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CHIT1-positive microglia drive motor neuron aging in the primate spinal cord

Abstract

Aging is a critical factor in spinal cord-associated disorders1, yet aging-specific mechanisms underlying this relationship remain poorly understood. To address this knowledge gap, we combined single-nucleus RNA sequencing with behavioral and neurophysiological analysis in non-human primates (NHPs). We identified motor neuron senescence and neuroinflammation with microglial hyperactivation as intertwined hallmarks of spinal cord aging. As an underlying mechanism, we identified a previously unreported neurotoxic microglial state demarcated by elevated expression of CHIT1 (a secreted mammalian chitinase) specific to the aged spinal cords in NHP and human biopsies. In the aged spinal cord, CHIT1-positive microglia preferentially localize around motor neurons (MNs), and they are capable of triggering senescence, partly by activating SMAD signaling. We further validated the driving role of secreted CHIT1 on MN senescence by multi-modal experiments both in vivo, utilizing the NHP spinal cord as a model and in vitro, employing a sophisticated human MN-and-microenvironment interplay modeling system. Moreover, we demonstrated that ascorbic acid, a geroprotective compound, counteracted the pro-senescent effect of CHIT1 and mitigated motor neuron senescence in aged monkeys. Our findings provide the first single-cell resolution cellular and molecular landscape of the aged primate spinal cord and identify a new biomarker and intervention target for spinal cord degeneration.

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Author information

Author notes

  1. These authors contributed equally: Shuhui Sun, Jiaming Li, Si Wang, Jingyi Li, Jie Ren, Zhaoshi Bao, Le Sun, Xibo Ma

  2. These authors jointly supervised this work: Jing Qu, Weiqi Zhang, Guang-Hui Liu

Authors and Affiliations

  1. State Key Laboratory of Membrane Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

    Shuhui Sun, Jingyi Li, Shuai Ma, Yan Yu, Miyang Ma, Zeming Wu, Hui Zhang, Kaowen Yan, Yuanhan Yang, Sheng Zhang & Guang-Hui Liu

  2. State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

    Shuhui Sun, Min Wang, Xuebao Wang, Yixin Zhang, Zhao-Qian Teng, Chang-Mei Liu & Jing Qu

  3. Institute for Stem Cell and Regeneration, CAS, Beijing, China

    Shuhui Sun, Jingyi Li, Jie Ren, Shuai Ma, Zeming Wu, Kaowen Yan, Zhao-Qian Teng, Chang-Mei Liu, Jing Qu, Weiqi Zhang & Guang-Hui Liu

  4. Beijing Institute for Stem Cell and Regenerative Medicine, Beijing, China

    Shuhui Sun, Jingyi Li, Shuai Ma, Zeming Wu, Kaowen Yan, Zhao-Qian Teng, Chang-Mei Liu, Jing Qu & Guang-Hui Liu

  5. CAS Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing, China

    Jiaming Li, Jie Ren, Qiaoran Wang & Weiqi Zhang

  6. University of Chinese Academy of Sciences, Beijing, China

    Jiaming Li, Jingyi Li, Jie Ren, Shuai Ma, Yan Yu, Miyang Ma, Qiaoran Wang, Xuebao Wang, Hui Zhang, Yuanhan Yang, Yixin Zhang, Sheng Zhang, Zhao-Qian Teng, Chang-Mei Liu, Jing Qu, Weiqi Zhang & Guang-Hui Liu

  7. Advanced Innovation Center for Human Brain Protection, and National Clinical Research Center for Geriatric Disorders, Xuanwu Hospital Capital Medical University, Beijing, China

    Si Wang, Jinghui Lei & Guang-Hui Liu

  8. Aging Translational Medicine Center, International Center for Aging and Cancer, Xuanwu Hospital, Capital Medical University, Beijing, China

    Si Wang, Jinghui Lei & Guang-Hui Liu

  9. Aging Biomarker Consortium, Beijing, China

    Si Wang, Jingyi Li, Jie Ren, Shuai Ma, Liang Sun, Yan-Jiang Wang, Jian Li, Jing Qu, Weiqi Zhang & Guang-Hui Liu

  10. Key Laboratory of RNA Science and Engineering, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing, China

    Jie Ren

  11. Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China

    Zhaoshi Bao & Tao Jiang

  12. The Chinese Glioma Genome Atlas, Beijing, China

    Zhaoshi Bao & Tao Jiang

  13. Beijing Institute of Brain Disorders, Capital Medical University, Beijing, China

    Le Sun & Xiaoqun Wang

  14. MAIS, State Key Laboratory of Multimodal Artificial Intelligence Systems, Institute of Automation, Chinese Academy of Sciences, Beijing, China

    Xibo Ma, Zhiyuan Chen & He Ma

  15. School of Artificial Intelligence, University of Chinese Academy of Sciences, Beijing, China

    Xibo Ma & Zhiyuan Chen

  16. College of Medicine and Biomedical Information Engineering, Northeastern University, Shenyang, China

    Xibo Ma & He Ma

  17. Department of Neurology, The Fifth People’s Hospital of Chongqing, Chongqing, China

    Si Wang & Fangshuo Zheng

  18. The MOH Key Laboratory of Geriatrics, Beijing Hospital, National Center of Gerontology, Beijing, China

    Liang Sun & Jian Li

  19. University of Science and Technology of China, Hefei, China

    Min Wang

  20. The MOE Frontier Research Center of Brain & Brain-Machine Integration, Zhejiang University School of Brain Science and Brain Medicine, Hangzhou, China

    Ge Bai

  21. Department of Neurology, Daping Hospital, Third Military Medical University, Chongqing, China

    Yan-Jiang Wang

  22. State Key Laboratory of Trauma and Chemical Poisoning, Daping Hospital, Third Military Medical University, Chongqing, China

    Yan-Jiang Wang

  23. State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, New Cornerstone Science Laboratory, Beijing Normal University, Beijing, China

    Xiaoqun Wang

  24. Department of Neurosurgery, Xuanwu Hospital Capital Medical University, Beijing, China

    Guoguang Zhao

  25. Clinical Research Center for Epilepsy Capital Medical University, Beijing, China

    Guoguang Zhao

  26. Beijing Municipal Geriatric Medical Research Center, Beijing, China

    Guoguang Zhao

  27. Beijing Neurosurgical Institute, Beijing, China

    Tao Jiang

  28. Altos Labs, Inc., San Diego, CA, USA

    Juan Carlos Izpisua Belmonte

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  1. Shuhui Sun
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  37. Guang-Hui Liu
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Corresponding authors

Correspondence to
Jing Qu, Weiqi Zhang or Guang-Hui Liu.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Fig. 1 (the uncropped blots) and full legends for Supplementary Tables 1–11.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–11 – see Supplementary Information document for full descriptions.

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Cite this article

Sun, S., Li, J., Wang, S. et al. CHIT1-positive microglia drive motor neuron aging in the primate spinal cord.
Nature (2023). https://doi.org/10.1038/s41586-023-06783-1

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  • Published: 31 October 2023

  • DOI: https://doi.org/10.1038/s41586-023-06783-1

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