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. Avigdor Eldar & Michael B. Elowitz, 2010. "Functional roles for noise in genetic circuits," Nature, Nature, vol. 467(7312), pages 167-173, September.
    2. 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.
    3. 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.
    4. 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.
    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. Mohammad Soltani & Cesar A Vargas-Garcia & Duarte Antunes & Abhyudai Singh, 2016. "Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-23, August.
    5. 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.
    6. Kazunari Iwamoto & Yuki Shindo & Koichi Takahashi, 2016. "Modeling Cellular Noise Underlying Heterogeneous Cell Responses in the Epidermal Growth Factor Signaling Pathway," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-18, November.
    7. 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).
    8. 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.
    9. Georg Fritz & Judith A Megerle & Sonja A Westermayer & Delia Brick & Ralf Heermann & Kirsten Jung & Joachim O Rädler & Ulrich Gerland, 2014. "Single Cell Kinetics of Phenotypic Switching in the Arabinose Utilization System of E. coli," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-12, February.
    10. 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.
    11. 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.
    12. Singh, Abhyudai & Vahdat, Zahra & Xu, Zikai, 2019. "Time-triggered stochastic hybrid systems with two timer-dependent resets," OSF Preprints u8fzg, Center for Open Science.
    13. Ming Ni & Antoine L Decrulle & Fanette Fontaine & Alice Demarez & Francois Taddei & Ariel B Lindner, 2012. "Pre-Disposition and Epigenetics Govern Variation in Bacterial Survival upon Stress," PLOS Genetics, Public Library of Science, vol. 8(12), pages 1-11, December.
    14. Jan Hasenauer & Christine Hasenauer & Tim Hucho & Fabian J Theis, 2014. "ODE Constrained Mixture Modelling: A Method for Unraveling Subpopulation Structures and Dynamics," PLOS Computational Biology, Public Library of Science, vol. 10(7), pages 1-17, July.
    15. 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.
    16. Martiny, Emil S. & Jensen, Mogens H. & Heltberg, Mathias S., 2022. "Detecting limit cycles in stochastic time series," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 605(C).
    17. Joachim Almquist & Loubna Bendrioua & Caroline Beck Adiels & Mattias Goksör & Stefan Hohmann & Mats Jirstrand, 2015. "A Nonlinear Mixed Effects Approach for Modeling the Cell-To-Cell Variability of Mig1 Dynamics in Yeast," PLOS ONE, Public Library of Science, vol. 10(4), pages 1-32, April.
    18. 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.
    19. Jessica A Lee & Siavash Riazi & Shahla Nemati & Jannell V Bazurto & Andreas E Vasdekis & Benjamin J Ridenhour & Christopher H Remien & Christopher J Marx, 2019. "Microbial phenotypic heterogeneity in response to a metabolic toxin: Continuous, dynamically shifting distribution of formaldehyde tolerance in Methylobacterium extorquens populations," PLOS Genetics, Public Library of Science, vol. 15(11), pages 1-38, November.
    20. Chen, Aimin & Tian, Tianhai & Chen, Yiren & Zhou, Tianshou, 2022. "Stochastic analysis of a complex gene-expression model," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).

    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.