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Nanotube-like processes facilitate material transfer between photoreceptors

Research output: Contribution to journalArticlepeer-review

Aikaterini A. Kalargyrou, Mark Basche, Aura Hare, Emma L. West, Alexander J. Smith, Robin R. Ali, Rachael A. Pearson

Original languageEnglish
Article numbere53732
JournalEMBO Reports
Issue number11
Accepted/In press2021
Published4 Nov 2021

Bibliographical note

Funding Information: We thank Professor V. Wallace and colleagues for the kind provision of lentiviral RhoA and DN‐Rac1 expression constructs. We thank O. Semenyuk, IoO vector production facility, for vector production, Drs M. Branch and R. Sampson, IoO FACS facility, Dr M. Hayes and D. Sefic Svara, UCL IoO Microscopy Unit, for technical support with FACS, imaging and electron microscopy, Professor F. Cordeiro for access to Dynamic Light Scatter and Dr A. Matsuyama for assistance with culture maintenance and Dr N. D. Aghaizu for cloning. We would like to thank all members of the Pearson and Ali groups for additional assistance and for constructive criticism and discussion of earlier drafts of the manuscript. This work was supported by Fight for Sight UK (1566/1567), Moorfields Eye Charity (E170004A; R180005A); Medical Research Council UK (MR/J004553/1 and MR/T002735/1); AKK was a Frankenburg Fight for Sight UK PhD Student. RAP was additionally supported by an unrestricted Alcon Research Institute Young Investigator Award. Publisher Copyright: © 2021 The Authors. Published under the terms of the CC BY NC ND 4.0 license Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors


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.

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