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Cited by 414Single-cell and spatial transcriptomicsDevelopmental Biology and Gene RegulationNeurogenesis and neuroplasticity mechanisms

Spatiotemporal transcriptomic divergence across human and macaque brain development

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Zhu, Ying, Sousa, André M. M., Gao, Tianliuyun, Skarica, Mario, Li, Mingfeng, Santpere, Gabriel, Esteller-Cucala, Paula, Juan, David +8 more·2018·Science
DOI 10.1126/science.aat8077PMC PMC6900982
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Abstract

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.

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  • TempShift revealed several genes displaying heterochronic expression in DS, including several synaptic proteins.

    “Furthermore, a recent study has applied a new algorithm, TempShift, that detects heterochronic expression of genes between species or between individuals with a disease and matched controls, and revealed several genes displaying heterochronic expression in DS, including several synaptic proteins106,152.”

    From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [152]

    The ‘Heterochronic changes in human and macaque brain transcriptome’ section reports using TempShift to identify heterochronic genes between species. The ‘Species difference in spatio-temporal expression of disease genes’ section identifies synaptic proteins with such differences, but describes human–macaque comparisons involving ASD-associated genes, not heterochronic expression in Down syndrome (DS) or comparisons with matched disease controls. Page numbers are unavailable in our copy. (LLM, conf=0.88)

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Authors
Zhu, Y., Sousa, A. M. M., Gao, T., Skarica, M., Li, M., Santpere, G., Esteller-Cucala, P., Juan, D., Ferrández-Peral, L., Gulden, F. O., Yang, M., Miller, D. J., Marques-Bonet, T., Imamura Kawasawa, Y., Zhao, H., & Sestan, N.
Affiliations
  • Yale University (US)
  • Department of Neuroscience and Kavli Institute for Neuroscience, Yale School of Medicine, New Haven, CT, USA.
  • Consejo Superior de Investigaciones Científicas (ES)
  • Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain.
  • Departments of Pharmacology and Biochemistry and Molecular Biology, Institute for Personalized Medicine, Penn State University College of Medicine, Hershey, PA, USA.
Corresponding author
  • Zhu, Ying
  • Sousa, André M. M.
  • Gao, Tianliuyun
  • Li, Mingfeng
ORCID
Venue
Science
Publisher
American Association for the Advancement of Science (AAAS)
Published
2018-12-14
Volume
362
Issue
6420
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
DOI
10.1126/science.aat8077
PMC
PMC6900982
OpenAlex
W2903689387
Cited by
414
References
14
Citations by year
2026: 47 · 2025: 54 · 2024: 55 · 2023: 75 · 2022: 51 · 2021: 52 · 2020: 48 · 2019: 30 · 2018: 2
FWCI
11.68
Type
journal article
Language
en
Open access
Locations
  • Science (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RECERCAT (Consorci de Serveis Universitaris de Catalunya) (acceptedVersion)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion)
Funders
National Institute of Mental Health (MH103339, MH089929, MH106934)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
human brain development, rhesus monkeys, developmental divergence, transcriptome evolution, heterochrony, heterotopy, prefrontal cortex, age matching, autism spectrum disorder, schizophrenia, gene co-expression modules, prenatal and postnatal development, chimpanzees, single-cell transcriptomics, single-nucleus transcriptomics, neuropsychiatric disorders
MeSH terms
Autism Spectrum Disorder, Animals, Brain, Humans, Macaca mulatta, Schizophrenia, Prefrontal Cortex, Gene Expression Regulation, Developmental, Neurogenesis, Transcriptome

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