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Intracellular energy controls dynamics of stress-induced ribonucleoprotein granules

Author

Listed:
  • Tao Wang

    (Johns Hopkins University
    Johns Hopkins University)

  • Xibin Tian

    (Johns Hopkins University
    Johns Hopkins University)

  • Han Byeol Kim

    (Johns Hopkins University)

  • Yura Jang

    (Johns Hopkins University)

  • Zhiyuan Huang

    (Johns Hopkins University
    Johns Hopkins University)

  • Chan Hyun Na

    (Johns Hopkins University)

  • Jiou Wang

    (Johns Hopkins University
    Johns Hopkins University)

Abstract

Energy metabolism and membraneless organelles have been implicated in human diseases including neurodegeneration. How energy deficiency regulates ribonucleoprotein particles such as stress granules (SGs) is still unclear. Here we identified a unique type of granules induced by energy deficiency under physiological conditions and uncovered the mechanisms by which the dynamics of diverse stress-induced granules are regulated. Severe energy deficiency induced the rapid formation of energy deficiency-induced stress granules (eSGs) independently of eIF2α phosphorylation, whereas moderate energy deficiency delayed the clearance of conventional SGs. The formation of eSGs or the clearance of SGs was regulated by the mTOR-4EBP1-eIF4E pathway or eIF4A1, involving assembly of the eIF4F complex or RNA condensation, respectively. In neurons or brain organoids derived from patients carrying the C9orf72 repeat expansion associated with amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), the eSG formation was enhanced, and the clearance of conventional SGs was impaired. These results reveal a critical role for intracellular energy in the regulation of diverse granules and suggest that disruptions in energy-controlled granule dynamics may contribute to the pathogenesis of relevant diseases.

Suggested Citation

  • Tao Wang & Xibin Tian & Han Byeol Kim & Yura Jang & Zhiyuan Huang & Chan Hyun Na & Jiou Wang, 2022. "Intracellular energy controls dynamics of stress-induced ribonucleoprotein granules," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33079-1
    DOI: 10.1038/s41467-022-33079-1
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    References listed on IDEAS

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    1. Hong Joo Kim & Nam Chul Kim & Yong-Dong Wang & Emily A. Scarborough & Jennifer Moore & Zamia Diaz & Kyle S. MacLea & Brian Freibaum & Songqing Li & Amandine Molliex & Anderson P. Kanagaraj & Robert Ca, 2013. "Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS," Nature, Nature, vol. 495(7442), pages 467-473, March.
    2. Zhong-Wei Du & Hong Chen & Huisheng Liu & Jianfeng Lu & Kun Qian & CindyTzu-Ling Huang & Xiaofen Zhong & Frank Fan & Su-Chun Zhang, 2015. "Generation and expansion of highly pure motor neuron progenitors from human pluripotent stem cells," Nature Communications, Nature, vol. 6(1), pages 1-9, May.
    3. Maneka Chitiprolu & Chantal Jagow & Veronique Tremblay & Emma Bondy-Chorney & Geneviève Paris & Alexandre Savard & Gareth Palidwor & Francesca A. Barry & Lorne Zinman & Julia Keith & Ekaterina Rogaeva, 2018. "A complex of C9ORF72 and p62 uses arginine methylation to eliminate stress granules by autophagy," Nature Communications, Nature, vol. 9(1), pages 1-18, December.
    4. Lindsay A. Becker & Brenda Huang & Gregor Bieri & Rosanna Ma & David A. Knowles & Paymaan Jafar-Nejad & James Messing & Hong Joo Kim & Armand Soriano & Georg Auburger & Stefan M. Pulst & J. Paul Taylo, 2017. "Therapeutic reduction of ataxin-2 extends lifespan and reduces pathology in TDP-43 mice," Nature, Nature, vol. 544(7650), pages 367-371, April.
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    1. Florian Pernin & Qiao-Ling Cui & Abdulshakour Mohammadnia & Milton G. F. Fernandes & Jeffery A. Hall & Myriam Srour & Roy W. R. Dudley & Stephanie E. J. Zandee & Wendy Klement & Alexandre Prat & Hanna, 2024. "Regulation of stress granule formation in human oligodendrocytes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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