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Single-cell atlas of a non-human primate reveals new pathogenic mechanisms of COVID-19

Lei Han, Xiaoyu Wei, Chuanyu Liu, Giacomo Volpe, Zhifeng Wang, Taotao Pan, Yue Yuan, Ying Lei, Yiwei Lai, Carl Ward, Yeya Yu, Mingyue Wang, Quan Shi, Tao Wu, Liang Wu, Ya Liu, Chunqing Wang, Yuanhang Zhang, Haixi Sun, Hao Yu, Zhenkun Zhuang, Tingting Tang, Yunting Huang, Haorong Lu, Liqin Xu, Jiangshan Xu, Mengnan Cheng, Yang Liu, Chi Wai Wong, Tao Tan, Weizhi Ji, Patrick H. Maxwell, Huanming Yang, Jian Wang, Shida Zhu, Shiping Liu, Xun Xu, Yong Hou, Miguel A. Esteban, Longqi Liu, South China Greater Bay Area-Single Cell Consortium (SC-GBA-C)
doi: https://doi.org/10.1101/2020.04.10.022103
Lei Han
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Xiaoyu Wei
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Chuanyu Liu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
14Shenzhen Bay Laboratory, Shenzhen 51800, China
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Giacomo Volpe
4Laboratory of Integrative biology, Guangzhou Institutes of Biomedicine and Health, CAS, Guangzhou 510530, China
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Zhifeng Wang
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Taotao Pan
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Yue Yuan
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Ying Lei
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
14Shenzhen Bay Laboratory, Shenzhen 51800, China
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Yiwei Lai
4Laboratory of Integrative biology, Guangzhou Institutes of Biomedicine and Health, CAS, Guangzhou 510530, China
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Carl Ward
4Laboratory of Integrative biology, Guangzhou Institutes of Biomedicine and Health, CAS, Guangzhou 510530, China
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Yeya Yu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
5BGI College, Zhengzhou University, Zhengzhou 450000, China
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Mingyue Wang
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Quan Shi
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
6Laboratory of Genomics and Molecular Biomedicine, Department of Biology, University of Copenhagen, Copenhagen 2200, Denmark
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Tao Wu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Liang Wu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Ya Liu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Chunqing Wang
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Yuanhang Zhang
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Haixi Sun
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Hao Yu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Zhenkun Zhuang
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
7School of Biology and Biological Engineering, South China University of Technology, Guangzhou 510006, China
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Tingting Tang
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Yunting Huang
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Haorong Lu
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Liqin Xu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
6Laboratory of Genomics and Molecular Biomedicine, Department of Biology, University of Copenhagen, Copenhagen 2200, Denmark
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Jiangshan Xu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Mengnan Cheng
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Yang Liu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
3BGI Education Center, University of Chinese Academy of Sciences (CAS), Shenzhen 518083, China
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Chi Wai Wong
8Huazhen Biosciences, Guangzhou 510900, China
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Tao Tan
9Yunnan Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming 650500, China
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Weizhi Ji
9Yunnan Key Laboratory of Primate Biomedical Research, Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming 650500, China
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Patrick H. Maxwell
12Cambridge Institute for Medical Research, Department of Medicine, University of Cambridge, Cambridge CB2 0XY, United Kingdom
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Huanming Yang
1BGI-Shenzhen, Shenzhen 518083, China
10James D. Watson Institute of Genome Science, Hangzhou, 310008, China
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Jian Wang
1BGI-Shenzhen, Shenzhen 518083, China
10James D. Watson Institute of Genome Science, Hangzhou, 310008, China
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Shida Zhu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
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Shiping Liu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
13Shenzhen Key Laboratory of Single-Cell Omics, BGI-Shenzhen, Shenzhen 518120, China
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Xun Xu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
11Institute for Stem Cells and Regeneration, CAS, Beijing 100101, China
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  • For correspondence: xuxun@genomics.cn houyong@genomics.cn miguel@gibh.ac.cn liulongqi@genomics.cn
Yong Hou
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
13Shenzhen Key Laboratory of Single-Cell Omics, BGI-Shenzhen, Shenzhen 518120, China
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  • For correspondence: xuxun@genomics.cn houyong@genomics.cn miguel@gibh.ac.cn liulongqi@genomics.cn
Miguel A. Esteban
4Laboratory of Integrative biology, Guangzhou Institutes of Biomedicine and Health, CAS, Guangzhou 510530, China
1BGI-Shenzhen, Shenzhen 518083, China
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  • For correspondence: xuxun@genomics.cn houyong@genomics.cn miguel@gibh.ac.cn liulongqi@genomics.cn
Longqi Liu
1BGI-Shenzhen, Shenzhen 518083, China
2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China
14Shenzhen Bay Laboratory, Shenzhen 51800, China
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  • For correspondence: xuxun@genomics.cn houyong@genomics.cn miguel@gibh.ac.cn liulongqi@genomics.cn
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ABSTRACT

Stopping COVID-19 is a priority worldwide. Understanding which cell types are targeted by SARS-CoV-2 virus, whether interspecies differences exist, and how variations in cell state influence viral entry is fundamental for accelerating therapeutic and preventative approaches. In this endeavor, we profiled the transcriptome of nine tissues from a Macaca fascicularis monkey at single-cell resolution. The distribution of SARS-CoV-2 facilitators, ACE2 and TMRPSS2, in different cell subtypes showed substantial heterogeneity across lung, kidney, and liver. Through co-expression analysis, we identified immunomodulatory proteins such as IDO2 and ANPEP as potential SARS-CoV-2 targets responsible for immune cell exhaustion. Furthermore, single-cell chromatin accessibility analysis of the kidney unveiled a plausible link between IL6-mediated innate immune responses aiming to protect tissue and enhanced ACE2 expression that could promote viral entry. Our work constitutes a unique resource for understanding the physiology and pathophysiology of two phylogenetically close species, which might guide in the development of therapeutic approaches in humans.

Bullet points

  1. We generated a single-cell transcriptome atlas of 9 monkey tissues to study COVID-19.

  2. ACE2+TMPRSS2+ epithelial cells of lung, kidney and liver are targets for SARS-CoV-2.

  3. ACE2 correlation analysis shows IDO2 and ANPEP as potential therapeutic opportunities.

  4. We unveil a link between IL6, STAT transcription factors and boosted SARS-CoV-2 entry.

Competing Interest Statement

Employees of BGI have stock holdings in BGI.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 24, 2020.
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Single-cell atlas of a non-human primate reveals new pathogenic mechanisms of COVID-19
Lei Han, Xiaoyu Wei, Chuanyu Liu, Giacomo Volpe, Zhifeng Wang, Taotao Pan, Yue Yuan, Ying Lei, Yiwei Lai, Carl Ward, Yeya Yu, Mingyue Wang, Quan Shi, Tao Wu, Liang Wu, Ya Liu, Chunqing Wang, Yuanhang Zhang, Haixi Sun, Hao Yu, Zhenkun Zhuang, Tingting Tang, Yunting Huang, Haorong Lu, Liqin Xu, Jiangshan Xu, Mengnan Cheng, Yang Liu, Chi Wai Wong, Tao Tan, Weizhi Ji, Patrick H. Maxwell, Huanming Yang, Jian Wang, Shida Zhu, Shiping Liu, Xun Xu, Yong Hou, Miguel A. Esteban, Longqi Liu, South China Greater Bay Area-Single Cell Consortium (SC-GBA-C)
bioRxiv 2020.04.10.022103; doi: https://doi.org/10.1101/2020.04.10.022103
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Single-cell atlas of a non-human primate reveals new pathogenic mechanisms of COVID-19
Lei Han, Xiaoyu Wei, Chuanyu Liu, Giacomo Volpe, Zhifeng Wang, Taotao Pan, Yue Yuan, Ying Lei, Yiwei Lai, Carl Ward, Yeya Yu, Mingyue Wang, Quan Shi, Tao Wu, Liang Wu, Ya Liu, Chunqing Wang, Yuanhang Zhang, Haixi Sun, Hao Yu, Zhenkun Zhuang, Tingting Tang, Yunting Huang, Haorong Lu, Liqin Xu, Jiangshan Xu, Mengnan Cheng, Yang Liu, Chi Wai Wong, Tao Tan, Weizhi Ji, Patrick H. Maxwell, Huanming Yang, Jian Wang, Shida Zhu, Shiping Liu, Xun Xu, Yong Hou, Miguel A. Esteban, Longqi Liu, South China Greater Bay Area-Single Cell Consortium (SC-GBA-C)
bioRxiv 2020.04.10.022103; doi: https://doi.org/10.1101/2020.04.10.022103

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