IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-30521-2.html
   My bibliography  Save this article

Dynamic arrest and aging of biomolecular condensates are modulated by low-complexity domains, RNA and biochemical activity

Author

Listed:
  • Miriam Linsenmeier

    (Institute for Chemical and Bioengineering, Swiss Federal Institute of Technology)

  • Maria Hondele

    (Institute for Biochemistry, Swiss Federal Institute of Technology
    University of Basel)

  • Fulvio Grigolato

    (Institute for Chemical and Bioengineering, Swiss Federal Institute of Technology)

  • Eleonora Secchi

    (Swiss Federal Institute of Technology)

  • Karsten Weis

    (Institute for Biochemistry, Swiss Federal Institute of Technology)

  • Paolo Arosio

    (Institute for Chemical and Bioengineering, Swiss Federal Institute of Technology)

Abstract

Biomolecular condensates require suitable control of material properties for their function. Here we apply Differential Dynamic Microscopy (DDM) to probe the material properties of an in vitro model of processing bodies consisting of out-of-equilibrium condensates formed by the DEAD-box ATPase Dhh1 in the presence of ATP and RNA. By applying this single-droplet technique we show that condensates within the same population exhibit a distribution of material properties, which are regulated on several levels. Removal of the low-complexity domains (LCDs) of the protein decreases the fluidity of the condensates. Structured RNA leads to a larger fraction of dynamically arrested condensates with respect to unstructured polyuridylic acid (polyU). Promotion of the enzymatic ATPase activity of Dhh1 reduces aging of the condensates and the formation of arrested structures, indicating that biochemical activity and material turnover can maintain fluid-like properties over time.

Suggested Citation

  • Miriam Linsenmeier & Maria Hondele & Fulvio Grigolato & Eleonora Secchi & Karsten Weis & Paolo Arosio, 2022. "Dynamic arrest and aging of biomolecular condensates are modulated by low-complexity domains, RNA and biochemical activity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30521-2
    DOI: 10.1038/s41467-022-30521-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-30521-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-30521-2?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. Karina K. Nakashima & Merlijn H. I. Haren & Alain A. M. André & Irina Robu & Evan Spruijt, 2021. "Active coacervate droplets are protocells that grow and resist Ostwald ripening," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    2. Marta Tena-Solsona & Caren Wanzke & Benedikt Riess & Andreas R. Bausch & Job Boekhoven, 2018. "Self-selection of dissipative assemblies driven by primitive chemical reaction networks," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    3. Ibraheem Alshareedah & Mahdi Muhammad Moosa & Matthew Pham & Davit A. Potoyan & Priya R. Banerjee, 2021. "Programmable viscoelasticity in protein-RNA condensates with disordered sticker-spacer polypeptides," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Archishman Ghosh & Divya Kota & Huan-Xiang Zhou, 2021. "Shear relaxation governs fusion dynamics of biomolecular condensates," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    5. 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.
    6. Pilong Li & Sudeep Banjade & Hui-Chun Cheng & Soyeon Kim & Baoyu Chen & Liang Guo & Marc Llaguno & Javoris V. Hollingsworth & David S. King & Salman F. Banani & Paul S. Russo & Qiu-Xing Jiang & B. Tra, 2012. "Phase transitions in the assembly of multivalent signalling proteins," Nature, Nature, vol. 483(7389), pages 336-340, March.
    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. Andres R. Tejedor & Ignacio Sanchez-Burgos & Maria Estevez-Espinosa & Adiran Garaizar & Rosana Collepardo-Guevara & Jorge Ramirez & Jorge R. Espinosa, 2022. "Protein structural transitions critically transform the network connectivity and viscoelasticity of RNA-binding protein condensates but RNA can prevent it," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Michael C. Owens & Hui Shen & Amber Yanas & Maria Saraí Mendoza-Figueroa & Ellen Lavorando & Xiaoyu Wei & Him Shweta & Hsin-Yao Tang & Yale E. Goldman & Kathy Fange Liu, 2024. "Specific catalytically impaired DDX3X mutants form sexually dimorphic hollow condensates," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Etienne Jambon-Puillet & Andrea Testa & Charlotta Lorenz & Robert W. Style & Aleksander A. Rebane & Eric R. Dufresne, 2024. "Phase-separated droplets swim to their dissolution," Nature Communications, Nature, vol. 15(1), pages 1-12, 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. Furqan Dar & Samuel R. Cohen & Diana M. Mitrea & Aaron H. Phillips & Gergely Nagy & Wellington C. Leite & Christopher B. Stanley & Jeong-Mo Choi & Richard W. Kriwacki & Rohit V. Pappu, 2024. "Biomolecular condensates form spatially inhomogeneous network fluids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Etienne Jambon-Puillet & Andrea Testa & Charlotta Lorenz & Robert W. Style & Aleksander A. Rebane & Eric R. Dufresne, 2024. "Phase-separated droplets swim to their dissolution," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Dinesh Sundaravadivelu Devarajan & Jiahui Wang & Beata Szała-Mendyk & Shiv Rekhi & Arash Nikoubashman & Young C. Kim & Jeetain Mittal, 2024. "Sequence-dependent material properties of biomolecular condensates and their relation to dilute phase conformations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Min Lee & Hyungseok C. Moon & Hyeonjeong Jeong & Dong Wook Kim & Hye Yoon Park & Yongdae Shin, 2024. "Optogenetic control of mRNA condensation reveals an intimate link between condensate material properties and functions," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Merlijn H. I. Haren & Brent S. Visser & Evan Spruijt, 2024. "Probing the surface charge of condensates using microelectrophoresis," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    6. Andres R. Tejedor & Ignacio Sanchez-Burgos & Maria Estevez-Espinosa & Adiran Garaizar & Rosana Collepardo-Guevara & Jorge Ramirez & Jorge R. Espinosa, 2022. "Protein structural transitions critically transform the network connectivity and viscoelasticity of RNA-binding protein condensates but RNA can prevent it," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Mrityunjoy Kar & Laura T. Vogel & Gaurav Chauhan & Suren Felekyan & Hannes Ausserwöger & Timothy J. Welsh & Furqan Dar & Anjana R. Kamath & Tuomas P. J. Knowles & Anthony A. Hyman & Claus A. M. Seidel, 2024. "Solutes unmask differences in clustering versus phase separation of FET proteins," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    8. Mina Farag & Samuel R. Cohen & Wade M. Borcherds & Anne Bremer & Tanja Mittag & Rohit V. Pappu, 2022. "Condensates formed by prion-like low-complexity domains have small-world network structures and interfaces defined by expanded conformations," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Simone M. Poprawa & Michele Stasi & Brigitte A. K. Kriebisch & Monika Wenisch & Judit Sastre & Job Boekhoven, 2024. "Active droplets through enzyme-free, dynamic phosphorylation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    10. Shuangcheng Alivia Wu & Chenchen Shen & Xiaoqiong Wei & Xiawei Zhang & Siwen Wang & Xinxin Chen & Mauricio Torres & You Lu & Liangguang Leo Lin & Huilun Helen Wang & Allen H. Hunter & Deyu Fang & Shen, 2023. "The mechanisms to dispose of misfolded proteins in the endoplasmic reticulum of adipocytes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. Zheng Shen & Daxiao Sun & Adriana Savastano & Sára Joana Varga & Maria-Sol Cima-Omori & Stefan Becker & Alf Honigmann & Markus Zweckstetter, 2023. "Multivalent Tau/PSD-95 interactions arrest in vitro condensates and clusters mimicking the postsynaptic density," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Beatrice Ramm & Dominik Schumacher & Andrea Harms & Tamara Heermann & Philipp Klos & Franziska Müller & Petra Schwille & Lotte Søgaard-Andersen, 2023. "Biomolecular condensate drives polymerization and bundling of the bacterial tubulin FtsZ to regulate cell division," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    13. 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.
    14. Bing-Ze Yang & Mei-Yin Liu & Kuan-Lin Chiu & Yuh-Ling Chien & Ching-An Cheng & Yu-Lin Chen & Li-Yu Tsui & Keng-Ru Lin & Hsueh-Ping Catherine Chu & Ching-Shyi Peter Wu, 2024. "DHX9 SUMOylation is required for the suppression of R-loop-associated genome instability," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Omar A. Saleh & Sam Wilken & Todd M. Squires & Tim Liedl, 2023. "Vacuole dynamics and popping-based motility in liquid droplets of DNA," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    16. Manisha Poudyal & Komal Patel & Laxmikant Gadhe & Ajay Singh Sawner & Pradeep Kadu & Debalina Datta & Semanti Mukherjee & Soumik Ray & Ambuja Navalkar & Siddhartha Maiti & Debdeep Chatterjee & Jyoti D, 2023. "Intermolecular interactions underlie protein/peptide phase separation irrespective of sequence and structure at crowded milieu," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    17. Mengru Yang & Nicolas Wenner & Gregory F. Dykes & Yan Li & Xiaojun Zhu & Yaqi Sun & Fang Huang & Jay C. D. Hinton & Lu-Ning Liu, 2022. "Biogenesis of a bacterial metabolosome for propanediol utilization," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Takayuki Miki & Masahiro Hashimoto & Hiroki Takahashi & Masatoshi Shimizu & Sae Nakayama & Tadaomi Furuta & Hisakazu Mihara, 2024. "De novo designed YK peptides forming reversible amyloid for synthetic protein condensates in mammalian cells," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Agustín Mangiarotti & Macarena Siri & Nicky W. Tam & Ziliang Zhao & Leonel Malacrida & Rumiana Dimova, 2023. "Biomolecular condensates modulate membrane lipid packing and hydration," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    20. Songyang Liu & Yanwen Zhang & Xiaoxiao He & Mei Li & Jin Huang & Xiaohai Yang & Kemin Wang & Stephen Mann & Jianbo Liu, 2022. "Signal processing and generation of bioactive nitric oxide in a model prototissue," Nature Communications, Nature, vol. 13(1), pages 1-12, 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:13:y:2022:i:1:d:10.1038_s41467-022-30521-2. 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.