IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49159-3.html
   My bibliography  Save this article

Mitochondria from osteolineage cells regulate myeloid cell-mediated bone resorption

Author

Listed:
  • Peng Ding

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Chuan Gao

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Jian Zhou

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Jialun Mei

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Gan Li

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Delin Liu

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Hao Li

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Peng Liao

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Meng Yao

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Bingqi Wang

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Yafei Lu

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Xiaoyuan Peng

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Chenyi Jiang

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Jimin Yin

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Yigang Huang

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Minghao Zheng

    (University of Western Australia)

  • Youshui Gao

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Changqing Zhang

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

  • Junjie Gao

    (Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
    Shanghai Sixth People’s Hospital Affiliated to Shanghai Jiao Tong University School of Medicine)

Abstract

Interactions between osteolineage cells and myeloid cells play important roles in maintaining skeletal homeostasis. Herein, we find that osteolineage cells transfer mitochondria to myeloid cells. Impairment of the transfer of mitochondria by deleting MIRO1 in osteolineage cells leads to increased myeloid cell commitment toward osteoclastic lineage cells and promotes bone resorption. In detail, impaired mitochondrial transfer from osteolineage cells alters glutathione metabolism and protects osteoclastic lineage cells from ferroptosis, thus promoting osteoclast activities. Furthermore, mitochondrial transfer from osteolineage cells to myeloid cells is involved in the regulation of glucocorticoid-induced osteoporosis, and glutathione depletion alleviates the progression of glucocorticoid-induced osteoporosis. These findings reveal an unappreciated mechanism underlying the interaction between osteolineage cells and myeloid cells to regulate skeletal metabolic homeostasis and provide insights into glucocorticoid-induced osteoporosis progression.

Suggested Citation

  • Peng Ding & Chuan Gao & Jian Zhou & Jialun Mei & Gan Li & Delin Liu & Hao Li & Peng Liao & Meng Yao & Bingqi Wang & Yafei Lu & Xiaoyuan Peng & Chenyi Jiang & Jimin Yin & Yigang Huang & Minghao Zheng &, 2024. "Mitochondria from osteolineage cells regulate myeloid cell-mediated bone resorption," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49159-3
    DOI: 10.1038/s41467-024-49159-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49159-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49159-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Simón Méndez-Ferrer & Tatyana V. Michurina & Francesca Ferraro & Amin R. Mazloom & Ben D. MacArthur & Sergio A. Lira & David T. Scadden & Avi Ma’ayan & Grigori N. Enikolopov & Paul S. Frenette, 2010. "Mesenchymal and haematopoietic stem cells form a unique bone marrow niche," Nature, Nature, vol. 466(7308), pages 829-834, August.
    2. Masayuki Furuya & Junichi Kikuta & Sayumi Fujimori & Shigeto Seno & Hiroki Maeda & Mai Shirazaki & Maki Uenaka & Hiroki Mizuno & Yoriko Iwamoto & Akito Morimoto & Kunihiko Hashimoto & Takeshi Ito & Yu, 2018. "Direct cell–cell contact between mature osteoblasts and osteoclasts dynamically controls their functions in vivo," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Karolina Piekarska & Zuzanna Urban-Wójciuk & Małgorzta Kurkowiak & Iwona Pelikant-Małecka & Adriana Schumacher & Justyna Sakowska & Jan Henryk Spodnik & Łukasz Arcimowicz & Hanna Zielińska & Bogusław , 2022. "Mesenchymal stem cells transfer mitochondria to allogeneic Tregs in an HLA-dependent manner improving their immunosuppressive activity," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xianzhu Zhang & Wei Jiang & Chang Xie & Xinyu Wu & Qian Ren & Fei Wang & Xilin Shen & Yi Hong & Hongwei Wu & Youguo Liao & Yi Zhang & Renjie Liang & Wei Sun & Yuqing Gu & Tao Zhang & Yishan Chen & Wei, 2022. "Msx1+ stem cells recruited by bioactive tissue engineering graft for bone regeneration," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Taichi Nakatani & Tatsuki Sugiyama & Yoshiki Omatsu & Hitomi Watanabe & Gen Kondoh & Takashi Nagasawa, 2023. "Ebf3+ niche-derived CXCL12 is required for the localization and maintenance of hematopoietic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Maki Uenaka & Erika Yamashita & Junichi Kikuta & Akito Morimoto & Tomoka Ao & Hiroki Mizuno & Masayuki Furuya & Tetsuo Hasegawa & Hiroyuki Tsukazaki & Takao Sudo & Keizo Nishikawa & Daisuke Okuzaki & , 2022. "Osteoblast-derived vesicles induce a switch from bone-formation to bone-resorption in vivo," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Runfeng Miao & Harim Chun & Xing Feng & Ana Cordeiro Gomes & Jungmin Choi & João P. Pereira, 2022. "Competition between hematopoietic stem and progenitor cells controls hematopoietic stem cell compartment size," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Christina M. Termini & Amara Pang & Tiancheng Fang & Martina Roos & Vivian Y. Chang & Yurun Zhang & Nicollette J. Setiawan & Lia Signaevskaia & Michelle Li & Mindy M. Kim & Orel Tabibi & Paulina K. Li, 2021. "Neuropilin 1 regulates bone marrow vascular regeneration and hematopoietic reconstitution," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    6. Alicia Villatoro & Vincent Cuminetti & Aurora Bernal & Carlos Torroja & Itziar Cossío & Alberto Benguría & Marc Ferré & Joanna Konieczny & Enrique Vázquez & Andrea Rubio & Peter Utnes & Almudena Tello, 2023. "Endogenous IL-1 receptor antagonist restricts healthy and malignant myeloproliferation," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    7. Trent D. Hall & Hyunjin Kim & Mahmoud Dabbah & Jacquelyn A. Myers & Jeremy Chase Crawford & Antonio Morales-Hernandez & Claire E. Caprio & Pramika Sriram & Emilia Kooienga & Marta Derecka & Esther A. , 2022. "Murine fetal bone marrow does not support functional hematopoietic stem and progenitor cells until birth," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Ting Huang & Ruyi Lin & Yuanqin Su & Hao Sun & Xixi Zheng & Jinsong Zhang & Xiaoyan Lu & Baiqin Zhao & Xinchi Jiang & Lingling Huang & Ni Li & Jing Shi & Xiaohui Fan & Donghang Xu & Tianyuan Zhang & J, 2023. "Efficient intervention for pulmonary fibrosis via mitochondrial transfer promoted by mitochondrial biogenesis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Madison L. Doolittle & Dominik Saul & Japneet Kaur & Jennifer L. Rowsey & Stephanie J. Vos & Kevin D. Pavelko & Joshua N. Farr & David G. Monroe & Sundeep Khosla, 2023. "Multiparametric senescent cell phenotyping reveals targets of senolytic therapy in the aged murine skeleton," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    10. Adrienne Anginot & Julie Nguyen & Zeina Abou Nader & Vincent Rondeau & Amélie Bonaud & Maria Kalogeraki & Antoine Boutin & Julia P. Lemos & Valeria Bisio & Joyce Koenen & Lea Hanna Doumit Sakr & Amand, 2023. "WHIM Syndrome-linked CXCR4 mutations drive osteoporosis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    11. Yongkuk Park & Tadatoshi Sato & Jungwoo Lee, 2023. "Functional and analytical recapitulation of osteoclast biology on demineralized bone paper," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    12. M. Gabriele Bixel & Kishor K. Sivaraj & Melanie Timmen & Vishal Mohanakrishnan & Anusha Aravamudhan & Susanne Adams & Bong-Ihn Koh & Hyun-Woo Jeong & Kai Kruse & Richard Stange & Ralf H. Adams, 2024. "Angiogenesis is uncoupled from osteogenesis during calvarial bone regeneration," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    13. Yinghui Li & Mei He & Wenshan Zhang & Wei Liu & Hui Xu & Ming Yang & Hexiao Zhang & Haiwei Liang & Wenjing Li & Zhaozhao Wu & Weichao Fu & Shiqi Xu & Xiaolei Liu & Sibin Fan & Liwei Zhou & Chaoqun Wan, 2023. "Expansion of human megakaryocyte-biased hematopoietic stem cells by biomimetic Microniche," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    14. Jia Q. Ng & Toghrul H. Jafarov & Christopher B. Little & Tongtong Wang & Abdullah M. Ali & Yan Ma & Georgette A. Radford & Laura Vrbanac & Mari Ichinose & Samuel Whittle & David J. Hunter & Tamsin R. , 2023. "Loss of Grem1-lineage chondrogenic progenitor cells causes osteoarthritis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49159-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.