Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen

Uwe Ernsberger, Lorena Esposito, Sandra Partimo, Katrin Huber, Aylin Franke, John Bixby, Chaya Kalcheim, Klaus Unsicker

Research output: Contribution to journalArticle

44 Citations (Scopus)

Abstract

We have analyzed the distribution of neural crest-derived precursors and the expression of catechol-aminergic and neuronal markers in developing adrenal tissue of chick embryos. Undifferentiated neural crest cells are found in presumptive adrenal regions from embryonic day 3 (E3) onward. An increasing proportion of cells expressing tyrosine hydroxylase (TH) mRNA indicates catecholaminergic differentiation of precursors not only in primary sympathetic ganglia, but also in presumptive adrenal regions. Whereas precursors and differentiating cells show mesenchymal distribution until E5, discrete adrenal anlagen form during E6. Even during E5, catecholaminergic cells with low or undetectable neurofilament M (NF-M) mRNA expression prevail in positions at which adrenal anlagen become distinct during E6. The predominance of TH-positive and NF-M-negative cells is maintained throughout embryogenesis in adrenal tissue. RNA encoding SCG10, a pan-neuronal marker like NF-M, is strongly expressed throughout adrenal anlagen during E6 but is found at reduced levels in chromaffin cells compared with neuronal cells at E15. Two additional neuronal markers, synaptotagmin 1 and neurexin 1, are expressed at low to undetectable levels in developing chromaffin cells throughout embryogenesis. The developmental regulation of neuronal markers shows at least three different patterns among the four mRNAs analyzed. Importantly, there is no generalized downregulation of neuronal markers in developing adrenal anlagen. Thus, our observations question the classical concept of chromaffin differentiation from a common sympathoadrenal progenitor expressing neuronal properties and suggest alternative models with changing instructive signals or separate progenitor populations for sympathetic neuronal and chromaffin endocrine cells.

Original languageEnglish
Pages (from-to)1-13
Number of pages13
JournalCell and Tissue Research
Volume319
Issue number1
DOIs
StatePublished - Jan 1 2005

Fingerprint

Chromaffin Cells
Tyrosine 3-Monooxygenase
Intermediate Filaments
Messenger RNA
Synaptotagmin I
Cells
Tissue
Neural Crest
Embryonic Development
Sympathetic Ganglia
Endocrine Cells
RNA
Chick Embryo
Down-Regulation
Population
catechol

Keywords

  • Adrenal tissue
  • Catecholaminergic differentiation
  • Chick
  • Chromaffin endocrine cells
  • Development
  • Neuronal markers
  • Sympathetic neuronal cells
  • Sympathoadrenal progenitor

ASJC Scopus subject areas

  • Anatomy
  • Clinical Biochemistry
  • Cell Biology

Cite this

Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen. / Ernsberger, Uwe; Esposito, Lorena; Partimo, Sandra; Huber, Katrin; Franke, Aylin; Bixby, John; Kalcheim, Chaya; Unsicker, Klaus.

In: Cell and Tissue Research, Vol. 319, No. 1, 01.01.2005, p. 1-13.

Research output: Contribution to journalArticle

Ernsberger, Uwe ; Esposito, Lorena ; Partimo, Sandra ; Huber, Katrin ; Franke, Aylin ; Bixby, John ; Kalcheim, Chaya ; Unsicker, Klaus. / Expression of neuronal markers suggests heterogeneity of chick sympathoadrenal cells prior to invasion of the adrenal anlagen. In: Cell and Tissue Research. 2005 ; Vol. 319, No. 1. pp. 1-13.
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AB - We have analyzed the distribution of neural crest-derived precursors and the expression of catechol-aminergic and neuronal markers in developing adrenal tissue of chick embryos. Undifferentiated neural crest cells are found in presumptive adrenal regions from embryonic day 3 (E3) onward. An increasing proportion of cells expressing tyrosine hydroxylase (TH) mRNA indicates catecholaminergic differentiation of precursors not only in primary sympathetic ganglia, but also in presumptive adrenal regions. Whereas precursors and differentiating cells show mesenchymal distribution until E5, discrete adrenal anlagen form during E6. Even during E5, catecholaminergic cells with low or undetectable neurofilament M (NF-M) mRNA expression prevail in positions at which adrenal anlagen become distinct during E6. The predominance of TH-positive and NF-M-negative cells is maintained throughout embryogenesis in adrenal tissue. RNA encoding SCG10, a pan-neuronal marker like NF-M, is strongly expressed throughout adrenal anlagen during E6 but is found at reduced levels in chromaffin cells compared with neuronal cells at E15. Two additional neuronal markers, synaptotagmin 1 and neurexin 1, are expressed at low to undetectable levels in developing chromaffin cells throughout embryogenesis. The developmental regulation of neuronal markers shows at least three different patterns among the four mRNAs analyzed. Importantly, there is no generalized downregulation of neuronal markers in developing adrenal anlagen. Thus, our observations question the classical concept of chromaffin differentiation from a common sympathoadrenal progenitor expressing neuronal properties and suggest alternative models with changing instructive signals or separate progenitor populations for sympathetic neuronal and chromaffin endocrine cells.

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