns is not substantial, indicating the existence of different molecular mechanisms and constraints for regional specification and species divergence. Notably, we also identified numerous genes and gene coexpression modules exhibiting human-distinct patterns in either temporal (heterochronic) or spatial (heterotopic) gene expression, as well as genes with human-distinct developmental expression, linked to autism spectrum disorder, schizophrenia, and other neurological or psychiatric diseases. This finding potentially suggests mechanistic underpinnings of these disorders. CONCLUSION Our study provides insights into the evolution of gene expression in the developing human brain and may shed some light on potentially human-specific underpinnings of certain neuropsychiatric disorders. Concerted ontogenetic and phylogenetic transcriptomic divergence in human and macaque brain. Left: Human and macaque brain regions spanning both prenatal and postnatal development were age-matched using TranscriptomeAge. Right: Phylogenetic transcriptomic divergence between humans and macaques resembles the developmental (ontogenetic) cup-shaped pattern of each species, with high divergence in prenatal development and adolescence/young adulthood and lower divergence during the early postnatal period (from perinatal to adolescence). Single-cell transcriptomics revealed shared and divergent transcriptomic features of distinct cell types. Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders. Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated tissue-level and single-cell transcriptomic data from up to 16 brain regions covering prenatal and postnatal rhesus macaque development. Integrative analysis with complementary human data revealed that global intraspecies (ontogenetic) and interspecies (phylogenetic) regional transcriptomic differences exhibit concerted cup-shaped patterns, with a late fetal-to-infancy (perinatal) convergence. Prenatal neocortical transcriptomic patterns revealed transient topographic gradients, whereas postnatal patterns largely reflected functional hierarchy. Genes exhibiting heterotopic and heterochronic divergence included those transiently enriched in the prenatal prefrontal cortex or linked to autism spectrum disorder and schizophrenia. Our findings shed light on transcriptomic programs underlying the evolution of human brain development and the pathogenesis of neuropsychiatric disorders. Also supported by BFU2017-86471-P (MINECO/FEDER, UE), U01 MH106874 grant, Howard Hughes International Early Career, 3P30AG021342-16S2 (H.Z.); Obra Social “La Caixa” and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880) (T.M.-B.); a Formació de Personal Investigador fellowship from Generalitat de Catalunya (FI_B00122) (P.E.-C.); La Caixa Foundation (L.F.-P.); a Juan de la Cierva fellowship (FJCI-2016-29558) from MICINN (D.J.); and NIH grants MH109904 and MH106874, the Kavli Foundation, and the James S. McDonnell Foundation. |
| Author | Zhu, Ying Skarica, Mario Sousa, André M M Gao, Tianliuyun Gulden, Forrest O Zhao, Hongyu Esteller-Cucala, Paula Santpere, Gabriel Sestan, Nenad Yang, Mo Li, Mingfeng Miller, Daniel J Ferrández-Peral, Luis Marques-Bonet, Tomas Juan, David Imamura Kawasawa, Yuka |
| Author_xml | – sequence: 1 givenname: Ying surname: Zhu fullname: Zhu, Ying organization: Department of Biostatistics, Yale School of Public Health, New Haven, CT, USA – sequence: 2 givenname: André M M orcidid: 0000-0003-1740-5066 surname: Sousa fullname: Sousa, André M M organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 3 givenname: Tianliuyun orcidid: 0000-0002-6261-8303 surname: Gao fullname: Gao, Tianliuyun organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 4 givenname: Mario orcidid: 0000-0002-2478-014X surname: Skarica fullname: Skarica, Mario organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 5 givenname: Mingfeng orcidid: 0000-0002-7959-6008 surname: Li fullname: Li, Mingfeng organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 6 givenname: Gabriel orcidid: 0000-0001-5909-8637 surname: Santpere fullname: Santpere, Gabriel organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 7 givenname: Paula orcidid: 0000-0003-3048-4280 surname: Esteller-Cucala fullname: Esteller-Cucala, Paula organization: Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain – sequence: 8 givenname: David orcidid: 0000-0003-1912-9667 surname: Juan fullname: Juan, David organization: Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain – sequence: 9 givenname: Luis orcidid: 0000-0003-0338-0603 surname: Ferrández-Peral fullname: Ferrández-Peral, Luis organization: Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain – sequence: 10 givenname: Forrest O orcidid: 0000-0003-3523-0247 surname: Gulden fullname: Gulden, Forrest O organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 11 givenname: Mo orcidid: 0000-0003-1670-5243 surname: Yang fullname: Yang, Mo organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 12 givenname: Daniel J orcidid: 0000-0002-4844-0828 surname: Miller fullname: Miller, Daniel J organization: Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA – sequence: 13 givenname: Tomas orcidid: 0000-0002-5597-3075 surname: Marques-Bonet fullname: Marques-Bonet, Tomas organization: Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Barcelona, Spain – sequence: 14 givenname: Yuka orcidid: 0000-0002-8638-6738 surname: Imamura Kawasawa fullname: Imamura Kawasawa, Yuka organization: Departments of Pharmacology and Biochemistry and Molecular Biology, Institute for Personalized Medicine, Penn State University College of Medicine, Hershey, PA, USA – sequence: 15 givenname: Hongyu surname: Zhao fullname: Zhao, Hongyu organization: Department of Biostatistics, Yale School of Public Health, New Haven, CT, USA – sequence: 16 givenname: Nenad orcidid: 0000-0003-0966-9619 surname: Sestan fullname: Sestan, Nenad email: nenad.sestan@yale.edu organization: Departments of Genetics, Psychiatry, and Comparative Medicine, Program in Cellular Neuroscience, Neurodegeneration and Repair, and Yale Child Study Center, Yale School of Medicine, New Haven, CT, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30545855$$D View this record in MEDLINE/PubMed |
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| Snippet | Human nervous system development is an intricate and protracted process that requires precise spatiotemporal transcriptional regulation. We generated... INTRODUCTION Improved understanding of how the developing human nervous system differs from that of closely related nonhuman primates is fundamental for... INTRODUCTIONImproved understanding of how the developing human nervous system differs from that of closely related nonhuman primates is fundamental for teasing... |
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| SubjectTerms | Adolescents Adults Age Animals Autism Autism Spectrum Disorder - genetics Biological evolution Brain Brain - embryology Brain - growth & development Child development Cognition Disorders Divergence Embryogenesis Evolution Fetuses Gene expression Gene Expression Regulation, Developmental Gene regulation Genes Human behavior Humans Macaca mulatta Mental disorders Meta Analysis Molecular modelling Nervous system Neural networks Neurogenesis - genetics Nuclei (cytology) Ontogeny Pathogenesis Phylogenetics Phylogeny Prefrontal cortex Prefrontal Cortex - enzymology Prefrontal Cortex - growth & development Primates Regional analysis Regional development Schizophrenia Schizophrenia - genetics Species Temporal cortex Tissues Transcription Transcriptome Uniqueness |
| Title | Spatiotemporal transcriptomic divergence across human and macaque brain development |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/30545855 https://www.proquest.com/docview/2156991014 https://www.proquest.com/docview/2157661104/abstract/ https://recercat.cat/handle/2072/367034 |
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