IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33339-0.html
   My bibliography  Save this article

Cytoplasmic organization promotes protein diffusion in Xenopus extracts

Author

Listed:
  • William Y. C. Huang

    (Stanford University School of Medicine)

  • Xianrui Cheng

    (Stanford University School of Medicine
    University of Southern California)

  • James E. Ferrell

    (Stanford University School of Medicine
    Stanford University School of Medicine)

Abstract

The cytoplasm is highly organized. However, the extent to which this organization influences the dynamics of cytoplasmic proteins is not well understood. Here, we use Xenopus laevis egg extracts as a model system to study diffusion dynamics in organized versus disorganized cytoplasm. Such extracts are initially homogenized and disorganized, and self-organize into cell-like units over the course of tens of minutes. Using fluorescence correlation spectroscopy, we observe that as the cytoplasm organizes, protein diffusion speeds up by about a factor of two over a length scale of a few hundred nanometers, eventually approaching the diffusion time measured in organelle-depleted cytosol. Even though the ordered cytoplasm contained organelles and cytoskeletal elements that might interfere with diffusion, the convergence of protein diffusion in the cytoplasm toward that in organelle-depleted cytosol suggests that subcellular organization maximizes protein diffusivity. The effect of organization on diffusion varies with molecular size, with the effects being largest for protein-sized molecules, and with the time scale of the measurement. These results show that cytoplasmic organization promotes the efficient diffusion of protein molecules in a densely packed environment.

Suggested Citation

  • William Y. C. Huang & Xianrui Cheng & James E. Ferrell, 2022. "Cytoplasmic organization promotes protein diffusion in Xenopus extracts," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33339-0
    DOI: 10.1038/s41467-022-33339-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33339-0
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-33339-0?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. Pengli Zheng & Christopher J. Obara & Ewa Szczesna & Jonathon Nixon-Abell & Kishore K. Mahalingan & Antonina Roll-Mecak & Jennifer Lippincott-Schwartz & Craig Blackstone, 2022. "ER proteins decipher the tubulin code to regulate organelle distribution," Nature, Nature, vol. 601(7891), pages 132-138, January.
    2. Eugene A. Katrukha & Marina Mikhaylova & Hugo X. van Brakel & Paul M. van Bergen en Henegouwen & Anna Akhmanova & Casper C. Hoogenraad & Lukas C. Kapitein, 2017. "Probing cytoskeletal modulation of passive and active intracellular dynamics using nanobody-functionalized quantum dots," Nature Communications, Nature, vol. 8(1), pages 1-8, April.
    3. Robert E. Powers & Songyu Wang & Tina Y. Liu & Tom A. Rapoport, 2017. "Reconstitution of the tubular endoplasmic reticulum network with purified components," Nature, Nature, vol. 543(7644), pages 257-260, March.
    4. Michael Baum & Fabian Erdel & Malte Wachsmuth & Karsten Rippe, 2014. "Retrieving the intracellular topology from multi-scale protein mobility mapping in living cells," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    5. Jeremy B. Chang & James E. Ferrell Jr, 2013. "Mitotic trigger waves and the spatial coordination of the Xenopus cell cycle," Nature, Nature, vol. 500(7464), pages 603-607, August.
    6. Carmine Di Rienzo & Vincenzo Piazza & Enrico Gratton & Fabio Beltram & Francesco Cardarelli, 2014. "Probing short-range protein Brownian motion in the cytoplasm of living cells," Nature Communications, Nature, vol. 5(1), pages 1-8, 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. Yuping Chen & Jo-Hsi Huang & Connie Phong & James E. Ferrell, 2024. "Viscosity-dependent control of protein synthesis and degradation," Nature Communications, Nature, vol. 15(1), pages 1-11, 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. Patrick A. Sandoz & Robin A. Denhardt-Eriksson & Laurence Abrami & Luciano A. Abriata & Gard Spreemann & Catherine Maclachlan & Sylvia Ho & Béatrice Kunz & Kathryn Hess & Graham Knott & Francisco S. M, 2023. "Dynamics of CLIMP-63 S-acylation control ER morphology," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Kirstin Meyer & Nicholas C. Lammers & Lukasz J. Bugaj & Hernan G. Garcia & Orion D. Weiner, 2023. "Optogenetic control of YAP reveals a dynamic communication code for stem cell fate and proliferation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Wang, Xudong & Chen, Yao, 2021. "Ergodic property of Langevin systems with superstatistical, uncorrelated or correlated diffusivity," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 577(C).
    4. George R. R. Bell & Esther Rincón & Emel Akdoğan & Sean R. Collins, 2021. "Optogenetic control of receptors reveals distinct roles for actin- and Cdc42-dependent negative signals in chemotactic signal processing," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Cátia Silva Janota & Andreia Pinto & Anna Pezzarossa & Pedro Machado & Judite Costa & Pedro Campinho & Cláudio A. Franco & Edgar R. Gomes, 2022. "Shielding of actin by the endoplasmic reticulum impacts nuclear positioning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Sikora, Grzegorz & Wyłomańska, Agnieszka & Krapf, Diego, 2018. "Recurrence statistics for anomalous diffusion regime change detection," Computational Statistics & Data Analysis, Elsevier, vol. 128(C), pages 380-394.
    7. Yun Xiang & Rui Lyu & Junjie Hu, 2023. "Oligomeric scaffolding for curvature generation by ER tubule-forming proteins," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    8. Yoko Shibata & Emily E. Mazur & Buyan Pan & Joao A. Paulo & Steven P. Gygi & Suyog Chavan & L. Sebastian Alexis Valerio & Jiuchun Zhang & Tom A. Rapoport, 2024. "The membrane curvature-inducing REEP1-4 proteins generate an ER-derived vesicular compartment," Nature Communications, Nature, vol. 15(1), pages 1-16, 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_s41467-022-33339-0. 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.