Abstract
Low remyelination efficiency after spinal cord injury (SCI) is a major restraint to successful axonal and functional regeneration in mammals. In contrast, adult zebrafish can: (i) regenerate oligodendrocytes and myelin sheaths within 2 weeks post lesion; (ii) re-grow axonal projections across the lesion site and (iii) recover locomotor function within 6 weeks after spinal cord transection. However, little is known about the intrinsic properties of oligodendrocyte progenitor cells (OPCs), the remyelinating cells of the central nervous system (CNS). Here, we demonstrate that purified OPCs from the adult zebrafish spinal cord are electrically active. They functionally express voltage-gated K+ and Na+ channels, glutamate receptors and exhibit depolarizing, tetrodotoxin (TTX)-sensitive spikes, as previously seen in rodent and human OPCs. Furthermore, we show that the percentage of zebrafish OPCs exhibiting depolarizing spikes and Nav-mediated currents is lower as compared to rodent white matter OPCs, where these membrane characteristics have been shown to underlie OPC injury susceptibility. These findings imply that adult zebrafish OPCs resemble electrical properties found in mammals and represent a relevant cell type towards understanding the biology of the primary cells targeted in remyelination therapies for non-regenerative species. The in vitro platform introduced in this study could be used in the future to: (i) elucidate how membrane characteristics of zebrafish OPCs change upon injury and (ii) identify potential signaling components underlying OPC injury recognition.
Highlights
Oligodendrocyte progenitor cells (OPCs) give rise to myelinating oligodendrocytes that insulate, support and maintain the impulse-carrying axon, thereby contributing to proper functioning of the central nervous system (CNS)
We set out to examine the expression of cell-type specific ion channels in OPCs from the adult zebrafish spinal cord
We used an RNA sequencing dataset previously published from our laboratory, in which the gene expression patterns of OPCs and oligodendrocytes from the adult zebrafish spinal cord were compared (Kroehne et al, 2017)
Summary
Oligodendrocyte progenitor cells (OPCs) give rise to myelinating oligodendrocytes that insulate, support and maintain the impulse-carrying axon, thereby contributing to proper functioning of the central nervous system (CNS). In 2000, in a pivotal study on cells of the oligodendroglial-lineage, using patchclamp recordings on rat hippocampal slices, Bergles et al (2000) showed that stimulation of excitatory axons in both young and adult hippocampus induces glutamate-mediated inward currents in OPCs that form synaptic junctions with vesicle-filled axonal terminals. The existence of such an active signaling pathway between neurons and OPCs indicated for the first time that these cells are able to sense and respond to glutamatergic input and suggested a prominent role for these cells, both in the developing and the adult mammalian CNS. Given the importance of glutamatergic signaling and the glutamatemediated damage in cases on injury in the CNS, these studies provided a new context of potential additional neuromodulatory roles of OPCs
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