Nanotube-like processes facilitate material transfer between photoreceptors

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

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

34 Citations (Scopus)

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.

Original languageEnglish
Article numbere53732
JournalEMBO Reports
Volume22
Issue number11
DOIs
Publication statusPublished - 4 Nov 2021

Keywords

  • extracellular vesicle
  • intercellular communication
  • material transfer
  • photoreceptor transplantation
  • tunnelling nanotube

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