Formation of the dorsal root ganglia in the avian embryo: Segmental origin and migratory behavior of neural crest progenitor cells

Marie Aimée Teillet*, Chaya Kalcheim, Nicole M. Le Douarin

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

213 Scopus citations

Abstract

The segmental origin and migratory pattern of neural crest cells at the trunk level of avian embryos was studied, with special emphasis on the formation of the dorsal root ganglia (DRG) which organize in the anterior half of each somite. Neural crest cells were visualized using the quail-chick marker and HNK-1 immunofluorescence. The migratory process turned out to be closely correlated with somitic development: when the somites are epithelial in structure few labeled cells were found in a dorsolateral position on the neural tube, uniformly distributed along the craniocaudal axis. Following somitic dissociation into dermomyotome and sclerotome labeled cells follow defined migratory pathways restricted to each anterior somitic half. In contrast, opposite the posterior half of the somites, cells remain grouped in a dorsolateral position on the neural tube. The fate of crest cells originating at the level of the posterior somitic half was investigated by grafting into chick hosts short segments of quail neural primordium, which ended at mid-somitic or at intersomitic levels. It was found that neural crest cells arising opposite the posterior somitic half participate in the formation of the DRG and Schwann cells lining the dorsal and ventral root fibers of the same somitic level as well as of the subsequent one, whereas those cells originating from levels facing the anterior half of a somite participate in the formation of the corresponding DRG. Moreover, crest cells from both segmental halves segregate within each ganglion in a distinct topographical arrangement which reflects their segmental origin on the neural primordium. Labeled cells which relocate from posterior into anterior somitic regions migrate longitudinally along the neural tube. Longitudinal migration of neural crest cells was first observed when the somites are epithelial in structure and is completed after the disappearance of the last cells from the posterior somitic region at a stage corresponding to the organogenesis of the DRG.

Original languageAmerican English
Pages (from-to)329-347
Number of pages19
JournalDevelopmental Biology
Volume120
Issue number2
DOIs
StatePublished - Apr 1987
Externally publishedYes

Bibliographical note

Funding Information:
We are grateful to Dr. Jack Diamond and Dr. Julian Smith for critical comments on the manuscript. We thank Monique Le Thierry and Ber-nadette Schuler for excellent technical assistance, Stephane Ouzounoff and Sophie Tissot for contributing to the illustrations of this article; and Evelyne Bourson and Anne Le Moue1 for the preparation of the typescript. This work was supported by the Centre National de la Recherche Scientifique and by grants from the Institut National de la Sante et de la Recherche Medicale, the Minis&e de la Recherche et de l’Industrie, the Fondation pour la Recherche Medicale Francaise et the Ligue Francaise contre le Cancer, and by a Basic Research Grant l-866 from March of Dimes Birth Defect Foundation. Chaya Kalcheim has a postdoctoral fellowship from EMBO (European Molecular Biology Organization).

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