Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Ao Chen; Yidi Sun; Ying Lei; Chao Li; Sha Liao; Juan Meng; Yiqin Bai; Zhen Liu; Zhifeng Liang; Zhiyong Zhu; Nini Yuan; Hao Yang; Zihan Wu; Feng Lin; Kexin Wang; Mei Li; Shuzhen Zhang; Meisong Yang; Tianyi Fei; Zhenkun Zhuang; Yiming Huang; Yong Zhang; Yuanfang Xu; Luman Cui; Ruiyi Zhang; Lei Han; Xing Sun; Bichao Chen; Wenjiao Li; Baoqian Huangfu; Kailong Ma; Jianyun Ma; Zhao Li; Yikun Lin; He Wang; Yanqing Zhong; Huifang Zhang; Qian Yu; Yaqian Wang; Xing Liu; Jian Peng; Chuanyu Liu; Wei Chen; Wentao Pan; Yingjie An; Shihui Xia; Yanbing Lu; Mingli Wang; Xinxiang Song; Shuai Liu; Zhifeng Wang; Chun Gong; Xin Huang; Yue Yuan; Yun Zhao; Qinwen Chai; Xing Tan; Jianfeng Liu; Mingyuan Zheng; Shengkang Li; Yaling Huang; Yan Hong; Zirui Huang; Min Li; Mengmeng Jin; Yan Li; Hui Zhang; Suhong Sun; Li Gao; Yinqi Bai; Mengnan Cheng; Guohai Hu; Shiping Liu; Bo Wang; Bin Xiang; Shuting Li; Huanhuan Li; Mengni Chen; Shiwen Wang; Minglong Li; Weibin Liu; Xin Liu; Qian Zhao; Michael Lisby; Jing Wang; Jiao Fang; Yun Lin; Qing Xie; Jie He; Huatai Xu; Wei Huang; Jan Mulder; Huanming Yang; Yangang Sun; Mathias Uhlen; Muming Poo; Jian Wang; Jianhua Yao; Wu Wei; Yuxiang Li; Zhiming Shen; Longqi Liu; Zhiyong Liu; Xun Xu; Chengyu Li

doi:10.1016/j.cell.2023.06.009

Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Ao Chen
, Yidi Sun
, Ying Lei
, Chao Li
, Sha Liao
, Juan Meng
, Yiqin Bai
, Zhen Liu
, Zhifeng Liang
, Zhiyong Zhu
, Nini Yuan
, Hao Yang
, Zihan Wu
, Feng Lin
, Kexin Wang
, Mei Li
, Shuzhen Zhang
, Meisong Yang
, Tianyi Fei
, Zhenkun Zhuang

Yiming Huang, Yong Zhang, Yuanfang Xu, Luman Cui, Ruiyi Zhang, Lei Han, Xing Sun, Bichao Chen, Wenjiao Li, Baoqian Huangfu, Kailong Ma, Jianyun Ma, Zhao Li, Yikun Lin, He Wang, Yanqing Zhong, Huifang Zhang, Qian Yu, Yaqian Wang, Xing Liu, Jian Peng, Chuanyu Liu, Wei Chen, Wentao Pan, Yingjie An, Shihui Xia, Yanbing Lu, Mingli Wang, Xinxiang Song, Shuai Liu, Zhifeng Wang, Chun Gong, Xin Huang, Yue Yuan, Yun Zhao, Qinwen Chai, Xing Tan, Jianfeng Liu, Mingyuan Zheng, Shengkang Li, Yaling Huang, Yan Hong, Zirui Huang, Min Li, Mengmeng Jin, Yan Li, Hui Zhang, Suhong Sun, Li Gao, Yinqi Bai, Mengnan Cheng, Guohai Hu, Shiping Liu, Bo Wang, Bin Xiang, Shuting Li, Huanhuan Li, Mengni Chen, Shiwen Wang, Minglong Li, Weibin Liu, Xin Liu, Qian Zhao, Michael Lisby, Jing Wang, Jiao Fang, Yun Lin, Qing Xie, Jie He, Huatai Xu, Wei Huang, Jan Mulder, Huanming Yang, Yangang Sun, Mathias Uhlen, Muming Poo, Jian Wang, Jianhua Yao, Wu Wei, Yuxiang Li, Zhiming Shen, Longqi Liu, Zhiyong Liu, Xun Xu, Chengyu Li

Research output: Contribution to journal › Article › peer-review

116 Scopus citations

Abstract

Elucidating the cellular organization of the cerebral cortex is critical for understanding brain structure and function. Using large-scale single-nucleus RNA sequencing and spatial transcriptomic analysis of 143 macaque cortical regions, we obtained a comprehensive atlas of 264 transcriptome-defined cortical cell types and mapped their spatial distribution across the entire cortex. We characterized the cortical layer and region preferences of glutamatergic, GABAergic, and non-neuronal cell types, as well as regional differences in cell-type composition and neighborhood complexity. Notably, we discovered a relationship between the regional distribution of various cell types and the region's hierarchical level in the visual and somatosensory systems. Cross-species comparison of transcriptomic data from human, macaque, and mouse cortices further revealed primate-specific cell types that are enriched in layer 4, with their marker genes expressed in a region-dependent manner. Our data provide a cellular and molecular basis for understanding the evolution, development, aging, and pathogenesis of the primate brain.

Original language	English
Pages (from-to)	3726-3743.e24
Journal	Cell
Volume	186
Issue number	17
DOIs	https://doi.org/10.1016/j.cell.2023.06.009
State	Published - 17 Aug 2023
Externally published	Yes

Keywords

cell-type organization
hierarchy
macaque cortex
single-cell
spatial transcriptome

Access to Document

10.1016/j.cell.2023.06.009

Cite this

@article{fb22051947c743edbf4f68d96d0d9e0a,

title = "Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex",

abstract = "Elucidating the cellular organization of the cerebral cortex is critical for understanding brain structure and function. Using large-scale single-nucleus RNA sequencing and spatial transcriptomic analysis of 143 macaque cortical regions, we obtained a comprehensive atlas of 264 transcriptome-defined cortical cell types and mapped their spatial distribution across the entire cortex. We characterized the cortical layer and region preferences of glutamatergic, GABAergic, and non-neuronal cell types, as well as regional differences in cell-type composition and neighborhood complexity. Notably, we discovered a relationship between the regional distribution of various cell types and the region's hierarchical level in the visual and somatosensory systems. Cross-species comparison of transcriptomic data from human, macaque, and mouse cortices further revealed primate-specific cell types that are enriched in layer 4, with their marker genes expressed in a region-dependent manner. Our data provide a cellular and molecular basis for understanding the evolution, development, aging, and pathogenesis of the primate brain.",

keywords = "cell-type organization, hierarchy, macaque cortex, single-cell, spatial transcriptome",

author = "Ao Chen and Yidi Sun and Ying Lei and Chao Li and Sha Liao and Juan Meng and Yiqin Bai and Zhen Liu and Zhifeng Liang and Zhiyong Zhu and Nini Yuan and Hao Yang and Zihan Wu and Feng Lin and Kexin Wang and Mei Li and Shuzhen Zhang and Meisong Yang and Tianyi Fei and Zhenkun Zhuang and Yiming Huang and Yong Zhang and Yuanfang Xu and Luman Cui and Ruiyi Zhang and Lei Han and Xing Sun and Bichao Chen and Wenjiao Li and Baoqian Huangfu and Kailong Ma and Jianyun Ma and Zhao Li and Yikun Lin and He Wang and Yanqing Zhong and Huifang Zhang and Qian Yu and Yaqian Wang and Xing Liu and Jian Peng and Chuanyu Liu and Wei Chen and Wentao Pan and Yingjie An and Shihui Xia and Yanbing Lu and Mingli Wang and Xinxiang Song and Shuai Liu and Zhifeng Wang and Chun Gong and Xin Huang and Yue Yuan and Yun Zhao and Qinwen Chai and Xing Tan and Jianfeng Liu and Mingyuan Zheng and Shengkang Li and Yaling Huang and Yan Hong and Zirui Huang and Min Li and Mengmeng Jin and Yan Li and Hui Zhang and Suhong Sun and Li Gao and Yinqi Bai and Mengnan Cheng and Guohai Hu and Shiping Liu and Bo Wang and Bin Xiang and Shuting Li and Huanhuan Li and Mengni Chen and Shiwen Wang and Minglong Li and Weibin Liu and Xin Liu and Qian Zhao and Michael Lisby and Jing Wang and Jiao Fang and Yun Lin and Qing Xie and Jie He and Huatai Xu and Wei Huang and Jan Mulder and Huanming Yang and Yangang Sun and Mathias Uhlen and Muming Poo and Jian Wang and Jianhua Yao and Wu Wei and Yuxiang Li and Zhiming Shen and Longqi Liu and Zhiyong Liu and Xun Xu and Chengyu Li",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = aug,

day = "17",

doi = "10.1016/j.cell.2023.06.009",

language = "英语",

volume = "186",

pages = "3726--3743.e24",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier B.V.",

number = "17",

}

Chen, A, Sun, Y, Lei, Y, Li, C, Liao, S, Meng, J, Bai, Y, Liu, Z, Liang, Z, Zhu, Z, Yuan, N, Yang, H, Wu, Z, Lin, F, Wang, K, Li, M, Zhang, S, Yang, M, Fei, T, Zhuang, Z, Huang, Y, Zhang, Y, Xu, Y, Cui, L, Zhang, R, Han, L, Sun, X, Chen, B, Li, W, Huangfu, B, Ma, K, Ma, J, Li, Z, Lin, Y, Wang, H, Zhong, Y, Zhang, H, Yu, Q, Wang, Y, Liu, X, Peng, J, Liu, C, Chen, W, Pan, W, An, Y, Xia, S, Lu, Y, Wang, M, Song, X, Liu, S, Wang, Z, Gong, C, Huang, X, Yuan, Y, Zhao, Y, Chai, Q, Tan, X, Liu, J, Zheng, M, Li, S, Huang, Y, Hong, Y, Huang, Z, Li, M, Jin, M, Li, Y, Zhang, H, Sun, S, Gao, L, Bai, Y, Cheng, M, Hu, G, Liu, S, Wang, B, Xiang, B, Li, S, Li, H, Chen, M, Wang, S, Li, M, Liu, W, Liu, X, Zhao, Q, Lisby, M, Wang, J, Fang, J, Lin, Y, Xie, Q, He, J, Xu, H, Huang, W, Mulder, J, Yang, H, Sun, Y, Uhlen, M, Poo, M, Wang, J, Yao, J, Wei, W, Li, Y, Shen, Z, Liu, L, Liu, Z, Xu, X & Li, C 2023, 'Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex', Cell, vol. 186, no. 17, pp. 3726-3743.e24. https://doi.org/10.1016/j.cell.2023.06.009

TY - JOUR

T1 - Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

AU - Chen, Ao

AU - Sun, Yidi

AU - Lei, Ying

AU - Li, Chao

AU - Liao, Sha

AU - Meng, Juan

AU - Bai, Yiqin

AU - Liu, Zhen

AU - Liang, Zhifeng

AU - Zhu, Zhiyong

AU - Yuan, Nini

AU - Yang, Hao

AU - Wu, Zihan

AU - Lin, Feng

AU - Wang, Kexin

AU - Li, Mei

AU - Zhang, Shuzhen

AU - Yang, Meisong

AU - Fei, Tianyi

AU - Zhuang, Zhenkun

AU - Huang, Yiming

AU - Zhang, Yong

AU - Xu, Yuanfang

AU - Cui, Luman

AU - Zhang, Ruiyi

AU - Han, Lei

AU - Sun, Xing

AU - Chen, Bichao

AU - Li, Wenjiao

AU - Huangfu, Baoqian

AU - Ma, Kailong

AU - Ma, Jianyun

AU - Li, Zhao

AU - Lin, Yikun

AU - Wang, He

AU - Zhong, Yanqing

AU - Zhang, Huifang

AU - Yu, Qian

AU - Wang, Yaqian

AU - Liu, Xing

AU - Peng, Jian

AU - Liu, Chuanyu

AU - Chen, Wei

AU - Pan, Wentao

AU - An, Yingjie

AU - Xia, Shihui

AU - Lu, Yanbing

AU - Wang, Mingli

AU - Song, Xinxiang

AU - Liu, Shuai

AU - Wang, Zhifeng

AU - Gong, Chun

AU - Huang, Xin

AU - Yuan, Yue

AU - Zhao, Yun

AU - Chai, Qinwen

AU - Tan, Xing

AU - Liu, Jianfeng

AU - Zheng, Mingyuan

AU - Li, Shengkang

AU - Huang, Yaling

AU - Hong, Yan

AU - Huang, Zirui

AU - Li, Min

AU - Jin, Mengmeng

AU - Li, Yan

AU - Zhang, Hui

AU - Sun, Suhong

AU - Gao, Li

AU - Bai, Yinqi

AU - Cheng, Mengnan

AU - Hu, Guohai

AU - Liu, Shiping

AU - Wang, Bo

AU - Xiang, Bin

AU - Li, Shuting

AU - Li, Huanhuan

AU - Chen, Mengni

AU - Wang, Shiwen

AU - Li, Minglong

AU - Liu, Weibin

AU - Liu, Xin

AU - Zhao, Qian

AU - Lisby, Michael

AU - Wang, Jing

AU - Fang, Jiao

AU - Lin, Yun

AU - Xie, Qing

AU - He, Jie

AU - Xu, Huatai

AU - Huang, Wei

AU - Mulder, Jan

AU - Yang, Huanming

AU - Sun, Yangang

AU - Uhlen, Mathias

AU - Poo, Muming

AU - Wang, Jian

AU - Yao, Jianhua

AU - Wei, Wu

AU - Li, Yuxiang

AU - Shen, Zhiming

AU - Liu, Longqi

AU - Liu, Zhiyong

AU - Xu, Xun

AU - Li, Chengyu

PY - 2023/8/17

Y1 - 2023/8/17

N2 - Elucidating the cellular organization of the cerebral cortex is critical for understanding brain structure and function. Using large-scale single-nucleus RNA sequencing and spatial transcriptomic analysis of 143 macaque cortical regions, we obtained a comprehensive atlas of 264 transcriptome-defined cortical cell types and mapped their spatial distribution across the entire cortex. We characterized the cortical layer and region preferences of glutamatergic, GABAergic, and non-neuronal cell types, as well as regional differences in cell-type composition and neighborhood complexity. Notably, we discovered a relationship between the regional distribution of various cell types and the region's hierarchical level in the visual and somatosensory systems. Cross-species comparison of transcriptomic data from human, macaque, and mouse cortices further revealed primate-specific cell types that are enriched in layer 4, with their marker genes expressed in a region-dependent manner. Our data provide a cellular and molecular basis for understanding the evolution, development, aging, and pathogenesis of the primate brain.

AB - Elucidating the cellular organization of the cerebral cortex is critical for understanding brain structure and function. Using large-scale single-nucleus RNA sequencing and spatial transcriptomic analysis of 143 macaque cortical regions, we obtained a comprehensive atlas of 264 transcriptome-defined cortical cell types and mapped their spatial distribution across the entire cortex. We characterized the cortical layer and region preferences of glutamatergic, GABAergic, and non-neuronal cell types, as well as regional differences in cell-type composition and neighborhood complexity. Notably, we discovered a relationship between the regional distribution of various cell types and the region's hierarchical level in the visual and somatosensory systems. Cross-species comparison of transcriptomic data from human, macaque, and mouse cortices further revealed primate-specific cell types that are enriched in layer 4, with their marker genes expressed in a region-dependent manner. Our data provide a cellular and molecular basis for understanding the evolution, development, aging, and pathogenesis of the primate brain.

KW - cell-type organization

KW - hierarchy

KW - macaque cortex

KW - single-cell

KW - spatial transcriptome

UR - https://www.scopus.com/pages/publications/85167841501

U2 - 10.1016/j.cell.2023.06.009

DO - 10.1016/j.cell.2023.06.009

M3 - 文章

C2 - 37442136

AN - SCOPUS:85167841501

SN - 0092-8674

VL - 186

SP - 3726-3743.e24

JO - Cell

JF - Cell

IS - 17

ER -

Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Abstract

Keywords

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