Requirement of a neural tube signal for the differentiation of neural crest cells into dorsal root ganglia

Chaya Kalcheim*, Nicole M. Le Douarin

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

96 Scopus citations

Abstract

The influence of the neural tube on early development of neural crest cells into sensory ganglia was studied in the chick embryo. Silastic membranes were implanted between the neural tube and the somites in 30-somite-stage embryos at the level of somites 21-24, thus separating the early migrated population of neural crest cells from the neural tube. Neural crest cells and peripheral ganglia were visualized by immunofluorescence using the HNK-1 monoclonal antibody and several histochemical techniques. Separation of crest cells from the neural tube caused the selective death of the neural crest cells from which dorsal root ganglia (DRG) would have developed. Complete disappearance of HNK-1 positive cells was evident already 10 hr after silastic implantation, before early differentiating sensory neurons could have reached their peripheral targets. In older embryos, DRG were absent at the level of implantation. In contrast, the development of ventral roots, sympathetic ganglia and adrenal gland was normal, and so was somitic differentiation into cartilage and muscle, while morphogenesis of the vertebrae was perturbed. To overcome the experimentally induced crest cell death, the silastic membranes were impregnated with a 3-day-old embryonic chick neural tube extract. Under these conditions, crest cells which were separated from the tube survived for a period of 30 hr after operation, compared to less than 10 hr in respective controls. The extract of another tissue, the liver, did not protract survival of DRG progenitor cells. Among the cells which survived with neural tube extract, some even succeeded in extending neurites; nevertheless, in absence of normal connections with the central nervous system (CNS) they finally died. Treatment of silastic implanted embryos with nerve growth factor (NGF) did not prevent the experimentally induced crest cell death. These results demonstrate that DRG develop from a population of neural crest cells which depends for its survival and probably for its differentiation upon a signal arising from the CNS, needed as early as the first hours after initiation of migration. Recovery experiments suggest that the subpopulation of crest cells which will develop along the sensory pathway probably depends for its survival and/or differentiation upon a factor contained in the neural tube, which is different from NGF.

Original languageAmerican English
Pages (from-to)451-466
Number of pages16
JournalDevelopmental Biology
Volume116
Issue number2
DOIs
StatePublished - Aug 1986
Externally publishedYes

Bibliographical note

Funding Information:
We are grateful to Dr. Julian Smith, Dr. Marie-Aim&e Teillet, and Dr. Berthe Salzgeber for their critical suggestions. We also thank Mo-nique Le Thierry for efficient technical assistance, Stephane Ouzounoff and Sophie Tissot for contributing to the illustrations of this article, and Anne Le Moue1 and Evelyne Bourson 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, and the Ligue Franqaise 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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