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

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 van Swinderen and Frédéric A. Meunier ()
Additional contact information
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
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
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
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

Nature Communications, 2016, vol. 7, issue 1, 1-16

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms12976

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