Abstract
From the results of previous studies in which developing peripheral ganglia from quail embryos were transplanted into younger chicken embryo hosts, we concluded that spinal and cranial sensory ganglia contain dormant precursors with autonomic potentialities. Here we describe the differentiation of these precursors in vitro, from dorsal root and nodose ganglion cell suspensions. Dorsal root ganglia were removed from quail embryos at 9 to 15 days of incubation, dissociated to single cells, and grown in tissue culture. The differentiation of cells with autonomic features was followed by monitoring properties associated with the adrenergic phenotype (absent from quail sensory ganglia during normal embryonic development). Provided that the medium was supplemented with chicken embryo extract, numerous cells displaying tyrosine hydroxylase immunoreactivity could be detected from day 4 onward. They possessed long, multiple processes but appeared morphologically distinct from primary sensory neurons. The catalytic activity of tyrosine hydroxylase and of other enzymes required for catecholamine production was demonstrated in the cultures by glyoxylic acid-induced histofluorescence and by radiochemical measurement of the conversion of exogenous tyrosine to norepinephrine. A large proportion of tyrosine hydroxylase-positive cells were found to incorporate [3H]thymidine before and after differentiating. In contrast, recognizable sensory neurons never exhibited adrenergic properties and did not divide. Qualitatively similar results were obtained with cultures of dissociated nodose ganglia. These findings lend further weight to the assumption that latent autonomic precursors are included in the non-neuronal compartment of sensory ganglia.
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- Ayer-Le Lievre C. S., Le Douarin N. M. The early development of cranial sensory ganglia and the potentialities of their component cells studied in quail-chick chimeras. Dev Biol. 1982 Dec;94(2):291–310. doi: 10.1016/0012-1606(82)90349-9. [DOI] [PubMed] [Google Scholar]
- Berod A., Hartman B. K., Keller A., Joh T. H., Pujol J. F. A new double labeling technique using tyrosine hydroxylase and dopamine-beta-hydroxylase immunohistochemistry: evidence for dopaminergic cells lying in the pons of the beef brain. Brain Res. 1982 May 27;240(2):235–243. doi: 10.1016/0006-8993(82)90219-0. [DOI] [PubMed] [Google Scholar]
- Carr V. M., Simpson S. B., Jr Proliferative and degenerative events in the early development of chick dorsal root ganglia. I. Normal development. J Comp Neurol. 1978 Dec 15;182(4):727–739. doi: 10.1002/cne.901820410. [DOI] [PubMed] [Google Scholar]
- Cohen A. M. Factors directing the expression of sympathetic nerve traits in cells of neural crest origin. J Exp Zool. 1972 Feb;179(2):167–182. doi: 10.1002/jez.1401790204. [DOI] [PubMed] [Google Scholar]
- D'Amico-Martel A. Temporal patterns of neurogenesis in avian cranial sensory and autonomic ganglia. Am J Anat. 1982 Apr;163(4):351–372. doi: 10.1002/aja.1001630407. [DOI] [PubMed] [Google Scholar]
- Dupin E. Cell division in the ciliary ganglion of quail embryos in situ and after back-transplantation into the neural crest migration pathways of chick embryos. Dev Biol. 1984 Oct;105(2):288–299. doi: 10.1016/0012-1606(84)90286-0. [DOI] [PubMed] [Google Scholar]
- Jonakait G. M., Markey K. A., Goldstein M., Black I. B. Transient expression of selected catecholaminergic traits in cranial sensory and dorsal root ganglia of the embryonic rat. Dev Biol. 1984 Jan;101(1):51–60. doi: 10.1016/0012-1606(84)90116-7. [DOI] [PubMed] [Google Scholar]
- Jonakait G. M., Markey K. A., Goldstein M., Dreyfus C. F., Black I. B. Selective expression of high-affinity uptake of catecholamines by transiently catecholaminergic cells of the rat embryo: studies in vivo and in vitro. Dev Biol. 1985 Mar;108(1):6–17. doi: 10.1016/0012-1606(85)90003-x. [DOI] [PubMed] [Google Scholar]
- Katz D. M., Markey K. A., Goldstein M., Black I. B. Expression of catecholaminergic characteristics by primary sensory neurons in the normal adult rat in vivo. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3526–3530. doi: 10.1073/pnas.80.11.3526. [DOI] [PMC free article] [PubMed] [Google Scholar]
- König R. Consecutive demonstration of catecholamines and dopamine-beta-hydroxylase within the same specimen. Histochemistry. 1979 Jul 11;61(3):301–305. doi: 10.1007/BF00508451. [DOI] [PubMed] [Google Scholar]
- Le Douarin N. M., Renaud D., Teillet M. A., Le Douarin G. H. Cholinergic differentiation of presumptive adrenergic neuroblasts in interspecific chimeras after heterotopic transplantations. Proc Natl Acad Sci U S A. 1975 Feb;72(2):728–732. doi: 10.1073/pnas.72.2.728. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Le Douarin N. M., Teillet M. A. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev Biol. 1974 Nov;41(1):162–184. doi: 10.1016/0012-1606(74)90291-7. [DOI] [PubMed] [Google Scholar]
- Le Douarin N. M., Teillet M. A. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol. 1973 Aug;30(1):31–48. [PubMed] [Google Scholar]
- Le Lievre C. S., Schweizer G. G., Ziller C. M., Le Douarin N. M. Restrictions of developmental capabilities in neural crest cell derivatives as tested by in vivo transplantation experiments. Dev Biol. 1980 Jun 15;77(2):362–378. doi: 10.1016/0012-1606(80)90481-9. [DOI] [PubMed] [Google Scholar]
- Norr S. C. In vitro analysis of sympathetic neuron differentiation from chick neural crest cells. Dev Biol. 1973 Sep;34(1):16–38. doi: 10.1016/0012-1606(73)90336-9. [DOI] [PubMed] [Google Scholar]
- Polak J. M., Rost F. W., Pearse A. G. Fluorogenic amine tracing of neural crest derivatives forming the adrenal medulla. Gen Comp Endocrinol. 1971 Feb;16(1):132–136. doi: 10.1016/0016-6480(71)90215-2. [DOI] [PubMed] [Google Scholar]
- Price J., Mudge A. W. A subpopulation of rat dorsal root ganglion neurones is catecholaminergic. Nature. 1983 Jan 20;301(5897):241–243. doi: 10.1038/301241a0. [DOI] [PubMed] [Google Scholar]
- Rohrer H., Sommer I. Simultaneous expression of neuronal and glial properties by chick ciliary ganglion cells during development. J Neurosci. 1983 Aug;3(8):1683–1693. doi: 10.1523/JNEUROSCI.03-08-01683.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothman T. P., Gershon M. D., Holtzer H. The relationship of cell division to the acquisition of adrenergic characteristics by developing sympathetic ganglion cell precursors. Dev Biol. 1978 Aug;65(2):322–341. doi: 10.1016/0012-1606(78)90030-1. [DOI] [PubMed] [Google Scholar]
- Schweizer G., Ayer-Le Lièvre C., Le Douarin N. M. Restrictions of developmental capacities in the dorsal root ganglia during the course of development. Cell Differ. 1983 Nov;13(3):191–200. doi: 10.1016/0045-6039(83)90089-1. [DOI] [PubMed] [Google Scholar]
- Smith J., Fauquet M. Glucocorticoids stimulate adrenergic differentiation in cultures of migrating and premigratory neural crest. J Neurosci. 1984 Aug;4(8):2160–2172. doi: 10.1523/JNEUROSCI.04-08-02160.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Teillet M. A., Le Douarin N. M. Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev Biol. 1983 Jul;98(1):192–211. doi: 10.1016/0012-1606(83)90349-4. [DOI] [PubMed] [Google Scholar]
- Teitelman G., Joh T. H., Grayson L., Park D. H., Reis D. J., Iacovitti L. Cholinergic neurons of the chick ciliary ganglia express adrenergic traits in vivo and in vitro. J Neurosci. 1985 Jan;5(1):29–39. doi: 10.1523/JNEUROSCI.05-01-00029.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xue Z. G., Smith J., Le Douarin N. M. Expression du phénotype adrénergique par des cellules du ganglion rachidien de Caille en culture in vitro. C R Acad Sci III. 1985;300(13):483–488. [PubMed] [Google Scholar]