Comparison of chromatin accessibility landscapes during early development of prefrontal cortex between rhesus macaque and human

Xuelong Yao; Zongyang Lu; Zhanying Feng; Lei Gao; Xin Zhou; Min Li; Suijuan Zhong; Qian Wu; Zhenbo Liu; Haofeng Zhang; Zeyuan Liu; Lizhi Yi; Tao Zhou; Xudong Zhao; Jun Zhang; Yong Wang; Xingxu Huang; Xiaoqun Wang; Jiang Liu

doi:10.1038/s41467-022-31403-3

Comparison of chromatin accessibility landscapes during early development of prefrontal cortex between rhesus macaque and human

Nat Commun. 2022 Jul 6;13(1):3883. doi: 10.1038/s41467-022-31403-3.

Authors

Xuelong Yao^#^{1

2

3}, Zongyang Lu^#^{2

4

5}, Zhanying Feng^#^{2

6}, Lei Gao^#¹, Xin Zhou⁷, Min Li^{2

7}, Suijuan Zhong^{8

9}, Qian Wu^{8

9}, Zhenbo Liu¹, Haofeng Zhang¹⁰, Zeyuan Liu^{2

7}, Lizhi Yi^{1

2}, Tao Zhou^{4

11}, Xudong Zhao¹², Jun Zhang¹⁰, Yong Wang^{2

6

13}, Xingxu Huang^{14

15}, Xiaoqun Wang^{16

17

18

19}, Jiang Liu^{20

21

22}

Affiliations

¹ CAS Key Laboratory of Genome Sciences and Information, Collaborative Innovation Center of Genetics and Development, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, 100101, Beijing, China.
² University of Chinese Academy of Sciences, 100049, Beijing, China.
³ Guangzhou Nvwa Life Technology Co., Ltd, Guangzhou, 510535, China.
⁴ School of Life Science and Technology, Shanghai Tech University, 100 Haike Rd., Pudong New Area, Shanghai, 201210, China.
⁵ Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, 320 Yueyang Road, Shanghai, 200031, China.
⁶ CEMS, NCMIS, MDIS, Academy of Mathematics and Systems Science, Chinese Academy of Sciences, 100190, Beijing, China.
⁷ State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Brain-Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, 100101, Beijing, China.
⁸ State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, 100875, Beijing, China.
⁹ IDG/McGovern Institute for Brain Research, Beijing Normal University, 100875, Beijing, China.
¹⁰ Obstetrics and Gynecology Medical Center of Severe Cardiovascular of Beijing Anzhen Hospital, Capital Medical University, 100029, Beijing, China.
¹¹ Shenzhen Key Lab of Drug Addiction; The Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen, 518055, China.
¹² Kunming Primate Research Center, Key Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Sciences, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223, Kunming, China.
¹³ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China.
¹⁴ School of Life Science and Technology, Shanghai Tech University, 100 Haike Rd., Pudong New Area, Shanghai, 201210, China. huangxx@shanghaitech.edu.cn.
¹⁵ Zhejiang Provincial Key Laboratory of Pancreatic Disease, The First Affiliated Hospital, and Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, Zhejiang, 310058, China. huangxx@shanghaitech.edu.cn.
¹⁶ University of Chinese Academy of Sciences, 100049, Beijing, China. xiaoqunwang@ibp.ac.cn.
¹⁷ State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Brain-Intelligence Technology (Shanghai), Institute of Biophysics, Chinese Academy of Sciences, 100101, Beijing, China. xiaoqunwang@ibp.ac.cn.
¹⁸ Institute for Stem Cell and Regeneration, Chinese Academy of Sciences, 100101, Beijing, China. xiaoqunwang@ibp.ac.cn.
¹⁹ Beijing Institute for Brain Disorders, 100069, Beijing, China. xiaoqunwang@ibp.ac.cn.
²⁰ CAS Key Laboratory of Genome Sciences and Information, Collaborative Innovation Center of Genetics and Development, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, 100101, Beijing, China. liuj@big.ac.cn.
²¹ University of Chinese Academy of Sciences, 100049, Beijing, China. liuj@big.ac.cn.
²² Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, 650223, China. liuj@big.ac.cn.

^# Contributed equally.

Abstract

Epigenetic information regulates gene expression and development. However, our understanding of the evolution of epigenetic regulation on brain development in primates is limited. Here, we compared chromatin accessibility landscapes and transcriptomes during fetal prefrontal cortex (PFC) development between rhesus macaques and humans. A total of 304,761 divergent DNase I-hypersensitive sites (DHSs) are identified between rhesus macaques and humans, although many of these sites share conserved DNA sequences. Interestingly, most of the cis-elements linked to orthologous genes with dynamic expression are divergent DHSs. Orthologous genes expressed at earlier stages tend to have conserved cis-elements, whereas orthologous genes specifically expressed at later stages seldom have conserved cis-elements. These genes are enriched in synapse organization, learning and memory. Notably, DHSs in the PFC at early stages are linked to human educational attainment and cognitive performance. Collectively, the comparison of the chromatin epigenetic landscape between rhesus macaques and humans suggests a potential role for regulatory elements in the evolution of differences in cognitive ability between non-human primates and humans.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Chromatin* / genetics
Deoxyribonuclease I / metabolism
Epigenesis, Genetic*
Humans
Macaca mulatta / genetics
Macaca mulatta / metabolism
Prefrontal Cortex / metabolism
Regulatory Sequences, Nucleic Acid

Substances

Chromatin
Deoxyribonuclease I