Nature, volume 574, issue 7778, pages 418-422
Organoid single-cell genomic atlas uncovers human-specific features of brain development
Kanton Sabina
1
,
Boyle Michael James
1
,
He Zhisong
1, 2
,
Santel Malgorzata
1
,
Weigert Anne
1
,
Sanchís Calleja Fátima
1, 2
,
Guijarro Patricia
3
,
Sidow Leila
1
,
Fleck Jonas Simon
2
,
Han Dingding
3
,
Qian Zhengzong
3
,
Heide Michael
4
,
Huttner Wieland B.
4
,
Khaitovich Philipp
1, 3, 5
,
Pääbo Svante
1
,
Treutlein Barbara
1, 2
,
Camp J. Gray
1, 6
1
Max Planck Institute For Evolutionary Anthropology, Leipzig, Germany
|
3
CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai, China
|
4
Max Planck institute of Molecular Cell Biology and Genetics, Dresden, Germany
|
6
Institute of Molecular and Clinical Ophthalmology, Basel, Switzerland
|
Publication type: Journal Article
Publication date: 2019-10-16
Multidisciplinary
Abstract
The human brain has undergone substantial change since humans diverged from chimpanzees and the other great apes1,2. However, the genetic and developmental programs that underlie this divergence are not fully understood. Here we have analysed stem cell-derived cerebral organoids using single-cell transcriptomics and accessible chromatin profiling to investigate gene-regulatory changes that are specific to humans. We first analysed cell composition and reconstructed differentiation trajectories over the entire course of human cerebral organoid development from pluripotency, through neuroectoderm and neuroepithelial stages, followed by divergence into neuronal fates within the dorsal and ventral forebrain, midbrain and hindbrain regions. Brain-region composition varied in organoids from different iPSC lines, but regional gene-expression patterns remained largely reproducible across individuals. We analysed chimpanzee and macaque cerebral organoids and found that human neuronal development occurs at a slower pace relative to the other two primates. Using pseudotemporal alignment of differentiation paths, we found that human-specific gene expression resolved to distinct cell states along progenitor-to-neuron lineages in the cortex. Chromatin accessibility was dynamic during cortex development, and we identified divergence in accessibility between human and chimpanzee that correlated with human-specific gene expression and genetic change. Finally, we mapped human-specific expression in adult prefrontal cortex using single-nucleus RNA sequencing analysis and identified developmental differences that persist into adulthood, as well as cell-state-specific changes that occur exclusively in the adult brain. Our data provide a temporal cell atlas of great ape forebrain development, and illuminate dynamic gene-regulatory features that are unique to humans. Species comparisons using single-cell transcriptomics and accessible chromatin profiling in stem cell-derived cerebral organoids are used to map dynamic gene-regulatory changes that are unique to humans.
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Kanton S. et al. Organoid single-cell genomic atlas uncovers human-specific features of brain development // Nature. 2019. Vol. 574. No. 7778. pp. 418-422.
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Kanton S., Boyle M. J., He Z., Santel M., Weigert A., Sanchís Calleja F., Guijarro P., Sidow L., Fleck J. S., Han D., Qian Z., Heide M., Huttner W. B., Khaitovich P., Pääbo S., Treutlein B., Camp J. G. Organoid single-cell genomic atlas uncovers human-specific features of brain development // Nature. 2019. Vol. 574. No. 7778. pp. 418-422.
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TY - JOUR
DO - 10.1038/s41586-019-1654-9
UR - https://doi.org/10.1038%2Fs41586-019-1654-9
TI - Organoid single-cell genomic atlas uncovers human-specific features of brain development
T2 - Nature
AU - Kanton, Sabina
AU - Boyle, Michael James
AU - He, Zhisong
AU - Santel, Malgorzata
AU - Weigert, Anne
AU - Sanchís Calleja, Fátima
AU - Guijarro, Patricia
AU - Sidow, Leila
AU - Fleck, Jonas Simon
AU - Han, Dingding
AU - Qian, Zhengzong
AU - Heide, Michael
AU - Huttner, Wieland B.
AU - Khaitovich, Philipp
AU - Pääbo, Svante
AU - Treutlein, Barbara
AU - Camp, J. Gray
PY - 2019
DA - 2019/10/16 00:00:00
PB - Springer Nature
SP - 418-422
IS - 7778
VL - 574
SN - 0028-0836
SN - 1476-4687
ER -
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@article{2019_Kanton,
author = {Sabina Kanton and Michael James Boyle and Zhisong He and Malgorzata Santel and Anne Weigert and Fátima Sanchís Calleja and Patricia Guijarro and Leila Sidow and Jonas Simon Fleck and Dingding Han and Zhengzong Qian and Michael Heide and Wieland B. Huttner and Philipp Khaitovich and Svante Pääbo and Barbara Treutlein and J. Gray Camp},
title = {Organoid single-cell genomic atlas uncovers human-specific features of brain development},
journal = {Nature},
year = {2019},
volume = {574},
publisher = {Springer Nature},
month = {oct},
url = {https://doi.org/10.1038%2Fs41586-019-1654-9},
number = {7778},
pages = {418--422},
doi = {10.1038/s41586-019-1654-9}
}
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Kanton, Sabina, et al. “Organoid single-cell genomic atlas uncovers human-specific features of brain development.” Nature, vol. 574, no. 7778, Oct. 2019, pp. 418-422. https://doi.org/10.1038%2Fs41586-019-1654-9.
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