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Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS

Abstract

Boundary cap (BC) cells are neural crest derivatives that form clusters at the surface of the neural tube, at entry and exit points of peripheral nerve roots. Using various knock-in alleles of the mouse gene Egr2 (also known as Krox20), the expression of which, in trunk regions, is initially restricted to BC cells, we were able to trace BC cell progeny during development and analyze their fate. Trunk BC-derived cells migrated along peripheral axons and colonized spinal nerve roots and dorsal root ganglia (DRG). All Schwann cell precursors occupying the dorsal roots were derived from BC cells. In the DRG, BC-derived cells were the progenitors of both neurons, mainly nociceptive afferents, and satellite cells. These data indicate that BC cells constitute a source of peripheral nervous system (PNS) components that, after the major neural crest ventrolateral migratory stream, feeds a secondary wave of migration to the PNS.

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Figure 1: Comparison of reporter expression patterns along the nerve roots at E12.5.
Figure 2: Fate tracing of BC cells.
Figure 3: Dorsal root glial cells are derived from the BC.
Figure 4: Analysis of BC-derived cells in embryonic DRG.
Figure 5: Analysis of BC-derived cells in the adult DRG.
Figure 6: Characterization of subtypes of BC-derived sensory neurons in the adult DRG.
Figure 7: Absence of peripheral migration of neuroepithelial cells.
Figure 8: Analysis of DRG development after BC cell ablation.

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Acknowledgements

We are grateful to P. Soriano, F. Costantini and Y. Lallemand for the R26R, R26R-EYFP and PGK-Crem mouse lines, respectively. We thank A. Chédotal, C. Goridis and F. Guillemot for critical reading of the manuscript. This work was supported by the Institut National de la Santé Et de la Recherche Médicale and by grants from the Ministère de l'Education Nationale et de la Recherche Technologique, the European Community, Association pour la Recherche sur le Cancer (ARC), Association Française contre les Myopathies (AFM) (P.C.) and the Wellcome Trust (J.C.).

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Correspondence to Patrick Charnay.

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Maro, G., Vermeren, M., Voiculescu, O. et al. Neural crest boundary cap cells constitute a source of neuronal and glial cells of the PNS. Nat Neurosci 7, 930–938 (2004). https://doi.org/10.1038/nn1299

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