Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro

J. W. Mandell, P. R. MacLeish, E. Townes-Anderson

Research output: Contribution to journalArticlepeer-review

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Abstract

To assess the regenerative capability of the photoreceptor synapse, we have isolated and cultured photoreceptors from the mature salamander retina. Both rod and cone photoreceptors were able to regenerate processes within 3 d of plating. Cells extended numerous actin-containing filopodia as well as a few neuritic processes. The neurites contained microtubules and formed synaptic vesicle-filled varicosities, as shown by immunostaining for tubulin and synaptic vesicle proteins and by electron microscopy. Furthermore, regenerated varicosities were capable of depolarization-induced vesicle labeling, suggesting that they can recycle synaptic vesicles and release neurotransmitter by synaptic vesicle exocytosis. Differences were observed between rod and cone cell synaptic regeneration in vitro, which resembled structural differences between their synaptic terminals in situ rod cells formed multiple synaptic vesicle-filled varicosities along neurites at a distance from the soma, whereas cone cells tended to accumulate synaptic vesicles within the soma. The regeneration of neurites and synaptic vesicle- filled varicosities was abolished by microtubule depolymerizing agents, suggesting a role for microtubule-based vesicle transport in the formation of varicosities. Finally, process outgrowth and varicosity formation were independent of cell-cell contact and, indeed, proceeded in the complete absence of other cells. These findings suggest not only that differentiated photoreceptors are capable of synaptic renewal but that the regeneration of presynaptic-like terminals is an intrinsic ability of rod and cone cells.

Original languageEnglish (US)
Pages (from-to)3533-3548
Number of pages16
JournalJournal of Neuroscience
Volume13
Issue number8
DOIs
StatePublished - 1993

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Keywords

  • neurite outgrowth
  • photoreceptor
  • regeneration
  • rod and cone cells
  • synapse
  • synaptic plasticity
  • synaptic vesicles

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