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

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  • 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
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    References listed on IDEAS

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    1. 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.
    2. 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.
    3. Avigdor Eldar & Michael B. Elowitz, 2010. "Functional roles for noise in genetic circuits," Nature, Nature, vol. 467(7312), pages 167-173, September.
    4. 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.
    5. 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.
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