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Stem Leydig cells support macrophage immunological homeostasis through mitochondrial transfer in mice

Author

Listed:
  • Ani Chi

    (Sun Yat-sen University
    South China University of Technology
    The First Affiliated Hospital of Sun Yat-sen University)

  • Bicheng Yang

    (Sun Yat-sen University)

  • Hao Dai

    (South China University of Technology)

  • Xinyu Li

    (Sun Yat-sen University)

  • Jiahui Mo

    (Sun Yat-sen University)

  • Yong Gao

    (The First Affiliated Hospital of Sun Yat-sen University)

  • Zhihong Chen

    (Sun Yat-sen University)

  • Xin Feng

    (Sun Yat-sen University)

  • Menghui Ma

    (Sun Yat-sen University)

  • Yanqing Li

    (Sun Yat-sen University)

  • Chao Yang

    (South China University of Technology)

  • Jie Liu

    (South China University of Technology)

  • Hanchao Liu

    (Sun Yat-sen University)

  • Zhenqing Wang

    (Sun Yat-sen University)

  • Feng Gao

    (Sun Yat-sen University
    The First Affiliated Hospital of Sun Yat-sen University)

  • Yan Liao

    (South China University of Technology)

  • Xuetao Shi

    (South China University of Technology
    National Engineering Research Centre for Tissue Restoration and Reconstruction and Key Laboratory of Biomedical Engineering of Guangdong Province South China University of Technology
    Shenzhen Beike Biotechnology Co., Ltd.)

  • Chunhua Deng

    (Sun Yat-sen University)

  • Min Zhang

    (Sun Yat-sen University
    The First Affiliated Hospital of Sun Yat-sen University)

Abstract

As testicular mesenchymal stromal cells, stem Leydig cells (SLCs) show great promise in the treatment of male hypogonadism. The therapeutic functions of mesenchymal stromal cells are largely determined by their reciprocal regulation by immune responses. However, the immunoregulatory properties of SLCs remain unclear. Here, we observe that SLCs transplantation restore male fertility and testosterone production in an ischemia‒reperfusion injury mouse model. SLCs prevent inflammatory cascades through mitochondrial transfer to macrophages. Reactive oxygen species (ROS) released from activated macrophages inducing mitochondrial transfer from SLCs to macrophages in a transient receptor potential cation channel subfamily member 7 (TRPM7)-mediated manner. Notably, knockdown of TRPM7 in transplanted SLCs compromised therapeutic outcomes in both testicular ischemia‒reperfusion and testicular aging mouse models. These findings reveal a new mechanism of SLCs transplantation that may contribute to preserve testis function in male patients with hypogonadism related to immune disorders.

Suggested Citation

  • Ani Chi & Bicheng Yang & Hao Dai & Xinyu Li & Jiahui Mo & Yong Gao & Zhihong Chen & Xin Feng & Menghui Ma & Yanqing Li & Chao Yang & Jie Liu & Hanchao Liu & Zhenqing Wang & Feng Gao & Yan Liao & Xueta, 2024. "Stem Leydig cells support macrophage immunological homeostasis through mitochondrial transfer in mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46190-2
    DOI: 10.1038/s41467-024-46190-2
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    References listed on IDEAS

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    1. Senyu Yao & Xiaoyue Wei & Wenrui Deng & Boyan Wang & Jianye Cai & Yinong Huang & Xiaofan Lai & Yuan Qiu & Yi Wang & Yuanjun Guan & Jiancheng Wang, 2022. "Nestin-dependent mitochondria-ER contacts define stem Leydig cell differentiation to attenuate male reproductive ageing," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Yu-chi Shen & Adrienne Niederriter Shami & Lindsay Moritz & Hailey Larose & Gabriel L. Manske & Qianyi Ma & Xianing Zheng & Meena Sukhwani & Michael Czerwinski & Caleb Sultan & Haolin Chen & Stephen J, 2021. "TCF21+ mesenchymal cells contribute to testis somatic cell development, homeostasis, and regeneration in mice," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Amira A. Barkal & Rachel E. Brewer & Maxim Markovic & Mark Kowarsky & Sammy A. Barkal & Balyn W. Zaro & Venkatesh Krishnan & Jason Hatakeyama & Oliver Dorigo & Layla J. Barkal & Irving L. Weissman, 2019. "CD24 signalling through macrophage Siglec-10 is a target for cancer immunotherapy," Nature, Nature, vol. 572(7769), pages 392-396, August.
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