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Nociceptive sensory neurons derive from contralaterally migrating, fate-restricted neural crest cells

Nature Neuroscience volume 10, pages 1287–1293 (2007)Cite this article

Abstract

Neural crest cells (NCCs) are a transient population of multipotent progenitors that give rise to numerous cell types in the embryo. An unresolved issue is the degree to which the fate of NCCs is specified prior to their emigration from the neural tube. In chick embryos, we identified a subpopulation of NCCs that, upon delamination, crossed the dorsal midline to colonize spatially discrete regions of the contralateral dorsal root ganglia (DRG), where they later gave rise to nearly half of the nociceptor sensory neuron population. Our data indicate that before emigration, this NCC subset is phenotypically distinct, with an intrinsic lineage potential that differs from its temporally synchronized, but ipsilaterally migrating, cohort. These findings not only identify a major source of progenitor cells for the pain- and temperature-sensing afferents, but also reveal a previously unknown migratory pathway for sensory-fated NCCs that requires the capacity to cross the embryonic midline.

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Figure 1: NCCs colonize discrete regions of the contralateral DRG.
Figure 2: Late-wave NCCs cross the dorsal midline and localize to discrete regions of the contralateral DRG.
Figure 3: Late-wave NCCs comprise two subsets.
Figure 4: Contralaterally migrating, late-wave NCCs give rise to nociceptive neurons.
Figure 5: Neural tube and DRG morphology in trunk neural tube–separated embryos.

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Acknowledgements

We thank M. Wegner for his kind gift of the Sox10 antibody, R. Bradley for providing us with the CS2-Myc plasmid and P. Kulesa for critical reading of the manuscript. This work was supported by the National Institutes of Health, National Institute of Neurological Disorders and Stroke R01 35714. (F.L.) and NRSA 7055571 (L.G.).

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Authors and Affiliations

  1. Department of Cell Biology and Neuroscience, Montana State University, Leon Johnson Hall, Rm 512, Bozeman, 59717, Montana, USA

    Lynn George, Marta Chaverra, Valerie Todd & Frances Lefcort

  2. Beckman Imaging Center, California Institute of Technology, MC 139-74, Pasadena, 91125, California, USA

    Rusty Lansford

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  1. Lynn George
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Contributions

L.G. conducted all experiments, imaging and data analyses. L.G. and F.L. supervised the project and wrote the manuscript. M.C. and V.T. assisted with injections, cryosectioning and immunocytochemistry. R.L. constructed the GFP retrovirus and edited the manuscript.

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Correspondence to Frances Lefcort.

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George, L., Chaverra, M., Todd, V. et al. Nociceptive sensory neurons derive from contralaterally migrating, fate-restricted neural crest cells. Nat Neurosci 10, 1287–1293 (2007). https://doi.org/10.1038/nn1962

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