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Activity-driven relaxation of the cortical actomyosin II network synchronizes Munc18-1-dependent neurosecretory vesicle docking

Author

Listed:
  • Andreas Papadopulos

    (The Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

  • Guillermo A. Gomez

    (The University of Queensland)

  • Sally Martin

    (The Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

  • Jade Jackson

    (Molecular and Cellular Neuroscience Laboratory, Flinders University)

  • Rachel S. Gormal

    (The Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

  • Damien J. Keating

    (Molecular and Cellular Neuroscience Laboratory, Flinders University)

  • Alpha S. Yap

    (The University of Queensland)

  • Frederic A. Meunier

    (The Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland)

Abstract

In neurosecretory cells, secretory vesicles (SVs) undergo Ca2+-dependent fusion with the plasma membrane to release neurotransmitters. How SVs cross the dense mesh of the cortical actin network to reach the plasma membrane remains unclear. Here we reveal that, in bovine chromaffin cells, SVs embedded in the cortical actin network undergo a highly synchronized transition towards the plasma membrane and Munc18-1-dependent docking in response to secretagogues. This movement coincides with a translocation of the cortical actin network in the same direction. Both effects are abolished by the knockdown or the pharmacological inhibition of myosin II, suggesting changes in actomyosin-generated forces across the cell cortex. Indeed, we report a reduction in cortical actin network tension elicited on secretagogue stimulation that is sensitive to myosin II inhibition. We reveal that the cortical actin network acts as a ‘casting net’ that undergoes activity-dependent relaxation, thereby driving tethered SVs towards the plasma membrane where they undergo Munc18-1-dependent docking.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:6:y:2015:i:1:d:10.1038_ncomms7297
    DOI: 10.1038/ncomms7297
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    Cited by:

    1. 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.
    2. Anmin Jiang & Kye Kudo & Rachel S. Gormal & Sevannah Ellis & Sikao Guo & Tristan P. Wallis & Shanley F. Longfield & Phillip J. Robinson & Margaret E. Johnson & Merja Joensuu & Frédéric A. Meunier, 2024. "Dynamin1 long- and short-tail isoforms exploit distinct recruitment and spatial patterns to form endocytic nanoclusters," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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