Tau forms synaptic nano-biomolecular condensates controlling the dynamic clustering of recycling synaptic vesicles

Shanley F. Longfield, Mahdie Mollazade, Tristan P. Wallis, Rachel S. Gormal, Merja Joensuu, Jesse R. Wark, Ashley J. Waardenberg, Christopher Small, Mark E. Graham, Frédéric A. Meunier () and Ramón Martínez-Mármol ()
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Shanley F. Longfield: The University of Queensland; St Lucia Campus
Mahdie Mollazade: The University of Queensland; St Lucia Campus
Tristan P. Wallis: The University of Queensland; St Lucia Campus
Rachel S. Gormal: The University of Queensland; St Lucia Campus
Merja Joensuu: The University of Queensland; St Lucia Campus
Jesse R. Wark: The University of Sydney
Ashley J. Waardenberg: i-Synapse
Christopher Small: The University of Queensland; St Lucia Campus
Mark E. Graham: The University of Sydney
Frédéric A. Meunier: The University of Queensland; St Lucia Campus
Ramón Martínez-Mármol: The University of Queensland; St Lucia Campus

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: Abstract Neuronal communication relies on the release of neurotransmitters from various populations of synaptic vesicles. Despite displaying vastly different release probabilities and mobilities, the reserve and recycling pool of vesicles co-exist within a single cluster suggesting that small synaptic biomolecular condensates could regulate their nanoscale distribution. Here, we performed a large-scale activity-dependent phosphoproteome analysis of hippocampal neurons in vitro and identified Tau as a highly phosphorylated and disordered candidate protein. Single-molecule super-resolution microscopy revealed that Tau undergoes liquid-liquid phase separation to generate presynaptic nanoclusters whose density and number are regulated by activity. This activity-dependent diffusion process allows Tau to translocate into the presynapse where it forms biomolecular condensates, to selectively control the mobility of recycling vesicles. Tau, therefore, forms presynaptic nano-biomolecular condensates that regulate the nanoscale organization of synaptic vesicles in an activity-dependent manner.

Date: 2023
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DOI: 10.1038/s41467-023-43130-4

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