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Spatial redistribution of neurosecretory vesicles upon stimulation accelerates their directed transport to the plasma membrane

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  • Elaine B Schenk
  • Frederic A Meunier
  • Dietmar B Oelz

Abstract

Through the integration of results from an imaging analysis of intracellular trafficking of labelled neurosecretory vesicles in chromaffin cells, we develop a Markov state model to describe their transport and binding kinetics. Our simulation results indicate that a spatial redistribution of neurosecretory vesicles occurs upon secretagogue stimulation leading vesicles to the plasma membrane where they undergo fusion thereby releasing adrenaline and noradrenaline. Furthermore, we find that this redistribution alone can explain the observed up-regulation of vesicle transport upon stimulation and its directional bias towards the plasma membrane. Parameter fitting indicates that in the deeper compartment within the cell, vesicle transport is asymmetric and characterised by a bias towards the plasma membrane.

Suggested Citation

  • Elaine B Schenk & Frederic A Meunier & Dietmar B Oelz, 2022. "Spatial redistribution of neurosecretory vesicles upon stimulation accelerates their directed transport to the plasma membrane," PLOS ONE, Public Library of Science, vol. 17(3), pages 1-17, March.
    • Handle: RePEc:plo:pone00:0264521
    DOI: 10.1371/journal.pone.0264521
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    References listed on IDEAS

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    1. Tong Wang & Sally Martin & Tam H. Nguyen & Callista B. Harper & Rachel S. Gormal & Ramon Martínez-Mármol & Shanker Karunanithi & Elizabeth J. Coulson & Nick R. Glass & Justin J. Cooper-White & Bruno v, 2016. "Correction: Corrigendum: Flux of signalling endosomes undergoing axonal retrograde transport is encoded by presynaptic activity and TrkB," Nature Communications, Nature, vol. 7(1), pages 1-1, December.
    2. Tong Wang & Sally Martin & Tam H. Nguyen & Callista B. Harper & Rachel S. Gormal & Ramon Martínez-Mármol & Shanker Karunanithi & Elizabeth J. Coulson & Nick R. Glass & Justin J. Cooper-White & Bruno v, 2016. "Flux of signalling endosomes undergoing axonal retrograde transport is encoded by presynaptic activity and TrkB," Nature Communications, Nature, vol. 7(1), pages 1-16, December.
    3. Andreas Papadopulos & Guillermo A. Gomez & Sally Martin & Jade Jackson & Rachel S. Gormal & Damien J. Keating & Alpha S. Yap & Frederic A. Meunier, 2015. "Activity-driven relaxation of the cortical actomyosin II network synchronizes Munc18-1-dependent neurosecretory vesicle docking," Nature Communications, Nature, vol. 6(1), pages 1-11, May.
    4. M. Birbaumer & F. Schweitzer, 2011. "Agent-based modeling of intracellular transport," The European Physical Journal B: Condensed Matter and Complex Systems, Springer;EDP Sciences, vol. 82(3), pages 245-255, August.
    5. Daungruthai Jarukanont & Imelda Bonifas Arredondo & Ricardo Femat & Martin E Garcia, 2015. "Vesicle Motion during Sustained Exocytosis in Chromaffin Cells: Numerical Model Based on Amperometric Measurements," PLOS ONE, Public Library of Science, vol. 10(12), pages 1-25, December.
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    Cited by:

    1. Ling-Gang Wu & Chung Yu Chan, 2024. "Membrane transformations of fusion and budding," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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