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Nanotube-like processes facilitate material transfer between photoreceptors

Kalargyrou, Aikaterini A; Basche, Mark; Hare, Aura; West, Emma L; Smith, Alexander J; Ali, Robin R; Pearson, Rachael A; (2021) Nanotube-like processes facilitate material transfer between photoreceptors. EMBO Reports , 22 , Article e53732. 10.15252/embr.202153732. Green open access

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Abstract

Neuronal communication is typically mediated via synapses and gap junctions. New forms of intercellular communication, including nanotubes (NTs) and extracellular vesicles (EVs), have been described for non-neuronal cells, but their role in neuronal communication is not known. Recently, transfer of cytoplasmic material between donor and host neurons (“material transfer”) was shown to occur after photoreceptor transplantation. The cellular mechanism(s) underlying this surprising finding are unknown. Here, using transplantation, primary neuronal cultures and the generation of chimeric retinae, we show for the first time that mammalian photoreceptor neurons can form open-end NT-like processes. These processes permit the transfer of cytoplasmic and membrane-bound molecules in culture and after transplantation and can mediate gain-of-function in the acceptor cells. Rarely, organelles were also observed to transfer. Strikingly, use of chimeric retinae revealed that material transfer can occur between photoreceptors in the intact adult retina. Conversely, while photoreceptors are capable of releasing EVs, at least in culture, these are taken up by glia and not by retinal neurons. Our findings provide the first evidence of functional NT-like processes forming between sensory neurons in culture and in vivo.

Type: Article
Title: Nanotube-like processes facilitate material transfer between photoreceptors
Location: England
Open access status: An open access version is available from UCL Discovery
DOI: 10.15252/embr.202153732
Publisher version: https://doi.org/10.15252/embr.202153732
Language: English
Additional information: Copyright 2021 The Authors. Published under the terms of the CC BY 4.0 licence. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Keywords: Science & Technology, Life Sciences & Biomedicine, Biochemistry & Molecular Biology, Cell Biology, extracellular vesicle, intercellular communication, material transfer, photoreceptor transplantation, tunnelling nanotube, TUNNELING NANOTUBES, IN-VIVO, NEURAL CREST, EXTRACELLULAR VESICLES, MEMBRANE NANOTUBES, CELL-COMMUNICATION, GAG PROTEIN, TRANSPLANTATION, MOUSE, RNA
UCL classification: UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Institute of Ophthalmology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL
URI: https://discovery.ucl.ac.uk/id/eprint/10142627
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