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Flux of signalling endosomes undergoing axonal retrograde transport is encoded by presynaptic activity and TrkB

Author

Listed:
  • Tong Wang

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

  • Sally Martin

    (Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute, The University of Queensland
    Present address: Australian Institute for Bioengineering and Nanotechnology, University of Queensland, Brisbane, Queensland 4072, Australia)

  • Tam H. Nguyen

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

  • Callista B. Harper

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

  • Rachel S. Gormal

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

  • Ramon Martínez-Mármol

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

  • Shanker Karunanithi

    (Menzies Health Institute Queensland, Griffith University)

  • Elizabeth J. Coulson

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

  • Nick R. Glass

    (Australian Institute for Bioengineering and Nanotechnology, The University of Queensland)

  • Justin J. Cooper-White

    (Australian Institute for Bioengineering and Nanotechnology, The University of Queensland
    School of Chemical Engineering, The University of Queensland
    CSIRO)

  • Bruno van Swinderen

    (Queensland Brain Institute, The University of Queensland)

  • Frédéric A. Meunier

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

Abstract

Axonal retrograde transport of signalling endosomes from the nerve terminal to the soma underpins survival. As each signalling endosome carries a quantal amount of activated receptors, we hypothesized that it is the frequency of endosomes reaching the soma that determines the scale of the trophic signal. Here we show that upregulating synaptic activity markedly increased the flux of plasma membrane-derived retrograde endosomes (labelled using cholera toxin subunit-B: CTB) in hippocampal neurons cultured in microfluidic devices, and live Drosophila larval motor neurons. Electron and super-resolution microscopy analyses revealed that the fast-moving sub-diffraction-limited CTB carriers contained the TrkB neurotrophin receptor, transiently activated by synaptic activity in a BDNF-independent manner. Pharmacological and genetic inhibition of TrkB activation selectively prevented the coupling between synaptic activity and the retrograde flux of signalling endosomes. TrkB activity therefore controls the encoding of synaptic activity experienced by nerve terminals, digitalized as the flux of retrogradely transported signalling endosomes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12976
    DOI: 10.1038/ncomms12976
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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.

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