IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41529-7.html
   My bibliography  Save this article

Efficient intervention for pulmonary fibrosis via mitochondrial transfer promoted by mitochondrial biogenesis

Author

Listed:
  • Ting Huang

    (Zhejiang University)

  • Ruyi Lin

    (Zhejiang University)

  • Yuanqin Su

    (Zhejiang University
    Zhejiang University)

  • Hao Sun

    (Zhejiang University)

  • Xixi Zheng

    (Zhejiang University
    Zhejiang University)

  • Jinsong Zhang

    (Zhejiang University)

  • Xiaoyan Lu

    (Zhejiang University)

  • Baiqin Zhao

    (Zhejiang University School of Medicine)

  • Xinchi Jiang

    (Zhejiang University)

  • Lingling Huang

    (Zhejiang University School of Medicine)

  • Ni Li

    (Ningbo University)

  • Jing Shi

    (Hangzhou Medical College)

  • Xiaohui Fan

    (Zhejiang University
    Zhejiang University)

  • Donghang Xu

    (Zhejiang University School of Medicine)

  • Tianyuan Zhang

    (Zhejiang University
    Zhejiang University
    Zhejiang University)

  • Jianqing Gao

    (Zhejiang University
    Zhejiang University
    Zhejiang University School of Medicine
    Zhejiang University)

Abstract

The use of exogenous mitochondria to replenish damaged mitochondria has been proposed as a strategy for the treatment of pulmonary fibrosis. However, the success of this strategy is partially restricted by the difficulty of supplying sufficient mitochondria to diseased cells. Herein, we report the generation of high-powered mesenchymal stem cells with promoted mitochondrial biogenesis and facilitated mitochondrial transfer to injured lung cells by the sequential treatment of pioglitazone and iron oxide nanoparticles. This highly efficient mitochondrial transfer is shown to not only restore mitochondrial homeostasis but also reactivate inhibited mitophagy, consequently recovering impaired cellular functions. We perform studies in mouse to show that these high-powered mesenchymal stem cells successfully mitigate fibrotic progression in a progressive fibrosis model, which was further verified in a humanized multicellular lung spheroid model. The present findings provide a potential strategy to overcome the current limitations in mitochondrial replenishment therapy, thereby promoting therapeutic applications for fibrotic intervention.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41529-7
    DOI: 10.1038/s41467-023-41529-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41529-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41529-7?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. Kazuhide Hayakawa & Elga Esposito & Xiaohua Wang & Yasukazu Terasaki & Yi Liu & Changhong Xing & Xunming Ji & Eng H. Lo, 2016. "Correction: Corrigendum: Transfer of mitochondria from astrocytes to neurons after stroke," Nature, Nature, vol. 539(7627), pages 123-123, November.
    2. 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.
    3. Kazuhide Hayakawa & Elga Esposito & Xiaohua Wang & Yasukazu Terasaki & Yi Liu & Changhong Xing & Xunming Ji & Eng H. Lo, 2016. "Transfer of mitochondria from astrocytes to neurons after stroke," Nature, Nature, vol. 535(7613), pages 551-555, July.
    4. Michael T. Lin & M. Flint Beal, 2006. "Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases," Nature, Nature, vol. 443(7113), pages 787-795, October.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Peng Liao & Long Chen & Hao Zhou & Jiong Mei & Ziming Chen & Bingqi Wang & Jerry Q. Feng & Guangyi Li & Sihan Tong & Jian Zhou & Siyuan Zhu & Yu Qian & Yao Zong & Weiguo Zou & Hao Li & Wenkan Zhang & , 2024. "Osteocyte mitochondria regulate angiogenesis of transcortical vessels," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    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. Peng Liao & Long Chen & Hao Zhou & Jiong Mei & Ziming Chen & Bingqi Wang & Jerry Q. Feng & Guangyi Li & Sihan Tong & Jian Zhou & Siyuan Zhu & Yu Qian & Yao Zong & Weiguo Zou & Hao Li & Wenkan Zhang & , 2024. "Osteocyte mitochondria regulate angiogenesis of transcortical vessels," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Jinjian Huang & Rong Yang & Jiao Jiao & Ze Li & Penghui Wang & Ye Liu & Sicheng Li & Canwen Chen & Zongan Li & Guiwen Qu & Kang Chen & Xiuwen Wu & Bo Chi & Jianan Ren, 2023. "A click chemistry-mediated all-peptide cell printing hydrogel platform for diabetic wound healing," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Yueli Yang & Xueyang Bai & Fanghao Hu, 2024. "Photoswitchable polyynes for multiplexed stimulated Raman scattering microscopy with reversible light control," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    4. Minfeng Huo & Zhimin Tang & Liying Wang & Linlin Zhang & Haiyan Guo & Yu Chen & Ping Gu & Jianlin Shi, 2022. "Magnesium hexacyanoferrate nanocatalysts attenuate chemodrug-induced cardiotoxicity through an anti-apoptosis mechanism driven by modulation of ferrous iron," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Mohsen S. Al-Omar & Mamuna Naz & Salman A. A. Mohammed & Momina Mansha & Mohd N. Ansari & Najeeb U. Rehman & Mehnaz Kamal & Hamdoon A. Mohammed & Mohammad Yusuf & Abubaker M. Hamad & Naseem Akhtar & R, 2020. "Pyrethroid-Induced Organ Toxicity and Anti-Oxidant-Supplemented Amelioration of Toxicity and Organ Damage: The Protective Roles of Ascorbic Acid and α-Tocopherol," IJERPH, MDPI, vol. 17(17), pages 1-28, August.
    6. Xin Liu, 2018. "The Effect of Rotenone on Ndfip1 in MES23.5 Cells," International Journal of Sciences, Office ijSciences, vol. 7(05), pages 39-43, May.
    7. Matthias Kettwig & Katharina Ternka & Kristin Wendland & Dennis Manfred Krüger & Silvia Zampar & Charlotte Schob & Jonas Franz & Abhishek Aich & Anne Winkler & M. Sadman Sakib & Lalit Kaurani & Robert, 2021. "Interferon-driven brain phenotype in a mouse model of RNaseT2 deficient leukoencephalopathy," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    8. Cesare Granata & Nikeisha J. Caruana & Javier Botella & Nicholas A. Jamnick & Kevin Huynh & Jujiao Kuang & Hans A. Janssen & Boris Reljic & Natalie A. Mellett & Adrienne Laskowski & Tegan L. Stait & A, 2021. "High-intensity training induces non-stoichiometric changes in the mitochondrial proteome of human skeletal muscle without reorganisation of respiratory chain content," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    9. Ziqi Liu & Fuhu Guo & Yufan Zhu & Shengnan Qin & Yuchen Hou & Haotian Guo & Feng Lin & Peng R. Chen & Xinyuan Fan, 2024. "Bioorthogonal photocatalytic proximity labeling in primary living samples," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Chaiheon Lee & Mingyu Park & W. C. Bhashini Wijesinghe & Seungjin Na & Chae Gyu Lee & Eunhye Hwang & Gwangsu Yoon & Jeong Kyeong Lee & Deok-Ho Roh & Yoon Hee Kwon & Jihyeon Yang & Sebastian A. Hughes , 2024. "Oxidative photocatalysis on membranes triggers non-canonical pyroptosis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Ying Shao & Zhongli Chen & Lingling Wu, 2019. "Oxidative Stress Effects of Soluble Sulfide on Human Hepatocyte Cell Line LO2," IJERPH, MDPI, vol. 16(9), pages 1-11, May.
    12. Cheng-Jie Zhou & Xing-Yue Wang & Yan-Hua Dong & Dong-Hui Wang & Zhe Han & Xiao-Jie Zhang & Qing-Yuan Sun & John Carroll & Cheng-Guang Liang, 2022. "CENP-F-dependent DRP1 function regulates APC/C activity during oocyte meiosis I," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Pankaj C. Patel & Marcus T. Wolfe, 2021. "Under Pressure: The Effect of Antioxidants on Health Consequences Related to Oxidative Stress," Entrepreneurship Theory and Practice, , vol. 45(1), pages 211-241, January.
    14. Ami Kobayashi & Kotaro Azuma & Toshihiko Takeiwa & Toshimori Kitami & Kuniko Horie & Kazuhiro Ikeda & Satoshi Inoue, 2023. "A FRET-based respirasome assembly screen identifies spleen tyrosine kinase as a target to improve muscle mitochondrial respiration and exercise performance in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Su-Youn Cho & Hee-Tae Roh, 2022. "Effects of Exercise Training on Neurotrophic Factors and Blood–Brain Barrier Permeability in Young-Old and Old-Old Women," IJERPH, MDPI, vol. 19(24), pages 1-10, 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:14:y:2023:i:1:d:10.1038_s41467-023-41529-7. 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.