Axonal ensheathment in the nervous system of lamprey : implications for the evolution of myelinating glia

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Weil, Marie-Theres
Heibeck, Saskia
Töpperwien, Mareike
tom Dieck, Susanne
Ruhwedel, Torben
Salditt, Tim
Rodicio, María Celina
Morgan, Jennifer R.
Nave, Klaus-Armin
Möbius, Wiebke
Werner, Hauke B.
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Axon–glia interaction
Electron microscopy
Radial sorting
Schwann cell
In the nervous system, myelination of axons enables rapid impulse conduction and is a specialized function of glial cells. Myelinating glia are the last cell type to emerge in the evolution of vertebrate nervous systems, presumably in ancient jawed vertebrates (gnathostomata) because jawless vertebrates (agnathans) lack myelin. We have hypothesized that, in these unmyelinated species, evolutionary progenitors of myelinating cells must have existed that should still be present in contemporary agnathan species. Here, we used advanced electron microscopic techniques to reveal axon–glia interactions in the sea lamprey Petromyzon marinus. By quantitative assessment of the spinal cord and the peripheral lateral line nerve, we observed a marked maturation-dependent growth of axonal calibers. In peripheral nerves, all axons are ensheathed by glial cells either in bundles or, when larger than the threshold caliber of 3 μm, individually. The ensheathing glia are covered by a basal lamina and express SoxE-transcription factors, features of mammalian Remak-type Schwann cells. In larval lamprey, the ensheathment of peripheral axons leaves gaps that are closed in adults. CNS axons are also covered to a considerable extent by glial processes, which contain a high density of intermediate filaments, glycogen particles, large lipid droplets, and desmosomes, similar to mammalian astrocytes. Indeed, by in situ hybridization, these glial cells express the astrocyte marker Aldh1l1. Specimens were of unknown sex. Our observations imply that radial sorting, ensheathment, and presumably also metabolic support of axons are ancient functions of glial cells that predate the evolutionary emergence of myelin in jawed vertebrates.
© The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Journal of Neuroscience 38 (2018): 6586-6596, doi:10.1523/JNEUROSCI.1034-18.2018.
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Journal of Neuroscience 38 (2018): 6586-6596
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