IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0032948.html
   My bibliography  Save this article

Confining Domains Lead to Reaction Bursts: Reaction Kinetics in the Plasma Membrane

Author

Listed:
  • Ziya Kalay
  • Takahiro K Fujiwara
  • Akihiro Kusumi

Abstract

Confinement of molecules in specific small volumes and areas within a cell is likely to be a general strategy that is developed during evolution for regulating the interactions and functions of biomolecules. The cellular plasma membrane, which is the outermost membrane that surrounds the entire cell, was considered to be a continuous two-dimensional liquid, but it is becoming clear that it consists of numerous nano-meso-scale domains with various lifetimes, such as raft domains and cytoskeleton-induced compartments, and membrane molecules are dynamically trapped in these domains. In this article, we give a theoretical account on the effects of molecular confinement on reversible bimolecular reactions in a partitioned surface such as the plasma membrane. By performing simulations based on a lattice-based model of diffusion and reaction, we found that in the presence of membrane partitioning, bimolecular reactions that occur in each compartment proceed in bursts during which the reaction rate is sharply and briefly increased even though the asymptotic reaction rate remains the same. We characterized the time between reaction bursts and the burst amplitude as a function of the model parameters, and discussed the biological significance of the reaction bursts in the presence of strong inhibitor activity.

Suggested Citation

  • Ziya Kalay & Takahiro K Fujiwara & Akihiro Kusumi, 2012. "Confining Domains Lead to Reaction Bursts: Reaction Kinetics in the Plasma Membrane," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-8, March.
  • Handle: RePEc:plo:pone00:0032948
    DOI: 10.1371/journal.pone.0032948
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0032948
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0032948&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0032948?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. Michelle N Costa & Krishnan Radhakrishnan & Bridget S Wilson & Dionisios G Vlachos & Jeremy S Edwards, 2009. "Coupled Stochastic Spatial and Non-Spatial Simulations of ErbB1 Signaling Pathways Demonstrate the Importance of Spatial Organization in Signal Transduction," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-9, July.
    2. Avigdor Eldar & Michael B. Elowitz, 2010. "Functional roles for noise in genetic circuits," Nature, Nature, vol. 467(7312), pages 167-173, September.
    3. P. D. Calvert & V. I. Govardovskii & N. Krasnoperova & R. E. Anderson & J. Lem & C. L. Makino, 2001. "Membrane protein diffusion sets the speed of rod phototransduction," Nature, Nature, vol. 411(6833), pages 90-94, May.
    4. Long Cai & Chiraj K. Dalal & Michael B. Elowitz, 2008. "Frequency-modulated nuclear localization bursts coordinate gene regulation," Nature, Nature, vol. 455(7212), pages 485-490, September.
    5. Inhee Chung & Robert Akita & Richard Vandlen & Derek Toomre & Joseph Schlessinger & Ira Mellman, 2010. "Spatial control of EGF receptor activation by reversible dimerization on living cells," Nature, Nature, vol. 464(7289), pages 783-787, April.
    Full references (including those not matched with items on IDEAS)

    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. Vera Bettenworth & Simon Vliet & Bartosz Turkowyd & Annika Bamberger & Heiko Wendt & Matthew McIntosh & Wieland Steinchen & Ulrike Endesfelder & Anke Becker, 2022. "Frequency modulation of a bacterial quorum sensing response," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Gabriele Micali & Gerardo Aquino & David M Richards & Robert G Endres, 2015. "Accurate Encoding and Decoding by Single Cells: Amplitude Versus Frequency Modulation," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-21, June.
    3. Marc Weber & Javier Buceta, 2013. "Stochastic Stabilization of Phenotypic States: The Genetic Bistable Switch as a Case Study," PLOS ONE, Public Library of Science, vol. 8(9), pages 1-8, September.
    4. Shwetha Srinivasan & Raju Regmi & Xingcheng Lin & Courtney A. Dreyer & Xuyan Chen & Steven D. Quinn & Wei He & Matthew A. Coleman & Kermit L. Carraway & Bin Zhang & Gabriela S. Schlau-Cohen, 2022. "Ligand-induced transmembrane conformational coupling in monomeric EGFR," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Lee, Julian, 2023. "Poisson distributions in stochastic dynamics of gene expression: What events do they count?," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 630(C).
    6. Lucy Ham & Megan A. Coomer & Kaan Öcal & Ramon Grima & Michael P. H. Stumpf, 2024. "A stochastic vs deterministic perspective on the timing of cellular events," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    7. Michael G. Sugiyama & Aidan I. Brown & Jesus Vega-Lugo & Jazlyn P. Borges & Andrew M. Scott & Khuloud Jaqaman & Gregory D. Fairn & Costin N. Antonescu, 2023. "Confinement of unliganded EGFR by tetraspanin nanodomains gates EGFR ligand binding and signaling," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Laura Corrales-Guerrero & Asaf Tal & Rinat Arbel-Goren & Vicente Mariscal & Enrique Flores & Antonia Herrero & Joel Stavans, 2015. "Spatial Fluctuations in Expression of the Heterocyst Differentiation Regulatory Gene hetR in Anabaena Filaments," PLOS Genetics, Public Library of Science, vol. 11(4), pages 1-21, April.
    9. Singh, Abhyudai & Vahdat, Zahra & Xu, Zikai, 2019. "Time-triggered stochastic hybrid systems with two timer-dependent resets," OSF Preprints u8fzg, Center for Open Science.
    10. Gyurin Kim & Doeun Kim & JuHyeong Lee & Juhwan Kim & Se-Yeon Heo & Young Min Song & Hyeon-Ho Jeong, 2025. "Quasi-ordered plasmonic metasurfaces with unclonable stochastic scattering for secure authentication," Nature Communications, Nature, vol. 16(1), pages 1-11, December.
    11. Andreas Doncic & Umut Eser & Oguzhan Atay & Jan M Skotheim, 2013. "An Algorithm to Automate Yeast Segmentation and Tracking," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-11, March.
    12. Koji Iwamoto & Satomi Matsuoka & Masahiro Ueda, 2025. "Excitable Ras dynamics-based screens reveal RasGEFX is required for macropinocytosis and random cell migration," Nature Communications, Nature, vol. 16(1), pages 1-20, December.
    13. Margaritis Voliotis & Philipp Thomas & Ramon Grima & Clive G Bowsher, 2016. "Stochastic Simulation of Biomolecular Networks in Dynamic Environments," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-18, June.
    14. Chen, Aimin & Tian, Tianhai & Chen, Yiren & Zhou, Tianshou, 2022. "Stochastic analysis of a complex gene-expression model," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).
    15. repec:plo:pone00:0014624 is not listed on IDEAS
    16. Hui Deng & Qian Lei & Chengdi Wang & Zhoufeng Wang & Hai Chen & Gang Wang & Na Yang & Dan Huang & Quanwei Yu & Mengling Yao & Xue Xiao & Guonian Zhu & Cheng Cheng & Yangqian Li & Feng Li & Panwen Tian, 2022. "A fluorogenic probe for predicting treatment response in non-small cell lung cancer with EGFR-activating mutations," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    17. Rui Cong & Chengyu Deng & Pengwei Li & Yiwei Tang & Jinfan Hou & Jiehui Zhao & Qili Wang & Yingying Chen & Jiasheng Tu & Xiqun Jiang & Lei Jiang, 2025. "Dimeric copper peptide incorporated hydrogel for promoting diabetic wound healing," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
    18. Abhyudai Singh & Mohammad Soltani, 2013. "Quantifying Intrinsic and Extrinsic Variability in Stochastic Gene Expression Models," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-12, December.
    19. Angélique Richard & Loïs Boullu & Ulysse Herbach & Arnaud Bonnafoux & Valérie Morin & Elodie Vallin & Anissa Guillemin & Nan Papili Gao & Rudiyanto Gunawan & Jérémie Cosette & Ophélie Arnaud & Jean-Ja, 2016. "Single-Cell-Based Analysis Highlights a Surge in Cell-to-Cell Molecular Variability Preceding Irreversible Commitment in a Differentiation Process," PLOS Biology, Public Library of Science, vol. 14(12), pages 1-35, December.
    20. Christine Andres & Jan Hasenauer & Frank Allgower & Tim Hucho, 2012. "Threshold-Free Population Analysis Identifies Larger DRG Neurons to Respond Stronger to NGF Stimulation," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-14, March.
    21. repec:plo:pcbi00:1006368 is not listed on IDEAS
    22. Kajántó, Sándor & Néda, Zoltán, 2018. "Universality in the coarse-grained fluctuations for a class of linear dynamical systems," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 503(C), pages 215-220.

    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:plo:pone00:0032948. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.