Human-specific features of spatial gene expression and regulation in eight brain regions
- Chuan Xu1,13,
- Qian Li1,13,
- Olga Efimova2,
- Liu He1,
- Shoji Tatsumoto3,
- Vita Stepanova2,
- Takao Oishi4,
- Toshifumi Udono5,
- Katsushi Yamaguchi6,
- Shuji Shigenobu6,7,
- Akiyoshi Kakita8,
- Hiroyuki Nawa8,
- Philipp Khaitovich2,9,10,11 and
- Yasuhiro Go3,7,12
- 1CAS Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
- 2Skolkovo Institute of Science and Technology, Moscow 143026, Russia;
- 3Cognitive Genomics Research Group, Exploratory Research Center on Life and Living Systems, National Institutes of Natural Sciences, Okazaki, Aichi 4448585, Japan;
- 4Primate Research Institute, Kyoto University, Inuyama, Aichi 4848506, Japan;
- 5Kumamoto Sanctuary, Wildlife Research Center, Kyoto University, Uki, Kumamoto 8693201, Japan;
- 6NIBB Core Research Facilities, National Institute for Basic Biology, Okazaki, Aichi 4448585, Japan;
- 7School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Okazaki, Aichi 4448585, Japan;
- 8Brain Research Institute, Niigata University, Niigata 9518585, Japan;
- 9Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China;
- 10Comparative Biology Laboratory, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China;
- 11School of Life Science and Technology, ShanghaiTech University, Shanghai 200031, China;
- 12Department of Physiological Sciences, National Institute for Physiological Sciences, Okazaki, Aichi 4448585, Japan
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↵13 These authors contributed equally to this work.
Abstract
Molecular maps of the human brain alone do not inform us of the features unique to humans. Yet, the identification of these features is important for understanding both the evolution and nature of human cognition. Here, we approached this question by analyzing gene expression and H3K27ac chromatin modification data collected in eight brain regions of humans, chimpanzees, gorillas, a gibbon, and macaques. An analysis of spatial transcriptome trajectories across eight brain regions in four primate species revealed 1851 genes showing human-specific transcriptome differences in one or multiple brain regions, in contrast to 240 chimpanzee-specific differences. More than half of these human-specific differences represented elevated expression of genes enriched in neuronal and astrocytic markers in the human hippocampus, whereas the rest were enriched in microglial markers and displayed human-specific expression in several frontal cortical regions and the cerebellum. An analysis of the predicted regulatory interactions driving these differences revealed the role of transcription factors in species-specific transcriptome changes, and epigenetic modifications were linked to spatial expression differences conserved across species.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.231357.117.
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Freely available online through the Genome Research Open Access option.
- Received October 16, 2017.
- Accepted June 4, 2018.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
