Spatiotemporal transcriptomic divergence across human and macaque brain development

Ying Zhu; André M.M. Sousa; Tianliuyun Gao; Mario Skarica; Mingfeng Li; Gabriel Santpere; Paula Esteller-Cucala; David Juan; Luis Ferrández-Peral; Forrest O. Gulden; Mo Yang; Daniel J. Miller; Tomas Marques-Bonet; Yuka Imamura Kawasawa; Hongyu Zhao; Nenad Sestan

doi:10.1126/science.aat8077

Spatiotemporal transcriptomic divergence across human and macaque brain development

Ying Zhu, André M.M. Sousa, Tianliuyun Gao, Mario Skarica, Mingfeng Li, Gabriel Santpere, Paula Esteller-Cucala, David Juan, Luis Ferrández-Peral, Forrest O. Gulden, Mo Yang, Daniel J. Miller, Tomas Marques-Bonet, Yuka Imamura Kawasawa, Hongyu Zhao, Nenad Sestan

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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.

Original language	English (US)
Article number	1267
Journal	Science
Volume	362
Issue number	6420
DOIs	https://doi.org/10.1126/science.aat8077
State	Published - Dec 14 2018
Externally published	Yes

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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., Kawasawa, Y. I., Zhao, H., & Sestan, N. (2018). Spatiotemporal transcriptomic divergence across human and macaque brain development. Science, 362(6420), Article 1267. https://doi.org/10.1126/science.aat8077

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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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doi = "10.1126/science.aat8077",

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AU - Zhu, Ying

AU - Sousa, André M.M.

AU - Gao, Tianliuyun

AU - Skarica, Mario

AU - Li, Mingfeng

AU - Santpere, Gabriel

AU - Esteller-Cucala, Paula

AU - Juan, David

AU - Ferrández-Peral, Luis

AU - Gulden, Forrest O.

AU - Yang, Mo

AU - Miller, Daniel J.

AU - Marques-Bonet, Tomas

AU - Kawasawa, Yuka Imamura

AU - Zhao, Hongyu

AU - Sestan, Nenad

PY - 2018/12/14

Y1 - 2018/12/14

N2 - 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.

AB - 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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Spatiotemporal transcriptomic divergence across human and macaque brain development

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