IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30067-3.html
   My bibliography  Save this article

RNA supply drives physiological granule assembly in neurons

Author

Listed:
  • Karl E. Bauer

    (Ludwig Maximilians University)

  • Niklas Bargenda

    (Ludwig Maximilians University)

  • Rico Schieweck

    (Ludwig Maximilians University)

  • Christin Illig

    (Ludwig Maximilians University)

  • Inmaculada Segura

    (Ludwig Maximilians University
    Max Planck Institute for Biological Intelligence (in foundation))

  • Max Harner

    (Ludwig Maximilians University)

  • Michael A. Kiebler

    (Ludwig Maximilians University)

Abstract

Membraneless cytoplasmic condensates of mRNAs and proteins, known as RNA granules, play pivotal roles in the regulation of mRNA fate. Their maintenance fine-tunes time and location of protein expression, affecting many cellular processes, which require complex protein distribution. Here, we report that RNA granules—monitored by DEAD-Box helicase 6 (DDX6)—disassemble during neuronal maturation both in cell culture and in vivo. This process requires neuronal function, as synaptic inhibition results in reversible granule assembly. Importantly, granule assembly is dependent on the RNA-binding protein Staufen2, known for its role in RNA localization. Altering the levels of free cytoplasmic mRNA reveals that RNA availability facilitates DDX6 granule formation. Specifically depleting RNA from DDX6 granules confirms RNA as an important driver of granule formation. Moreover, RNA is required for DDX6 granule assembly upon synaptic inhibition. Together, this data demonstrates how RNA supply favors RNA granule assembly, which not only impacts subcellular RNA localization but also translation-dependent synaptic plasticity, learning, and memory.

Suggested Citation

  • Karl E. Bauer & Niklas Bargenda & Rico Schieweck & Christin Illig & Inmaculada Segura & Max Harner & Michael A. Kiebler, 2022. "RNA supply drives physiological granule assembly in neurons," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30067-3
    DOI: 10.1038/s41467-022-30067-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30067-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-30067-3?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. Wickham, Hadley, 2011. "The Split-Apply-Combine Strategy for Data Analysis," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 40(i01).
    2. Sebastien M. Weyn-Vanhentenryck & Huijuan Feng & Dmytro Ustianenko & Rachel Duffié & Qinghong Yan & Martin Jacko & Jose C. Martinez & Marianne Goodwin & Xuegong Zhang & Ulrich Hengst & Stavros Lomvard, 2018. "Precise temporal regulation of alternative splicing during neural development," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    3. Marina Garcia-Jove Navarro & Shunnichi Kashida & Racha Chouaib & Sylvie Souquere & Gérard Pierron & Dominique Weil & Zoher Gueroui, 2019. "RNA is a critical element for the sizing and the composition of phase-separated RNA–protein condensates," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    4. Zhong-Yi Wang & Evgeny Leushkin & Angélica Liechti & Svetlana Ovchinnikova & Katharina Mößinger & Thoomke Brüning & Coralie Rummel & Frank Grützner & Margarida Cardoso-Moreira & Peggy Janich & David G, 2020. "Transcriptome and translatome co-evolution in mammals," Nature, Nature, vol. 588(7839), pages 642-647, December.
    5. Kavya Vinayan Pushpalatha & Mathilde Solyga & Akira Nakamura & Florence Besse, 2022. "RNP components condense into repressive RNP granules in the aging brain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Maria Hondele & Ruchika Sachdev & Stephanie Heinrich & Juan Wang & Pascal Vallotton & Beatriz M. A. Fontoura & Karsten Weis, 2019. "DEAD-box ATPases are global regulators of phase-separated organelles," Nature, Nature, vol. 573(7772), pages 144-148, September.
    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. Kavya Vinayan Pushpalatha & Mathilde Solyga & Akira Nakamura & Florence Besse, 2022. "RNP components condense into repressive RNP granules in the aging brain," Nature Communications, Nature, vol. 13(1), pages 1-15, 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. Dolejš Martin & Forejt Michal, 2019. "Franziscean cadastre in landscape structure research: a systematic review," Quaestiones Geographicae, Sciendo, vol. 38(1), pages 131-144, March.
    2. Sheung Chun Ng & Abin Biswas & Trevor Huyton & Jürgen Schünemann & Simone Reber & Dirk Görlich, 2023. "Barrier properties of Nup98 FG phases ruled by FG motif identity and inter-FG spacer length," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Ravic Nijbroek & Kristin Piikki & Mats Söderström & Bas Kempen & Katrine G. Turner & Simeon Hengari & John Mutua, 2018. "Soil Organic Carbon Baselines for Land Degradation Neutrality: Map Accuracy and Cost Tradeoffs with Respect to Complexity in Otjozondjupa, Namibia," Sustainability, MDPI, vol. 10(5), pages 1-20, May.
    4. Merl, Robert & Stöckl, Thomas & Palan, Stefan, 2023. "Insider trading regulation and shorting constraints. Evaluating the joint effects of two market interventions," Journal of Banking & Finance, Elsevier, vol. 154(C).
    5. Miller, Christine M.F. & Waterhouse, Hannah & Harter, Thomas & Fadel, James G. & Meyer, Deanne, 2020. "Quantifying the uncertainty in nitrogen application and groundwater nitrate leaching in manure based cropping systems," Agricultural Systems, Elsevier, vol. 184(C).
    6. Elizabeth A. Werren & Geneva R. LaForce & Anshika Srivastava & Delia R. Perillo & Shaokun Li & Katherine Johnson & Safa Baris & Brandon Berger & Samantha L. Regan & Christian D. Pfennig & Sonja Munnik, 2024. "TREX tetramer disruption alters RNA processing necessary for corticogenesis in THOC6 Intellectual Disability Syndrome," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    7. Sarlas, Georgios & Páez, Antonio & Axhausen, Kay W., 2020. "Betweenness-accessibility: Estimating impacts of accessibility on networks," Journal of Transport Geography, Elsevier, vol. 84(C).
    8. Marin FOTACHE & Florin DUMITRU & Valerica GREAVU-SERBAN, 2015. "An Information Systems Master Programme in Romania. Some Commonalities and Specificities," Informatica Economica, Academy of Economic Studies - Bucharest, Romania, vol. 19(3), pages 5-18.
    9. Martijn Van Heel & Dinska Van Gucht & Koen Vanbrabant & Frank Baeyens, 2017. "The Importance of Conditioned Stimuli in Cigarette and E-Cigarette Craving Reduction by E-Cigarettes," IJERPH, MDPI, vol. 14(2), pages 1-18, February.
    10. Sean McKenzie & Hilary Parkinson & Jane Mangold & Mary Burrows & Selena Ahmed & Fabian Menalled, 2018. "Perceptions, Experiences, and Priorities Supporting Agroecosystem Management Decisions Differ among Agricultural Producers, Consultants, and Researchers," Sustainability, MDPI, vol. 10(11), pages 1-19, November.
    11. Milad Abbasiharofteh & Tom Broekel, 2021. "Still in the shadow of the wall? The case of the Berlin biotechnology cluster," Environment and Planning A, , vol. 53(1), pages 73-94, February.
    12. 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.
    13. Andee J. Kaplan & Eric R. Hare, 2019. "Putting down roots: a graphical exploration of community attachment," Computational Statistics, Springer, vol. 34(4), pages 1449-1464, December.
    14. Ahmad Alsaber & Jiazhu Pan & Adeeba Al-Herz & Dhary S. Alkandary & Adeeba Al-Hurban & Parul Setiya & on behalf of the KRRD Group, 2020. "Influence of Ambient Air Pollution on Rheumatoid Arthritis Disease Activity Score Index," IJERPH, MDPI, vol. 17(2), pages 1-17, January.
    15. Kane, Michael & Emerson, John W. & Weston, Stephen, 2013. "Scalable Strategies for Computing with Massive Data," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 55(i14).
    16. Haunschild, Robin & Bornmann, Lutz, 2023. "Which papers cited which tweets? An exploratory analysis based on Scopus data," Journal of Informetrics, Elsevier, vol. 17(2).
    17. Fulya Gokalp Yavuz & Barret Schloerke, 2020. "Parallel computing in linear mixed models," Computational Statistics, Springer, vol. 35(3), pages 1273-1289, September.
    18. Rebecca Hong & Monica Perkins & Belinda J. Gabbe & Lincoln M. Tracy, 2022. "Comparing Peak Burn Injury Times and Characteristics in Australia and New Zealand," IJERPH, MDPI, vol. 19(15), pages 1-9, August.
    19. Ioannis Politis & Ioannis Fyrogenis & Efthymis Papadopoulos & Anastasia Nikolaidou & Eleni Verani, 2020. "Shifting to Shared Wheels: Factors Affecting Dockless Bike-Sharing Choice for Short and Long Trips," Sustainability, MDPI, vol. 12(19), pages 1-25, October.
    20. Paul J McMurdie & Susan Holmes, 2014. "Waste Not, Want Not: Why Rarefying Microbiome Data Is Inadmissible," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-12, April.

    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:13:y:2022:i:1:d:10.1038_s41467-022-30067-3. 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.