IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43529-z.html
   My bibliography  Save this article

MicroRNA-mediated attenuation of branched-chain amino acid catabolism promotes ferroptosis in chronic kidney disease

Author

Listed:
  • Hisakatsu Sone

    (Augusta University)

  • Tae Jin Lee

    (Augusta University)

  • Byung Rho Lee

    (Augusta University)

  • Dan Heo

    (Augusta University)

  • Sekyung Oh

    (Catholic Kwandong University College of Medicine)

  • Sang-Ho Kwon

    (Augusta University)

Abstract

Chronic kidney disease can develop from kidney injury incident to chemotherapy with cisplatin, which complicates the prognosis of cancer patients. MicroRNAs regulate gene expression by pairing with specific sets of messenger RNAs. Therefore, elucidating direct physical interactions between microRNAs and their target messenger RNAs can help decipher crucial biological processes associated with cisplatin-induced kidney injury. Through intermolecular ligation and transcriptome-wide sequencing, we here identify direct pairs of microRNAs and their target messenger RNAs in the kidney of male mice injured by cisplatin. We find that a group of cisplatin-induced microRNAs can target select messenger RNAs that affect the mitochondrial metabolic pathways in the injured kidney. Specifically, a cisplatin-induced microRNA, miR-429-3p, suppresses the pathway that catabolizes branched-chain amino acids in the proximal tubule, leading to cell death dependent on lipid peroxidation, called ferroptosis. Identification of miRNA-429-3p-mediated ferroptosis stimulation suggests therapeutic potential for modulating the branched-chain amino acid pathway in ameliorating cisplatin-induced kidney injury.

Suggested Citation

  • Hisakatsu Sone & Tae Jin Lee & Byung Rho Lee & Dan Heo & Sekyung Oh & Sang-Ho Kwon, 2023. "MicroRNA-mediated attenuation of branched-chain amino acid catabolism promotes ferroptosis in chronic kidney disease," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43529-z
    DOI: 10.1038/s41467-023-43529-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43529-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43529-z?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. Eric L. Nostrand & Peter Freese & Gabriel A. Pratt & Xiaofeng Wang & Xintao Wei & Rui Xiao & Steven M. Blue & Jia-Yu Chen & Neal A. L. Cody & Daniel Dominguez & Sara Olson & Balaji Sundararaman & Liju, 2020. "A large-scale binding and functional map of human RNA-binding proteins," Nature, Nature, vol. 583(7818), pages 711-719, July.
    2. Froukje Vanweert & Michael Neinast & Edmundo Erazo Tapia & Tineke Weijer & Joris Hoeks & Vera B. Schrauwen-Hinderling & Megan C. Blair & Marc R. Bornstein & Matthijs K. C. Hesselink & Patrick Schrauwe, 2022. "A randomized placebo-controlled clinical trial for pharmacological activation of BCAA catabolism in patients with type 2 diabetes," Nature Communications, Nature, vol. 13(1), pages 1-9, 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. Haofan Sun & Bin Fu & Xiaohong Qian & Ping Xu & Weijie Qin, 2024. "Nuclear and cytoplasmic specific RNA binding proteome enrichment and its changes upon ferroptosis induction," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Timofey A. Karginov & Antoine Ménoret & Anthony T. Vella, 2022. "Optimal CD8+ T cell effector function requires costimulation-induced RNA-binding proteins that reprogram the transcript isoform landscape," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Anna Knörlein & Chris P. Sarnowski & Tebbe Vries & Moritz Stoltz & Michael Götze & Ruedi Aebersold & Frédéric H.-T. Allain & Alexander Leitner & Jonathan Hall, 2022. "Nucleotide-amino acid π-stacking interactions initiate photo cross-linking in RNA-protein complexes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Johanna Luige & Alexandros Armaos & Gian Gaetano Tartaglia & Ulf Andersson Vang Ørom, 2024. "Predicting nuclear G-quadruplex RNA-binding proteins with roles in transcription and phase separation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Tamar Sapir & Aditya Kshirsagar & Anna Gorelik & Tsviya Olender & Ziv Porat & Ingrid E. Scheffer & David B. Goldstein & Orrin Devinsky & Orly Reiner, 2022. "Heterogeneous nuclear ribonucleoprotein U (HNRNPU) safeguards the developing mouse cortex," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Erika Schaudy & Kathrin Hölz & Jory Lietard & Mark M. Somoza, 2022. "Simple synthesis of massively parallel RNA microarrays via enzymatic conversion from DNA microarrays," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    7. Mariela Cortés-López & Laura Schulz & Mihaela Enculescu & Claudia Paret & Bea Spiekermann & Mathieu Quesnel-Vallières & Manuel Torres-Diz & Sebastian Unic & Anke Busch & Anna Orekhova & Monika Kuban &, 2022. "High-throughput mutagenesis identifies mutations and RNA-binding proteins controlling CD19 splicing and CART-19 therapy resistance," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Zili Song & Shuang Zhou & Hongjiao Zhang & Nancy P. Keller & Berl R. Oakley & Xiao Liu & Wen-Bing Yin, 2023. "Fungal secondary metabolism is governed by an RNA-binding protein CsdA/RsdA complex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Wei Hu & Yangjun Wu & Qili Shi & Jingni Wu & Deping Kong & Xiaohua Wu & Xianghuo He & Teng Liu & Shengli Li, 2022. "Systematic characterization of cancer transcriptome at transcript resolution," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. Xiangbin Ruan & Kaining Hu & Xiaochang Zhang, 2023. "PIE-seq: identifying RNA-binding protein targets by dual RNA-deaminase editing and sequencing," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. David Wang & Mathieu Quesnel-Vallieres & San Jewell & Moein Elzubeir & Kristen Lynch & Andrei Thomas-Tikhonenko & Yoseph Barash, 2023. "A Bayesian model for unsupervised detection of RNA splicing based subtypes in cancers," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Haoran Zhu & Yuning Yang & Yunhe Wang & Fuzhou Wang & Yujian Huang & Yi Chang & Ka-chun Wong & Xiangtao Li, 2023. "Dynamic characterization and interpretation for protein-RNA interactions across diverse cellular conditions using HDRNet," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    13. Scott D. Findlay & Lindsay Romo & Christopher B. Burge, 2024. "Quantifying negative selection in human 3ʹ UTRs uncovers constrained targets of RNA-binding proteins," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Xianjun Dong & Yunfei Bai & Zhixiang Liao & David Gritsch & Xiaoli Liu & Tao Wang & Rebeca Borges-Monroy & Alyssa Ehrlich & Geidy E. Serrano & Mel B. Feany & Thomas G. Beach & Clemens R. Scherzer, 2023. "Circular RNAs in the human brain are tailored to neuron identity and neuropsychiatric disease," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    15. JohnCarlo Kristofich & Christopher V. Nicchitta, 2023. "Signal-noise metrics for RNA binding protein identification reveal broad spectrum protein-RNA interaction frequencies and dynamics," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    16. Qiong Guo & Shidong Zhao & Rosario Francisco-Velilla & Jiahai Zhang & Azman Embarc-Buh & Salvador Abellan & Mengqi Lv & Peiping Tang & Qingguo Gong & Huaizong Shen & Linfeng Sun & Xuebiao Yao & Jinron, 2022. "Structural basis for Gemin5 decamer-mediated mRNA binding," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    17. Arashdeep Singh & Arati Rajeevan & Vishaka Gopalan & Piyush Agrawal & Chi-Ping Day & Sridhar Hannenhalli, 2022. "Broad misappropriation of developmental splicing profile by cancer in multiple organs," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    18. Jian Han & Omer An & Xi Ren & Yangyang Song & Sze Jing Tang & Haoqing Shen & Xinyu Ke & Vanessa Hui En Ng & Daryl Jin Tai Tay & Hui Qing Tan & Dennis Kappei & Henry Yang & Leilei Chen, 2022. "Multilayered control of splicing regulatory networks by DAP3 leads to widespread alternative splicing changes in cancer," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. Michelle Maurin & Mohammadreza Ranjouri & Cristina Megino-Luque & Justin Y. Newberg & Dongliang Du & Katelyn Martin & Robert E. Miner & Mollie S. Prater & Dave Keng Boon Wee & Barbara Centeno & Shondr, 2023. "RBFOX2 deregulation promotes pancreatic cancer progression and metastasis through alternative splicing," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Michelle M. Kameda-Smith & Helen Zhu & En-Ching Luo & Yujin Suk & Agata Xella & Brian Yee & Chirayu Chokshi & Sansi Xing & Frederick Tan & Raymond G. Fox & Ashley A. Adile & David Bakhshinyan & Kevin , 2022. "Characterization of an RNA binding protein interactome reveals a context-specific post-transcriptional landscape of MYC-amplified medulloblastoma," Nature Communications, Nature, vol. 13(1), pages 1-19, 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_s41467-023-43529-z. 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.