Journal
GLIA
Volume 61, Issue 8, Pages 1364-1377Publisher
WILEY
DOI: 10.1002/glia.22520
Keywords
myelin evolution; oligodendrocyte; Schwann cell; phosphoinositide; zebrafish; cartilaginous fish; teleost fish
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Funding
- Deutsche Forschungsgemeinschaft [DFG WE 2720/2-1]
- European Commission (EU-Health FP7-LeukoTreat)
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Rapid nerve conduction in jawed vertebrates is facilitated by the myelination of axons, which evolved in ancient cartilaginous fish. We aim to understand the coevolution of myelin and the major myelin proteins. We found that myelin basic protein (MBP) derived from living cartilaginous fish (sharks and rays) associated with the plasma membrane of glial cells similar to the phosphatidylinositol (4,5)-bisphosphate (PIP2)-binding marker PH-PLC1, and that ionomycin-induced PIP2-hydrolysis led to its cellular redistribution. We identified two paralogous mbp genes in multiple teleost species, consistent with a genome duplication at the root of the teleost clade. Zebrafish mbpb is organized in a complex transcription unit together with the unrelated gene-of-the-oligodendrocyte-lineage (golli) while mbpa does not encode GOLLI. Moreover, the embryonic expression of mbpa and mbpb differed, indicating functional specialization after duplication. However, both mbpa and mbpb-mRNAs were detected in mature oligodendrocytes and Schwann cells, MBPa and MBPb were mass spectrometrically identified in zebrafish myelin, both associated with the plasma membrane via PIP2, and the ratio of nonsynonymous to synonymous nucleotide-substitution rates (K-a/K-s) was low. Together, this indicates selective pressure to conserve many aspects of the cellular expression and function of MBP across vertebrate species. We propose that the PIP2-binding function of MBP is evolutionarily old and that its emergence in ancient gnathostomata provided glial cells with the competence to myelinate. GLIA 2013;61:1364-1377
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