IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36060-8.html
   My bibliography  Save this article

Biomolecular condensates formed by designer minimalistic peptides

Author

Listed:
  • Avigail Baruch Leshem

    (Tel Aviv University)

  • Sian Sloan-Dennison

    (University of Strathclyde)

  • Tlalit Massarano

    (Tel Aviv University)

  • Shavit Ben-David

    (Tel Aviv University)

  • Duncan Graham

    (University of Strathclyde)

  • Karen Faulds

    (University of Strathclyde)

  • Hugo E. Gottlieb

    (Bar Ilan University)

  • Jordan H. Chill

    (Bar Ilan University)

  • Ayala Lampel

    (Tel Aviv University
    Center for Nanoscience and Nanotechnology Tel Aviv University
    Sagol Center for Regenerative Biotechnology Tel Aviv University
    Center for the Physics and Chemistry of Living Systems Tel Aviv University, Tel Aviv 69978, Israel)

Abstract

Inspired by the role of intracellular liquid-liquid phase separation (LLPS) in formation of membraneless organelles, there is great interest in developing dynamic compartments formed by LLPS of intrinsically disordered proteins (IDPs) or short peptides. However, the molecular mechanisms underlying the formation of biomolecular condensates have not been fully elucidated, rendering on-demand design of synthetic condensates with tailored physico-chemical functionalities a significant challenge. To address this need, here we design a library of LLPS-promoting peptide building blocks composed of various assembly domains. We show that the LLPS propensity, dynamics, and encapsulation efficiency of compartments can be tuned by changes to the peptide composition. Specifically, with the aid of Raman and NMR spectroscopy, we show that interactions between arginine and aromatic amino acids underlie droplet formation, and that both intra- and intermolecular interactions dictate droplet dynamics. The resulting sequence-structure-function correlation could support the future development of compartments for a variety of applications.

Suggested Citation

  • Avigail Baruch Leshem & Sian Sloan-Dennison & Tlalit Massarano & Shavit Ben-David & Duncan Graham & Karen Faulds & Hugo E. Gottlieb & Jordan H. Chill & Ayala Lampel, 2023. "Biomolecular condensates formed by designer minimalistic peptides," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36060-8
    DOI: 10.1038/s41467-023-36060-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36060-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-36060-8?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. Rachel S. Fisher & Shana Elbaum-Garfinkle, 2020. "Tunable multiphase dynamics of arginine and lysine liquid condensates," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    2. Carsten Donau & Fabian Späth & Marilyne Sosson & Brigitte A. K. Kriebisch & Fabian Schnitter & Marta Tena-Solsona & Hyun-Seo Kang & Elia Salibi & Michael Sattler & Hannes Mutschler & Job Boekhoven, 2020. "Active coacervate droplets as a model for membraneless organelles and protocells," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    3. Bartosz Gabryelczyk & Hao Cai & Xiangyan Shi & Yue Sun & Piet J. M. Swinkels & Stefan Salentinig & Konstantin Pervushin & Ali Miserez, 2019. "Hydrogen bond guidance and aromatic stacking drive liquid-liquid phase separation of intrinsically disordered histidine-rich peptides," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    4. Georg Krainer & Timothy J. Welsh & Jerelle A. Joseph & Jorge R. Espinosa & Sina Wittmann & Ella Csilléry & Akshay Sridhar & Zenon Toprakcioglu & Giedre Gudiškytė & Magdalena A. Czekalska & William E. , 2021. "Reentrant liquid condensate phase of proteins is stabilized by hydrophobic and non-ionic interactions," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    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. Shoupeng Cao & Tsvetomir Ivanov & Julian Heuer & Calum T. J. Ferguson & Katharina Landfester & Lucas Caire da Silva, 2024. "Dipeptide coacervates as artificial membraneless organelles for bioorthogonal catalysis," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Maruša Ramšak & Dominique A. Ramirez & Loren E. Hough & Michael R. Shirts & Sara Vidmar & Kristina Eleršič Filipič & Gregor Anderluh & Roman Jerala, 2023. "Programmable de novo designed coiled coil-mediated phase separation in mammalian cells," Nature Communications, Nature, vol. 14(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. Yuri Hong & Saeed Najafi & Thomas Casey & Joan-Emma Shea & Song-I Han & Dong Soo Hwang, 2022. "Hydrophobicity of arginine leads to reentrant liquid-liquid phase separation behaviors of arginine-rich proteins," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. 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.
    3. Agustín Mangiarotti & Nannan Chen & Ziliang Zhao & Reinhard Lipowsky & Rumiana Dimova, 2023. "Wetting and complex remodeling of membranes by biomolecular condensates," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Jiahua Wang & Manzar Abbas & Junyou Wang & Evan Spruijt, 2023. "Selective amide bond formation in redox-active coacervate protocells," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. 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.
    6. Hema M. Swasthi & Joseph L. Basalla & Claire E. Dudley & Anthony G. Vecchiarelli & Matthew R. Chapman, 2023. "Cell surface-localized CsgF condensate is a gatekeeper in bacterial curli subunit secretion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    7. Georg Krainer & Kadi L. Saar & William E. Arter & Timothy J. Welsh & Magdalena A. Czekalska & Raphaël P. B. Jacquat & Quentin Peter & Walther C. Traberg & Arvind Pujari & Akhila K. Jayaram & Pavankuma, 2023. "Direct digital sensing of protein biomarkers in solution," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    8. Andrew Z. Lin & Kiersten M. Ruff & Furqan Dar & Ameya Jalihal & Matthew R. King & Jared M. Lalmansingh & Ammon E. Posey & Nadia A. Erkamp & Ian Seim & Amy S. Gladfelter & Rohit V. Pappu, 2023. "Dynamical control enables the formation of demixed biomolecular condensates," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. 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.
    10. Qi Guo & Guijin Zou & Xuliang Qian & Shujun Chen & Huajian Gao & Jing Yu, 2022. "Hydrogen-bonds mediate liquid-liquid phase separation of mussel derived adhesive peptides," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    11. 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.
    12. Tomas Sneideris & Nadia A. Erkamp & Hannes Ausserwöger & Kadi L. Saar & Timothy J. Welsh & Daoyuan Qian & Kai Katsuya-Gaviria & Margaret L. L. Y. Johncock & Georg Krainer & Alexander Borodavka & Tuoma, 2023. "Targeting nucleic acid phase transitions as a mechanism of action for antimicrobial peptides," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Aishwarya Agarwal & Lisha Arora & Sandeep K. Rai & Anamika Avni & Samrat Mukhopadhyay, 2022. "Spatiotemporal modulations in heterotypic condensates of prion and α-synuclein control phase transitions and amyloid conversion," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Sihan Tang & Jiang Gong & Yunsong Shi & Shifeng Wen & Qiang Zhao, 2022. "Spontaneous water-on-water spreading of polyelectrolyte membranes inspired by skin formation," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    15. 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.
    16. William E. Arter & Runzhang Qi & Nadia A. Erkamp & Georg Krainer & Kieran Didi & Timothy J. Welsh & Julia Acker & Jonathan Nixon-Abell & Seema Qamar & Jordina Guillén-Boixet & Titus M. Franzmann & Dav, 2022. "Biomolecular condensate phase diagrams with a combinatorial microdroplet platform," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    17. Tuan Nguyen & Sai Li & Jeremy T-H Chang & John W. Watters & Htet Ng & Adewola Osunsade & Yael David & Shixin Liu, 2022. "Chromatin sequesters pioneer transcription factor Sox2 from exerting force on DNA," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    18. Alexander M. Bergmann & Jonathan Bauermann & Giacomo Bartolucci & Carsten Donau & Michele Stasi & Anna-Lena Holtmannspötter & Frank Jülicher & Christoph A. Weber & Job Boekhoven, 2023. "Liquid spherical shells are a non-equilibrium steady state of active droplets," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    19. Tommaso P. Fraccia & Nicolas Martin, 2023. "Non-enzymatic oligonucleotide ligation in coacervate protocells sustains compartment-content coupling," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    20. Shoupeng Cao & Tsvetomir Ivanov & Julian Heuer & Calum T. J. Ferguson & Katharina Landfester & Lucas Caire da Silva, 2024. "Dipeptide coacervates as artificial membraneless organelles for bioorthogonal catalysis," Nature Communications, Nature, vol. 15(1), pages 1-14, 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_s41467-023-36060-8. 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.