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    • Cell Res. 2020.

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    Single-cell transcriptomic atlas of primate cardiopulmonary aging

    Shuai Ma1 2 3, Shuhui Sun1 4, Jiaming Li5 6 7, Yanling Fan5 6 7, Jing Qu2 3 7, Liang Sun8 9, Si Wang1 3 10, Yiyuan Zhang4, Shanshan Yang10, Zunpeng Liu2 7, Zeming Wu2 7, Sheng Zhang4 7, Qiaoran Wang5 6 7, Aihua Zheng7 11, Shuguang Duo12, Yang Yu13 14, Juan Carlos Izpisua Belmonte15, Piu Chan10, Qi Zhou2 3 7, Moshi Song16 17 18, Weiqi Zhang19 20 21, Guang-Hui Liu22 23 24 25 26

    1. 1 State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.
    2. 2 State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.
    3. 3 Institute for Stem cell and Regeneration, Chinese Academy of Sciences, Beijing, 100101, China.
    4. 4 National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China.
    5. 5 CAS Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, 100101, China.
    6. 6 China National Center for Bioinformation, Beijing, 100101, China.
    7. 7 University of Chinese Academy of Sciences, Beijing, 100049, China.
    8. 8 The MOH Key Laboratory of Geriatrics, Beijing Hospital, National Center of Gerontology, Beijing, 100730, China.
    9. 9 NHC Key Laboratory of Drug Addiction Medicine, Kunming Medical University, Kunming, Yunnan, 650223, China.
    10. 10 Advanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing, 100053, China.
    11. 11 State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.
    12. 12 Laboratory Animal Center, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.
    13. 13 Department of Obstetrics and Gynecology, Center for Reproductive Medicine, Peking University Third Hospital, Beijing, 100191, China.
    14. 14 Stem Cell Research Center, Peking University Third Hospital, Beijing, 100191, China.
    15. 15 Gene Expression Laboratory, Salk Institute for Biological Studies, La Jolla, CA, 92037, USA.
    16. 16 State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China. songmoshi@ioz.ac.cn.
    17. 17 Institute for Stem cell and Regeneration, Chinese Academy of Sciences, Beijing, 100101, China. songmoshi@ioz.ac.cn.
    18. 18 University of Chinese Academy of Sciences, Beijing, 100049, China. songmoshi@ioz.ac.cn.
    19. 19 CAS Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, 100101, China. zhangwq@big.ac.cn.
    20. 20 China National Center for Bioinformation, Beijing, 100101, China. zhangwq@big.ac.cn.
    21. 21 University of Chinese Academy of Sciences, Beijing, 100049, China. zhangwq@big.ac.cn.
    22. 22 State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China. ghliu@ioz.ac.cn.
    23. 23 Institute for Stem cell and Regeneration, Chinese Academy of Sciences, Beijing, 100101, China. ghliu@ioz.ac.cn.
    24. 24 National Laboratory of Biomacromolecules, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China. ghliu@ioz.ac.cn.
    25. 25 University of Chinese Academy of Sciences, Beijing, 100049, China. ghliu@ioz.ac.cn.
    26. 26 Advanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing, 100053, China. ghliu@ioz.ac.cn.

    Aging is a major risk factor for many diseases, especially in highly prevalent cardiopulmonary comorbidities and infectious diseases including Coronavirus Disease 2019 (COVID-19). Resolving cellular and molecular mechanisms associated with aging in higher mammals is therefore urgently needed. Here, we created young and old non-human primate single-nucleus/cell transcriptomic atlases of lung, heart and artery, the top tissues targeted by SARS-CoV-2. Analysis of cell type-specific aging-associated transcriptional changes revealed increased systemic inflammation and compromised virus defense as a hallmark of cardiopulmonary aging. With age, expression of the SARS-CoV-2 receptor angiotensin-converting enzyme 2 (ACE2) was increased in the pulmonary alveolar epithelial barrier, cardiomyocytes, and vascular endothelial cells. We found that interleukin 7 (IL7) accumulated in aged cardiopulmonary tissues and induced ACE2 expression in human vascular endothelial cells in an NF-κB-dependent manner. Furthermore, treatment with vitamin C blocked IL7-induced ACE2 expression. Altogether, our findings depict the first transcriptomic atlas of the aged primate cardiopulmonary system and provide vital insights into age-linked susceptibility to SARS-CoV-2, suggesting that geroprotective strategies may reduce COVID-19 severity in the elderly.